Hyphochytriomycota and Oomycota

Beakes, Gordon W.; Thines, Marco

doi:10.1007/978-3-319-28149-0_26

Gordon W. Beakes⁴ &
Marco Thines⁵

5861 Accesses
37 Citations

Abstract

The anteriorally uniflagellate Hyphochytriomycota and biflagellate Oomycota are in the Kingdom Straminipila (commonly referred to as stramenopiles) which are part of the SAR superkingdom. Both appear to be basal to the large assemblage of golden-brown algae, the Ochrophyta. Both feature osmotrophic nutrition and have traditionally been considered as zoosporic “fungi,” but are unrelated to organisms in the monophyletic kingdom Mycota. The Hyphochytriomycota is a small group encompassing around half a dozen genera, which have simple nonmycelial, holocarpic thalli, traditionally encompassing three families: the endobiotic Anisolpidiaceae, the polycentric Hyphochytriaceae, and the monocentric Rhizidiomycetaceae. Recently the former have been shown to be placed among the early diverging Oomycota, leaving just the latter two families in the monophyletic Hyphochytriomycota clade. Hyphochytriomycota are widespread in occurrence, and most are saprotrophs or parasites, infecting the resting spores of Oomycota and Glomeromycota. In contrast, the Oomycota are a large and diverse assemblage, consisting of two major (class level) clades, the Saprolegniomycetes and Peronosporomycetes, and several early diverging classes most of which are simple holocarpic organisms that lack mycelial organisation. Many of these early-diverging clades are as yet poorly resolved because of sparse taxon sampling. The early-diverging orders include the Eurychasmales and Olpidiopsidales, both of which are marine seaweed parasites, the nematode infecting Haptoglossales and crustacean infecting Haliphthorales. The Saprolegniomycetes mostly have fungal-like mycelial thalli and include the orders Atkinsiellales s.lat., Leptomitales, and Saprolegniales, which are mostly saprophytes or parasites of invertebrates and, occasionally, vertebrates such as fish and amphibians. A few species in the Saprolegniales are root infecting parasites of plants. The Peronosporomycetes are the second major fungal-like class, and include the largely saprotrophic Rhipidiales, the facultively parasitic Pythiales s.lat., which can infect both animals and plants and the predominantly plant pathogenic Albuginales and Peronosporales sensu lato. Indeed, the Oomycota are significant parasites of both animals and plants, impacting both natural ecosystems and causing significant economic losses in both aquacultural and agricultural systems. The molecular systematics of the Oomycota is still in a state of flux, and in this account a relatively conservative approach has been taken. It is apparent that most of the early-diverging genera are almost exclusively marine and that the Peronosporales represents the main terrestrial and plant pathogenic lineage. Most early-diverging genera lack the oogamous sexual reproduction that characterizes this group and suggests that the oogenesis evolved around the time of emmergence from the sea to the land and freshwater ecosystems. It is also clear that obligate biotrophy in the white blister rusts (Albuginales) and downy mildews (Peronosporales s.str.) has evolved independently.

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Hyphochytriomycota and Oomycota

Chytridiomycota

3 Systematics of the Straminipila: Labyrinthulomycota, Hyphochytriomycota, and Oomycota

Keywords

Summary Classification

●Hyphochytriomycota
●●Hyphochytriomycetes
●●●Hyphochytriales
●●●●Hyphochytriaceae (Canteriomyces, Cystochytrium, Hyphochytrium)
●●●●Rhizidiomycetaceae (Latrostium, Reesia, Rhizidiomyces)
●Oomycota
●●Basal Class(es) incertae sedis
●●●Eurychasmales
●●●●Eurychasmaceae (Eurychasma)
●●●Haptoglossales
●●●●Haptoglossaceae (~Haptoglossa)
●●●~Olpidiopsidales
●●●●Anisolpidiaceae (Anisolpidium)
●●●●~Olpidiopsidiaceae (~Olpidiopsis)
●●● “Haliphthorales”
●●●●Haliphthoraceae ( Halocrusticida [syn. Halodaphnia], ~Haliphthoros, Halioticida)
●●●Incertae sedis
●●●●Pontismataceae ^a (Pontisma ^a , Petersenia ^a)
●●●●Sirolpidaceae ^a (Sirolpidium ^a)
●●●●Ectrogellaceae ^a (Ectrogella)
●●Saprolegniomycetes
●●● “Atkinsiellales” s. lat.
●●●● “Atkinsiellaceae” (Atkinsiella)
●●●●Crypticolaceae ( Crypticola)
●●●●Lagenismataceae (Lagenisma)
●●●●Incertae sedis (~Chlamydomyzium, Cornumyces)
●●●Leptomitales
●●●●Leptomitaceae (Apodachlya, Apodachyella ^a , Blastulidium, Leptomitus)
●●●● Ducellieriaceae ^a (Ducellieria ^a)
●●●Saprolegniales
●●●●Verrucalvaceae (e.g., ~Aphanomyces, Pachymetra ^a , Plectospira, Sommerstorffia Verrucalvus)
●●●●Saprolegniaceae s. lat. (e.g., ~Achlya, Dictyuchus, ~Leptolegnia, ~Saprolegnia, Thraustotheca)
●●Peronosporomycetes
●●●Rhipidiales
●●●●Rhipidiaceae (e.g., Araiospora ^a , Rhipidium ^a, Sapromyces)
●●● “Paralagenidiales” ^b
●●●● “Paralegenidiaceae” ^b (Paralagenidium)
●●●Albuginales
●●●●Albuginaceae (Albugo, Pustula, Wilsoniana)
●●●Peronosporales s. lat.
●●●●Salisapiliaceae ^c (Salisapilia)
●●●●Pythiaceae ^d s. lat. (e.g., Lagena, ~Lagenidium, ~Myzocytiopsis, Pythiogeton, ~Pythium s.l.)
●●●●Peronosporaceae ^e s. lat. (e.g., Bremia, Halophytophthora, Peronosclerospora, ~Phytophthora, Phytopythium, Plasmopara, Peronospora, Pseudoperonospora, Sclerospora)
Where s. lat. is used after a name, there are significant subclades which suggests this taxon will require splitting, although at present the low statistical support, or incomplete taxon sampling means it cannot be done with confidence.
Where names are placed between “ ” means names have not been formally published.
~Before the name means this Order, Family or genus appears to be para- or polyphyletic and will require taxonomic revision.
^aIndicates Family or species has not been sequenced, so taxonomic position not confirmed by molecular data.
^bRecent multigene trees, suggest this clade may merit a new order and family rank (Paralagenidiales, Paralagenidiaceae) (Spies et al. 2016).
^cThis family’s Order placement still not fully resolved.
^dRecent multigene trees, suggest this clade may merit order rank (Pythiales), but may also require further splitting (Spies et al. 2016).
^eRecent multigene trees, suggest this clade may merit order rank as Peronosporales s. str. (Spies et al. 2016).

Introduction

General Characteristics

Historically, the zoosporic fungi studied by mycologists encompassed chytrids, hyphochytrids, labyrinthulids, thraustochytrids, oomycetes, and plasmodiophorids. All generally had walled thalli that fed by osmotrophic absorption, although many had small holocarpic thalli rather than a typical mycelium. These organisms are a polyphyletic assemblage with only the Chytridiomycota now included in the kingdom Fungi (Fig. 1a; Adl et al. 2012). The Plasmodiophorids are now placed in the Cercozoa, a sister clade to Rhizaria (Heuhauser et al. 2010), which together with all other biflagellate fungal-like groups fall within the recently defined “SAR” (Straminipila, Alveolata, Rhizaria) superkingdom (Fig. 1a; Burki et al. 2007, 2008; Burki and Keeling 2014). Molecular studies confirm that both the anteriorly uniflagellate Hyphochytriomycota and the biflagellate Oomycota (Fig. 1b; Tsui et al. 2009; Van der Auwera et al. 1995) are part of the same lineage as the chlorophyll c containing Ochrophyta (Cavalier-Smith and Chao 2006), which together form the sister clade to the Labyrinthulomycota and Opalinids (Tsui et al. 2009). Dick (2001) placed all of these mastigonate fungal-like groups in his revised Kingdom Straminipila, while Cavalier-Smith and Chao (2006) placed the Hyphochytriomycota and Oomycota in the phylum Pseudofungi, together with a number of protists, including the bacteriotrophic flagellate Developayella (Leipe et al. 1994) and the parasitoid Pirsonia (Kühn et al. 2004).

Members of the Hyphochytriomycota are characterized by their small holocarpic, chytrid-like thalli and zoospores with a single, anteriorly-directed flagellum (Figs. 2a and 7a). At the end of a motile period, the zoospores encyst, germinate, and grow to form simple epi- or endobiontic chytrid-like thalli (Fig. 2a–e). Hyphochytriomycota is a small phylum/subphylum consisting of a single order (Hyphochytriales) containing only four or five described genera encompassing around two dozen species. These were grouped by Karling (1942, 1977) into three families: the Anisolpidiaceae, Rhizidiomycetaceae, and Hyphochytriaceae. Molecular sequencing studies of Hyphochytrium catenoides (Van der Auwera et al. 1995) and Rhizidomyces inflatus (Hausner et al. 2000) confirmed that the Hyphochytriomycota form a well-defined clade sister to the Oomycota (Fig. 1b). However, recent sequence data for the marine phaeophyte parasite Anisolpidium ectocarpi have revealed that the Anisolpidiaceae fall within the basal Oomycota, close to Olpidiopsis spp. (Gachon et al. 2015), and thus, are excluded from the Hyphochytriomycota (Table 1).

Table 1 A provisional taxonomic framework for the Hyphochytiomycota and Oomycota based on molecular data

Full size table

In contrast, the Oomycota is a large and diverse phylum/subphylum containing mostly fungal-like organisms (Fig. 2q, r–u; Money 1998; Richards et al. 2006). There are around 1500 or more species grouped into about a 100 genera, the majority of which, however, contain fewer than five species (Table 1; Dick 2001). They typically produce biflagellate zoospores (Fig. 7b–e) and many saprolegniomycete genera produce two generations of zoospores (diplanetic; Fig. 7b, d) or aplanospores and zoospores. The anterior flagellum is mastigonate (Fig. 7e), while the posterior flagellum is smooth with a terminal acroneme (Fig. 7c; Vlk 1939; Manton et al. 1951; Fig. 2). Characteristics that separate Oomycota from true Fungi include having a diploid rather than haploid vegetative thallus (Win-Tin and Dick 1975), cell wall microfibrils composed of cellulose and glucans rather than chitin (Bartnick-Garcia 1970), and a different biochemical pathway for lysine biosynthesis (Vogel 1960). In addition, they store β1–3 mycolaminarins rather than glycogen as their main carbohydrate reserve (Wang and Bartnicki-Garcia 1974). Molecular phylogeny based on ribosomal subunit genes confirmed that the Oomycota share the same common ancestor as the Ochrophyte algae (Fig. 1b: Adl et al. 2012; Cavalier-Smith and Chao 2006; Förster et al. 1990; Gunderson et al. 1987; Leipe et al. 1994; Rilsberg et al. 2009).

Occurrence

The Hyphochytriomycota are found in both soil and water in freshwater, marine, and terrestrial environments and are cosmopolitan in distribution (Fuller 1990, 2001; Gleason et al. 2009). There are both saprotrophs and low-impact parasites, particularly of other chromistans (Oomycota and Phaeophyta) and possibly of crustacea. Although relatively small numbers of species have been described, environmental sequencing from both marine (Diéz et al. 2001; Massana and Pedró-Alió 2008; Massana et al. 2002, 2004, 2006) and freshwater (Richards et al. 2012) environments has revealed many unknowns that fall within the hyphochytrid clade, suggesting that as a group they are both more diverse and widespread than generally appreciated. Hyphochytrid cultures are not widely available although both H. catenoides and R. inflatus are listed in the American Type Culture Collection (ATCC).

Oomycetes are also ubiquitous in marine, freshwater, and terrestrial ecoystems, where they occur as widespread saprotrophs infesting decaying plant and animal detritus (Dick 1990, 2001; Hulvey et al. 2010; Newell and Fell 1995; Riethmüller and Langer 2004) or as necrotrophic and biotrophic pathogens of a wide range of animals (Fig. 3a–k: Karling 1981; Phillips et al. 2008) and plants (Fig. 4a–v: Constantinescu 1991; Dick 2001; Thines 2014; Voglmayr 2008). Plant pathogenic species (Fig. 4a–v) show the greatest diversity, and recent molecular studies have explored the phylogenetic relationships between these pathogens and their hosts (Choi and Thines 2015; Göker et al. 2007; Thines et al. 2008, 2009a; Voglmayr 2003, 2008). Many oomycete plant pathogens, notably Albugo and Hyaloperonospora infecting Arabidopsis, have provided model systems for exploring the molecular interactions between biotrophic pathogens and their hosts (Jiang and Tyler 2012; Kemen and Jones 2012; Thines and Kamoun 2010; Thines et al. 2009c). The occurrence and diversity of marine oomycetes have been greatly underestimated (Hulvey et al. 2010; Nigrelli and Thines 2013), and many recent studies on marine picoplankton samples have revealed many unknown stramenopiles within the Oomycota clade (Diéz et al. 2001; Massana and Pedró-Alió 2008; Massana et al. 2002, 2004, 2006; Richards et al. 2012).

Culture collection holdings of oomycetes are largely confined to the saprophytic and facultatively parasitic species with the largest collections held in the major culture collections such as the American Type Culture Collection (ATCC), Maryland; the Commonweath Agricultural Bureau International fungal collection (CABI), Egham; the Centraalbureau voor Schimmelcultures (CBS), Baarn, and the National Biological Resource Centre (NBRC), Chiba. Some academic institutions hold specialist collections, mainly of Phytophthora and Pythium isolates, such as the World Oomycete Genetic Resource Collection at the University of California, Riverside; the Department of Agriculture Mycology Culture Collection Ottawa; and a collection of Aphanomyces and fish-pathogenic Saprolegnia isolates in the Oomycete Culture Collection, Real Jardin Botanico (CSIC), Madrid. The Culture Collection for Algae and Protozoa (CCAP) in Oban has recently established a small collection of dual clonal cultures of marine oomycetes on their seaweed hosts (Strittmatter et al. 2013).

Literature and History of Knowledge

While there have been no dedicated monographs on the Hyphochytriomycota, they were included by Karling (1977) in his richly illustrated monograph of the chytrids sensu lato. In this he illustrates over half of the 23 accepted species and gives the important references for their study. Other reviews of this phylum include those by Fuller (1990, 2001), Dick (2001), and Beakes et al. (2014a). The first observations of zoosporic fungi possessing a single anterior flagellum were first made in the late nineteenth century (Zopf 1884), although the hyphochytrids were not formally separated from the posteriorly flagellate chytrids until later (Karling 1939, 1943).

The most recent comprehensive monograph of the Oomycota is the scholarly overview by Dick (2001) which lists much of the extensive taxonomic and general biological literature up to end of the millennium. Two important plant pathogenic genera, Pythium and Phytophthora, have been previously monographed, respectively, by Plaats-Niterink (1981) and Waterhouse (1970). The former is currently being comprehensively updated (previewed by de Cock et al. 2012). Recent literature sources for the plant pathogenic downy mildews can be found in Thines and Choi (2016), Lebeda and Spencer-Phillips (2007), Thines (2014), Thines et al. (2009a, b), and Voglmayr (2008). A review of the updated taxonomy of the Albuginaceae is given in Choi et al. (2006, 2008) and Thines and Voglmayr (2009). The three principal genera in the Saprolegniales (Achlya, Aphanomyces and Saprolegnia) have been monographed, respectively, by Johnson (1956), Scott (1961), and Johnson et al. (2002 updated from Seymour 1970). For other taxa, particularly the holocarpic species, reference should be made to Dick (2001), Karling (1981), and Sparrow (1960).

Detailed accounts of the extensive historical studies on the Oomycota have been given by both Dick (2001) and Johnson et al. (2002) and only highlights will be covered here. During the late eighteenth century, there were a number of reports of what we now recognize to be Saprolegnia infections of fish (reviewed by Hughes 1994). Similarly the first documented plant pathogenic oomycete was by Persoon who described the white blister rust Aecidium candidum, which was subsequently transferred by de Roussel in 1806 to the genus Albugo (Choi et al. 2007), although at that time it was still not recognized as an oomycete (Dick 2001). Much of the early documentation of the Oomycota stems from the pioneering researches of Pringsheim, de Bary, Regel, and Tulasne among others (Dick 2001). The higher oomycete taxa were recognized almost as soon as sufficient species had been described to put them into groups. De Bary separated the “Peronsporei” from the mucoraceous phycomycetes and shortly after proposed the “saprolegnieen” and “peronosporeen” family concepts (de Bary 1881). Albugo was eventually recognized as an oomycete when its sexual stages were described by Léveillé (1847) and subsequently placed in the “peronosporeen group” by de Bary (1881). The first attributable oomycete parasites of aquatic plants, protozoa and invertebrate animals were described by Schenk (1858), Cornu (1872), and Zopf (1884). The first plant pathogenic member of the oomycetes to be described was Albugo candida (Persoon, in Gmelin 1792). By the mid nineteenth century, there had also been descriptions of the first three downy mildew genera: Peronospora (Corda 1837), Bremia (Regel 1843), and Basidiophora (Roze and Cornu 1869). However, it was not until the end of the century that Schröter (1893) placed these plant pathogenic species into their own separate family, the Peronosporaceae.

In the latter half of the twentieth century, the taxonomic synthesis of the Oomycota was forged by three outstanding scholars of zoosporic fungi: Dick (1973a, b; 2001), Karling (1981), and Sparrow (1960, 1976). In the second edition of “Aquatic Phycomycetes,” Sparrow (1960) listed four major oomycete orders, the Saprolegniales, Leptomitales, Lagenidiales, and Peronosporales. In his final synthesis, Sparrow (1976) proposed splitting of the oomycetes into two ‘galaxies’, which Dick (2001) later formalized into the subclasses Saprolegniomycetidae and Peronosporomycetidae and also introduced a new order the Eurychasmales, in which he placed a number of little known marine taxa. He considered this new order to be part of the “saprolegnian galaxy” together with the Leptomitales and Saprolegniales. His “peronosporalean galaxy” included the orders Peronosporales, which encompassed most important plant pathogens, and Lagenidiales, which encompassed most of the holocarpic parasites of invertebrates and algae. Dick had continued to refine the classification of the Oomycota (Dick 1976a, b, 1997, 1998; Dick et al. 1984) culminating in his final synthesis which he outlined in his encyclopaedic treatise, “Straminipilous Fungi” in which he expanded the number of orders to around a dozen (Dick 2001). However, as a result of subsequent molecular studies, a substantial revision of Dick’s (2001) scheme has recently been proposed (Beakes et al. 2014a).

Economic and Practical Importance

No hyphochytrid (i.e., excluding Anisolpidium) is known to cause any economically significant disease of plants or animals. Artemchuk and Zelezinskaya (1969) described a species (Hyphochytrium peniliae) that caused a severe mycosis of a freshwater crawfish, but there have been no subsequent reports of this disease, and Dick (2001) questioned whether this organism was even a hyphochytrid. Both Rhizidiomyces spp. and Hyphochytrium catenoides are known to parasitize oospores of plant pathogenic oomycetes (Ayers and Lumsden 1977; Sneh et al. 1977; Wynn and Epton 1979), and Rhizidiomycopsis stomatosa (Sparrow 1977) infects the resting spores of the endomycorrhizal fungus Gigaspora margarita (Schenck and Nicolson 1977; Sparrow 1977). Hyphochytrids may, therefore, adversely affect populations of both potentially harmful oomycetes and beneficial mycorrhizal fungi in soil ecosystems (Sneh et al. 1977). The closely related parasitoids belonging to the genus Pirsonia infect centric diatoms and bring about a decline in planktonic blooms (Kühn 1997; Schnepf et al. 1990). Members of the genus Anisolpidium infect both freshwater algae (Canter 1950) and filamentous phaeophyte seaweeds (Karling 1943; Küpper and Müller 1999); however, this genus is now thought to be an oomycete (Gachon et al. 2015).

In contrast, the economic importance of the Oomycota is well known. Many are devastating and economically important plant pathogens (Fig. 4a–v), with even threatening natural ecoystems such as the Jarrah forest in Australia (Fig. 4e). In the mid-nineteenth century, de Bary and Berkeley established that the species we now know as Phytophthora infestans (Fig. 4a, b) was the causal agent of the devastating potato blight epidemic responsible for the great Irish famine (Berkeley 1846; de Bary 1876; Yoshida et al. 2013). Other species cause serious losses to wild and farmed fish (Fig. 3i, k) and crustaceans (Fig. 3e, g), and there are a few species that can opportunistically infect mammals, including humans (Bruno et al. 2011; de Grooters et al. 2013; Mendoza 2005; Phillips et al. 2008; Schurko et al. 2004; Van West 2006). Economically important genera include the obligate biotrophic white blister rusts (Albugo; Fig. 4f–l) and the downy mildews (e.g., Bremia, Peronospora, Sclerospora etc.; Fig. 4n–v) and facultatively parasitic genera such as Aphanomyces, Phytophthora (Fig. 4a–e), Pythium and Saprolegnia. White blister rusts (Fig. 4f–l) and downy mildews (Fig. 4n–v) infect plants, the latter often causing stunting (Fig. 4f, q) and may result in significant yield losses to many economically important crop plants (Constantinescu 1991; Thines and Choi 2016; Van Wyk et al. 1995). The graminicolous downy mildews (GDM; Fig. 4n, o) in particular pose a serious threat to agriculture in the semi-arid tropics (Bock et al. 2000; Kenneth 1981; Telle et al. 2012; Vilgoen et al. 1997). Many Phytophthora species cause economically and ecologically devastating dieback diseases of trees and scrubs, such as sudden oak death caused by Phytophthora ramorum (Davidson et al. 2003) and jarrah forest dieback (Fig. 4e) caused by Phytophthora cinnamomii (Newhook and Podger 1972; Podger 1972). Aphanomyces euteiches causes serious economic losses by infecting the roots of leguminous crops such as peas and beans (Gaulin et al. 2007). Comprehensive catalogues of oomycete diseases of crop plants have been given by, among others, Dick (2001) and Constantinescu (1991).

Both Nematophthora, which infects nematode eggs (Dick 2001), and Lagenidium giganteum, which infects mosquito larvae (Kerwin 2007), have been explored as potential biocontrol agents. Marine species such as Atkinsiella, Haliphthoros (Fig. 2l, m), Halodaphnea (Fig. 2j, k), and Salilagenidium spp. can cause serious economic losses to cultured crustaceans (crabs and prawns etc.) in coastal aquaculture systems (Hatai 2012; Hatai et al. 1980). Aphanomyces astaci (Fig. 3e–g), which was introduced to Europe around a century ago on imported signal crayfish (Pacifastacus leniusculus) from north America, now threatens to wipe out the native European white-clawed crayfish (Astacus astacus) which has no innate resistance to this pathogen (Cerenius et al. 1988; Edgerton et al. 2004).

Saprolegnia infections of fish and their eggs have been extensively documented and are responsible for significant losses to salmonids worldwide (Bruno et al. 2011; Van West 2006). Epizotoic ulcerative syndrome (EUS) caused by Aphanomyces invadans (syn A. piscida) is an emerging disease of farmed fish in warmer countries, from the Indian subcontinent eastwards (Johnson et al. 2004; Lilley et al. 1998). Equine phycomycosis is an opportunistic pathogen of mammals caused by Pythium insidiosum (Krajaejum et al. 2011; Schurko et al. 2004), which, although largely affecting domesticated livestock in tropical countries, can cause potentially fatal infections to humans (Mendoza 2005). A newly recognized holocarpic lagenidiaceous species (Paralagenidium karlingii) has recently been shown to be the cause of fatal mycoses in dogs (de Grooters et al. 2013). In contrast to their importance as pathogens, no hyphochytrid or oomycete is known as a source for any economically important product, although, as with other heterokonts, they are able to synthesize valuable fatty acids (Domergue et al. 2005), but have not so far been commercially exploited.

Habitats And Ecology

Hyphochytriomycota, in common with the Chytridiomycota and Oomycota, are likely to be encountered in soil and water samples from any area of the world (Gleason et al. 2009; Thines 2014). Soil samples baited with pollen and boiled grasses commonly yield isolates of Rhizidiomyces (Figs. 2c, 6a–b) and Hyphochytrium (Fig. 2b, d). Gleason et al. (2009) demonstrated that H. catenoides is capable of surviving extreme environmental conditions. Viable colonies were recovered after subjecting dried material to extremes of pH (2.8–11.2), hypersalinity and freezing temperatures. Species belonging to the genera Hyphochytrium, Latrostium, and Rhizidiomyces have all been reported to infect algal thalli (Canter 1950). Hyphochytrium infestans was isolated from the decaying ascocarps of ascomycetous fungi, while both Hyphochytrium and Rhizidiomyces spp. infect oogonia of Saprolegnia and Pythium spp. and the resting spores of endomycorrhizal fungi (Fuller 2001; Schenck and Nicolson 1977; Sparrow 1977).

The Oomycota are likewise ubiquitous in marine, terrestrial, and aquatic ecosystems worldwide. Water moulds in the Saprolegniales have been recovered from almost every freshwater ecosystem but appear most abundant at the margins of lakes and ponds (Dick 1976; Johnson et al. 2002; Willoughby 1962; Wood and Willoughby 1986). In general population levels of saprolegniaceous water molds appear higher in cooler and wetter seasons, often showing peaks in spring and autumn (Ali-Shtayeh et al. 1986; Dick and Ali-Shtayeh 1986). Stagnant water and anaerobic environments also have their own distinctive communities of oomycetes, in which members of the Leptomitales and Rhipidiales (such as Sapromyces, Fig. 2p) predominate, and these fungi are often referred to as sewage fungi (Emerson and Natvig 1981; Riethmüller and Langer 2004). In coastal ecosystems, genera such as Halophytophthora and Salisapilia are now known to play a major role in the initial colonization, degradation and recycling of organic substrates, such as cord grass and mangrove leaves (Hulvey et al. 2010; Nakagiri et al. 1994; Newell and Fell 1995; Nigrelli and Thines 2013). Oomycota also infect a wide range of invertebrate animals such as crustaceans (Fig. 3e–g; Duffey et al. 2015; Hatai et al. 1980, 1992), insects (Frances et al. 1989; Kerwin 2007; Martin 1977), nematodes (Figs. 2f, o; 3a–c; Dick 2001; Glockling and Beakes 2000a; Karling 1981), and rotifers (Fig. 3d; Molloy et al. 2014).

Oomycota play significant roles in terrestrial ecosystems. In soils, saprotrophic or facultatively pathogenic genera such as Aphanomyces, Phytophthora, and Pythium spp. predominate (Ali-Shtayeh et al. 1986; Arcate et al. 2006; Duncan 1990; Gaulin et al. 2007). Many oomycetes are obligate plant pathogens infecting annual or perennial herbs (Fig. 4f, q) and grasses (Fig. 4n). The white blister rusts (Fig. 4f–l) are found almost exclusively on herbaceous angiosperm hosts (Dick 2001; Choi et al. 2008; Constantinescu and Fetehi 2002; Spencer 1981; Spencer and Dick 2001; Thines 2009; Thines and Voglmayr 2009; Volgmayr and Riethmüller 2006; Van Wyk et al. 1995) with genera that appear to be restricted to specific host lineages (e.g., Albugo s.str. to the Rosidae, Albugo s.lat. to the Solanales, Pustula to the Asteridae, and Wilsoniana to the Caryphyllidae; Thines and Voglmayr 2009). Recent molecular phylogenetic studies have revealed downy mildew and white blister rust species that are restricted to a single host species (Choi and Thines 2015; Choi et al. 2007, 2008; García-Blázquez et al. 2008; Göker et al. 2004; Ploch et al. 2010; Thines et al. 2009b; Voglmayr 2003; Voglmayr et al. 2004). In contrast, some downy mildew genera such as Peronospora and Plasmopara have a very wide host ranges (Voglmayr and Constantinescu 2008; Voglmayr et al. 2004). While a few species of downy mildews are known to be parasitic to trees (e.g., Plasmopara cercidis, Pseudoperonospora celtidis), shrubs, and lianae (e.g., Plasmopara viburni, Plasmopara viticola, Plasmopara australis, Pseudoperonospora humuli, Peronospora sparsa), it is the hemibiotrophic genus Phytophthora that is more commonly encountered as pathogens of woody plants (Fig. 4e; Davidson et al. 2003; Newhook and Podger 1972).

Characterization and Recognition

Thallus Organization

Spore germination in monocenric hyphochytrids such as Rhizidiomyces results in the formation of a primary rhizoid from which the basal rhizoidal system develops, while the spore body expands to form the main vegetative thallus (Fig. 2a, c; Karling 1971; Sparrow 1960). In the polycentric Hyphochytrium, a much broader germ tube emerges, into which a nucleus moves and divides, and develops into a rhizomycelium of interconnected thalli (Fig. 2a, b, d; Wells 1982; Karling 1977). Young thalli of Hyphochytrium contain many small vacuoles with electron-dense inclusion bodies (Fig. 2e; Clay et al. 1991). Hyphochytriomyota are characterized by the presence of both chitin and cellulose in their cell walls (Bartnick-Garcia 1970; Clay et al. 1991; Fuller 1960). Immunogold labeling reveals the vegetative thallus walls are predominantly composed of cellulose, while chitin is principally located in the septa and the sporangial discharge tubes and restraining vesicle (Clay et al. 1991).

Many early-diverging Oomycota also have simple endobiotic holocarpic thalli, which directly differentiate into sporangia on maturity (Figs. 5b, c, f; 6a, b). Many holocarpic oomycetes, such as the parasities of algae Ectrogella (Ragukumar 1980), Eurychasma (Sekimoto et al. 2008a), and Olpidiopsis (Sekimoto et al. 2008b), have naked plasmodia stages during the earliest stages of infection (Fig. 5d). Taxa that have more extensive lobed, branched or segmented thalli (Fig. 2j, k, n) include the marine crustacean parasites, such as Atkinsiella (Karling 1981), Haliphthoros, Halodaphnea (Sekimoto et al. 2007), and algal parasites, such as Lagenisma (Schnepf et al. 1977, 1978a, b, c; Thines et al. 2015a) and Petersenia (Molina 1981; Pueschel and van der Meer 1985) as well as terrestrial genera such as Chlamydomyzium (Beakes et al. 2014b; Glockling and Beakes 2006b) and Cornumyces (Inaba and Hariyama 2006). Although none of these species produce typical hyphal-like thalli, most can be cultured on solid artificial media, where they form slow-growing irregular colonies (Glockling and Beakes 2006b; Sekimoto et al. 2007). Most thalli in the Rhipidiales (Fig. 2p) and Leptomitales form more typical fungal-like colonies on solid media, although they still have segmented thalli with regular constrictions. It appears that as in the Hyphochytriomycota, the Oomycota also have the capacity to synthesize chitin or chitin-like analogues, as evidenced by the widespread presence of chitin synthase genes within the phylum (Badreddine et al. 2008). In the Leptomitales, the pores in the constricted regions are plugged with refractile chitin-containing cellulin granules (Huizar and Aronson 1986).

The majority saprolegniomycete and peronosporomycete species have branched filamentous mycelial thalli that grow as fungus-like colonies on agar media (Fig. 2q, r). The hyphal tips contain accumulations of vesicles although they lack a well-defined Spitzenkörper analog found in most Fungi (Bartnicki-Garcia 1996). Hyphae vary in diameter from around 2 μm in genera such as Pythiogeton and Verrucalvus to nearly 150 μm in many genera in the Saprolegniaceae (Dick 2001). Hyphal vacuoles contain soluble β1–3 glucans (mycolaminarins), which are a major storage reserve in the Oomycota (Bartnicki-Garcia and Wang 1983; Wang and Bartnicki-Garcia 1974) as in the Ochrophyta. Most obligate biotrophic plant pathogens produce extensive intercellular hyphae in the infected leaf tissues from which haustoria intrude into the surrounding host cells (Hickey and Coffey 1977, 1978). The hyphae of the relatively early diverging white-blister rusts, such as Albugo, form small stalked globose haustoria (Coffey 1975; Mims and Richardson 2002; Soylu et al. 2003), whereas Phytophthora (Coffey and Wilson 1983) and the downy mildews form generally larger digit-like to globose saccoid haustoria (Göker et al. 2003; Voglmayr et al. 2004).

Sporogenesis

In the Hyphochytriomycota, the expanded thallus is directly converted into simple zoosporangia. The cytoplasm then differentiates into uninucleate and uniflagellate zoospores during the zoosporogenesis phase of development (Karling 1977). In Rhizidiomyces, the sporangial cytoplasm flows into an external vesicle (Fig. 6a) where the completion of zoospore differentiation takes place (Fig. 6b; Clay et al. 1991; Fuller and Jaworksi 1987). In Hyphochytrium , the zoospores form within the sporangium and are released via open discharge tubes (Karling 1977).

Asexual reproductive structures provide many of the morphological characters which have been traditionally used to define genera (Dick 2001; Coker 1923; Johnson et al. 2002; Sparrow 1960), although recent molecular studies have revealed the inherent unreliability of many of these traditional morphological characters (Thines 2006). In early diverging Oomycota genera with plasmodial thalli, the thallus becomes walled prior to spore differentiation (Fig. 5f; Molina 1981; Raghukumar 1980; Schnepf et al. 1978b; Sekimoto et al. 2008a, b). Holocarpic endobiotic species usually form one or more elongate exit tubes (Figs. 2f, 3a, 5g, f, j) to facilitate the release of their spores from their hosts (Glockling and Beakes 2000a; Karling 1981). In species such as Haliphthoros milfordensis, these discharge tubes may be very long and hyphal-like in appearance (Fig. 5j). In Aphanomyces, primary aplanospores differentiate within what appear to be undifferentiated hyphae (Hoch and Mitchell 1972, Johnson et al. 2002). However, most species with eucarpic thalli form septum-delimited sporangia with a characteristic morphology (Fig. 6f–j) that are typically formed terminally (Johnson et al. 2002; Sparrow 1960). In the Saprolegniales, sporangia are delimited by a double-walled septum (Gay and Greenwood 1966), whereas in the Peronosporales they are separated by a callose plug (Fig. 6i, j; Hohl and Hammamoto 1967). There are a significant number of taxa that produce nonmotile primary aplanospores (e.g., Achlya: Fig. 6h; Aphanomyces: Figs. 3f, 6c; Calyptralegnia: Fig. 6d, Eurychasma: Fig. 5c, Protascus: Fig. 7n, and Thraustotheca Fig. 6e). Many downy mildew genera in the Peronosporaceae such as Bremia, Hyaloperonospora (Fig. 4u) and Peronospora (Fig. 4s) form condiosporangia that germinate directly by means of germ tubes.

Zoospores or aplanospores are released (Fig. 6g, h, l) following the dissolution of the apical papillum wall (Beakes 1987; Gay and Greenwood 1966). In the Peronosporales, the papillum usually contains a plug (Fig. 6k, m), which often gives rise to extra-sporangial vesicles into which partially differentiated cytoplasm (Fig. 6m) or fully differentiated zoospores (Fig. 6l) are released (Beakes 1987; Glockling and Beakes 2006b; Lunney and Bland 1976). In the hyphochytrid Rhizidiomyces (Fig. 6a, b; Fuller and Reichle 1965) and some Peronosporomycete genera, such as ~Lagenidium (Gotelli 1974), Myzocytiopsis (Fig. 6m; Glockling and Beakes 2006a), and Pythium (Lunney and Bland 1976), the final stages of zoospore differentiation take place within the extra-sporangial vesicle, outside of the thallus. In other Peronosporomycete genera, such as Phytophthora and Halophytophthora (Fig. 6l), fully motile zoospores form within the sporangium and are also released into a transient restraining vesicle (Hyde et al. 1991a), while in downy mildew species such as Plasmopara spp. and Pseudoperonospora spp., zoospores are directly released from the sporangium (Thines 2006). In most downy mildews, the sporangia are formed on determinate sporangiophores of distinctive branched morphology (Fig. 4s, v). In most leaf-borne plant pathogens , the mature reproductive structures are disseminated by disarticulation (Fig. 4s) and dispersed by wind and rain splash (Dick 2001, Thines 2006). In the white blister rusts, basipetally maturing chains of conidia/sporangia are produced subepidermally by sporogenous hyphae (Fig. 4g, h), remiscent to true rusts, and again disseminated by disarticulation after lysis of the plant epiermis (Fig. 4j; Heller and Thines 2009; Kemen and Jones 2012; Mims and Richardson 2002).

In the genus Saprolegnia, two morphologically distinct types of zoospore are produced, traditionally referred to as primary and secondary zoospores (Beakes 1987; Coker 1923; Holloway and Heath 1977a; Sparrow 1960). Primary zoospores simply serve to disperse the spores from the immediate vicinity of the parent sporangium and are generally weak swimmers. They are usually pip or pear shaped and have apically inserted flagella (Fig. 7b)) which are retracted upon encystment (Holloway and Heath 1977a). The resulting primary cysts (Fig. 7o) typically release the stronger swimming dispersive secondary zoospores (Fig. 7d) which are typically reniform in shape and have laterally inserted flagella (Fig. 7d, g, i) that are shed upon encystment (Holloway and Heath 1977a). This ability to produce two generations of zoospore appears to have been lost in many Saprolegniomycete genera (Beakes et al. 2014a; Johnson et al. 2002), such as where the primary spore initials encyst at the mouth of the exit tube as in Aphanomyces (Fig. 3f, 6c) and Achlya (Fig. 6h) or within the sporangium as in Dictyuchus and Thraustotheca (Fig. 6d).

The ability to produce both primary zoospores (Fig. 7b) and cysts (Fig. 7o) has been entirely lost in Peronosporomycetes, which only form secondary type zoospores and cysts (Fig. 7i, n–r; Beakes 1987; Dick 2001; Hohl and Hammamoto 1967; Lunney and Bland 1976; Sparrow 1960). In the downy mildews, the complete loss of zoospore production has taken place independently in several genera (e.g., Bremia, Hyaloperonospora, Paraperonospora, Peronosclerpospora, and Peronospora; Göker et al. 2007; Thines 2006; Thines et al. 2009a; Voglmayr et al. 2004). The recent finding of a complete absence of genes associated with flagellum formation and function in the genome of Hyaloperonospora indicates that, in some downy mildews at least, this is an irreversible loss (Baxter et al. 2010).

In order to maximize zoospore production, sporangium proliferation frequently occurs throughout the Oomycota following zoospore discharge. Regrowth may take place through the basal septum (internal renewal), or from a lateral branch (cymose renewal) or by outgrowth of the sporangiophore from sites where sporangia were discharged as in some Phytophthora species and the grass parasite Viennotia (Thines et al. 2007; Thines 2009). In the Albuginales, sporangia are produced in basipetal sequence by the sporogenous hyphae as occurs in true rust fungi (Fig. 4g, h; Heller and Thines 2009; Kemen and Jones 2012; Mims and Richardson 2002).

Encysted zoospores in Oomycota (cysts; Fig. 7o–r) are typically spherical, although in some nematode infecting species, such as Protoascus (Fig. 7n), may be elongate and spindle-shaped. They are typically uninucleate and thin walled and contain abundant lipid and vacuolar dense-body/fingerprint vesicles (Fig. 7n–r). Most secondary cysts germinate directly by means of a vegetative germ tube, thus completing the asexual life cycle (Fig. 2s–u). However, the encysted zoospores of the nematode-infecting genus Haptoglossa (Beakes and Glockling 1998, 2000, 2002) germinate to produce specialized infection structures known as gun cells (Fig. 7q; Robb and Barron 1982). These cells contain a needle-like structure within an inverted tube (Beakes and Glocklng 1998, 2000, 2002). Upon contact with a suitable host, the tube everts and the needle ruptures the host cuticle, resulting in the injection of a minute infective sporidium into the body cavity of the nematode (Glockling and Beakes 2000b).

Most Oomycota also produce vegetative resting structures, variously referred to as chlamydospores in the Peronosporomycetes (Hemmes 1983) and gemmae in Saprolegniomycetes (Dick 2001; Johnson et al. 2002). These structures are delimited by similar septa to sporangia but are thicker-walled. They typically contain abundant storage reserves, particularly lipid (Beakes 1994; Hemmes 1983). When environmental conditions become favorable, they either germinate by producing germ tubes or convert into zoosporangia.

Sexual Reproduction

Sexuality has never been documented in the Hyphochytriomycota sensu stricto (i.e., excluding Anisolpidiaceae; Karling 1977), although structures that have been described as resistant sporangia have been reported in Rhizidiomyces spp. and H. catenoides (Karling 1977) which might explain why these species appears to be able to survive extreme environmental conditions (Gleason et al. 2009).

Most early diverging Oomycota (Table 1) are usually stated to lack a sexual stage (Sparrow 1976; Karling 1981). However, as Sparrow (1976) points out it seems improbable that all such species are genuinely asexual and suggested that they must have some form of cryptic (i.e., non oogamous) sexual reproduction. The best documented evidence supporting this comes from Lagenisma coscinodisci, which has recently been established to be an early diverging member of the Saprolegniomycetes closely related to Atkinsiella (Thines et al. 2015a). This species produces zoomeiospores which form cysts that conjugate to form the diploid resting zygote (Schnepf et al. 1977). Recent unpublished observations suggest that this might also be the form of sexual reproduction in Eurychasma, although this has only been observed on certain host seaweeds (Gachon, personal communication). Further support that conjugative, nonoogamous, sexual reproduction is prevalent in early diverging Oomycota also comes from Anisolpidium ectocarpii (Johnson 1957; Karling 1943, 1981). This species has recently been shown to be an early diverging member of the Oomycota closely related to marine Olpidiopsis spp. (Gachon et al. 2015) and reproduces by the fusion of adjacent protoplasts, derived from different cysts (Johnson 1957). Plasmogamy is immediately followed by nuclear fusion (karyogamy). The resulting zygote nucleus divides repeatedly as the cell enlarges and the wall thickens (Johnson 1957). All of these recent observations suggest that oogamy might have evolved at around the time of the Peronosporomycete divergence (Fig. 9a, b) and may even have arisen independently in saprolegniomycete and peronosporomycete lines (Thines et al. 2015a). However, the paraphyletic/polyphyletic genus Olpidiopsis needs further investigation in this respect, as oogenesis has been reported in freshwater species such as Olpidiopsis varians (Martin and Miller 1986c) but not in any of the marine species (Sekimoto et al. 2008b, 2009).

In holocarpic Peronosporomycete species, such as Lagenidium and Myzocytiopsis adjacent thallus segments differentiate into male and female gametangia which have been interpreted as antheridial and oogonial segments, and give rise to a typical oosporic zygote (Dick 1995; Glockling and Beakes 2006a; Karling 1981; Martin and Miller 1986c). In the holocarpic, basal saprolegniomycete genus Chlam ydomyzium thick-walled oospore-like structures are formed, but without the apparent involvement of antheridial segments (Beakes et al. 2014b; Glockling and Beakes 2006b). Unfortunately, no information is available regarding nuclear changes that take place during resting spore formation in this genus to confirm whether this is a genuine sexual process, such as described in Saprolegnia species that lack antheridia (Beakes 1980b).

Oomycota as a group were named after their distinctive oogamous sexual reproduction present in the vast majority of species, involving the production of spherical to ovoid female oogonia, containing one (Fig. 8i) to several (Fig. 8a, f) large eggs (oospheres), and the associated male antheridia (Fig. 8f, i). In the diploid Oomycota gametangial meiosis preceeds gamete formation (Beakes and Gay 1977; Dick and Win-Tin 1973; Howard and Moore 1970). The female oosphere nuclei and male antheridial nuclei are the only haploid stages in the life cycle (Howard and Moore 1970; Beakes 1980b). The diploid state is restored by the fusion of the gamete nuclei, which normally takes place before the oospores (zygotes) have reached maturity (Beakes 1980b; Beakes and Gay 1977; Howard and Moore 1970). The morphology of gametangia (Fig. 8a, f, i) and oospores (Fig. 8g, h, k–p) have been widely used as key taxonomic characters (Dick 1969, 1990, 2001; Sparrow 1960). In the genus Saprolegnia , but also in the Albuginales, species identification is almost entirely dependent upon sexual characters (Choi et al. 2007, 2008; Coker 1923; Johnson et al. 2002; Ploch et al. 2010; Thines et al. 2009c; Voglmayr and Riethmüller 2006). It seems likely that in the Oomycota gametangium differentiation is regulated and coordinated by diffusible steroid hormones (antheridiols and oogoniols), whose functions have been well documented particularly in Achlya bisexualis (McMorris and Barksdale 1967; Raper 1939) and certain Phytophthora spp. (Ko 1988). In contrast to Saprolegniomycetes, several Peronosporomycetes were reported not to be able to synthesise their own sterols and require these as supplements in order to reproduce sexually (Jee and Ko 1997; Kerwin and Washino 1983). The male antheridia typically are formed on either subtending branches (monoclinous; Fig. 8a) or hyphal compartments (hypogynous) or from separate hyphae produced either on the same thallus (diclinous; Fig. 8f) or in the case of heterothallic species from separate thalli (Dick 1972, 1995, 2001). Many Phytophthora species show a unique type of amphigynous antheridium-oogonium association, where the oogonium penetrates the young antheridium which then forms a collar around the base of the oogonium (Fig. 8i; Hemmes and Bartnick-García 1975; Beakes et al. 1998).

In the Saprolegniomycetes, egg (oosphere) differentiation occurs as a result of the fusion of the central tonoplast membrane with the plasma membrane (Fig. 8a) resulting in naked oospheres (Fig. 8b), which within 30 minutes acquire an outer primary oosphere wall (Fig. 8a; Beakes and Gay 1978b). Following fertilization (Fig. 8a, d) thick inner oospore wall layers are accreted below a thin intervening electron-dense layer. In contrast in all Peronosporomycetes, a uninucleate oosphere (Fig. 8e) is cleaved from the cytoplasmic mass, surrounded by an outer periplasmic layer containing supernumerary nuclei (Fig. 8c; Beakes 1981; Hemmes and Bartnicki-Garcia 1975; Stevens 1901), which also contributes to the oospore formation by the the formation of an outer wall of the oospore.

Ultrastructure

Mitosis in the Hyphochytiomycota has only been described at the ultrastructural level in Rhizidiomyces (Barstow et al. 1989). During prophase the centrioles of unequal length divide and migrate to the poles of the nucleus. During metaphase small polar fenestrae (gaps) develop in the nuclear envelope, allowing the spindle microtubules to span the nucleus. By metaphase the chromosomes are grouped equatorially and vesicles appear and fuse with each other on the poleward side of chromosomes (Barstow et al. 1989). At metaphase the nucleolus is located in a pocket to the side of the chromosomes, after which it disperses completely. During anaphase the intranuclear cisternae migrate ahead of the advancing chromosomes. A perinuclear endoplasmic reticulum and microbodies surround dividing nuclei during anaphase and telophase. During telophase, offspring nuclei are formed by the addition of new envelope to existing membranes and the mid-region of the original nucleus is excluded (Barstow et al. 1989).

This contrasts with the completely closed mitosis described in most Oomycota (Beakes 1980c). Mitosis has been documented at the ultrastructural level in Albugo (Khan 1976), Lagenisma (Schnepf et al. 1978a), Olpidiopsis (Martin and Miller 1986a), Phytophthora (Hemmes and Hohl 1973) and Saprolegnia (Beakes 1980b, c; Heath and Greenwood 1970a). In most, the nuclear membrane persists throughout mitosis and an intranuclear spindle forms between pairs of polar or sub-polar centrioles, which are usually oriented at 180° (end to end) to each other. Only in Olpidiopsis varians are small polar fenestrae reported to form during prophase (Martin and Miller 1986a).

The vegetative thallus in both the Hyphochytriomycota and Oomycota is filled with large somatic vacuoles, which contain osmiophilic inclusion bodies of unknown composition that are often associated with the tonoplast membrane (Figs 2e, 5a, h). Nuclei and other cytoplasmic organelles are distributed throughout the peripheral cytoplasm (Fig. 5a, f, h). In both groups mitochondria have prominent tubular cristae (Fig. 5i), which are a characteristic feature of the chromalveolate lineage (Cavalier-Smith and Chao 2006). In vegetative hyphae and young sporangia in the Saprolegniales, the Golgi dictyosomes are associated with mitochondria and an intervening cisternum of endoplasmic reticulum (ER), a feature shared with many diatoms (Beakes 1989).

During sporangium differentiation in both the Saprolegniales and Peronosporales vacuolar dense body/fingerprint vesicles (DBV/FPV) increase (Beakes 1980a, 1994; Gay and Greenwood 1966; Glockling and Beakes 2006a) and their osmiophilic inclusion bodies become associated with lamellate material of regular periodicity (Fig. 6n–q). In Phytophthora phosphorylated glucan derivatives (phospho-mycolaminarin) have been shown to co-localize with isolated FPV (Powell and Bracker 1977). However, no lamellate DBV have been observed in early diverging genera (Beakes and Glockling 2000; Sekimoto 2008; Sekimoto et al. 2008a, b, 2009), which may indicate phosphorylated mycolaminarins are not synthesised by these species, although this needs experimental confirmation.

In most species spore formation involves the division (cleavage) of the multinucleate protoplast into uninucleate spore initials each with a defined complement of organelles. In early diverging genera such as Eurychasma (Sekimoto et al. 2008a), Haliphthoros (Fig. 5i), Haptoglossa (Fig. 5b; Beakes and Glockling 2000), Olpidiopsis (Martin and Miller 1986b; Sekimoto et al. 2008b, 2009) and Petersenia (Molina 1981) there is a tight association mitochondria around nuclei prior to cytoplasmic cleavage. Cytoplasmic cleavage in the Oomycota follows one of two general patterns (Beakes 1994; Dick 2001). The first, usually referred to as centrifugal cleavage (Beakes 1989, 1994) is found in most early diverging genera (Sekimoto 2008) and Saprolegniomycetes (Beakes et al. 2014a). A central vacuole expands delimiting a peripheral layer of uninucleate initials (Fig. 5h) and spore initial formation is effected by the fusion of the tonoplast with the plasma membrane (Gay and Greenwood 1966; Sekimoto et al. 2008b, 2009), as occurs in oosphere differentiation illustrated in Fig. 8a. In most Saprolegniomycetes flagellum formation occurs after the zoospore initials have differentiated (Beakes 1987; Gay and Greenwood 1966; Glockling and Beakes 2006b).

The second pattern, described as centripetal cleavage (Beakes 1994), predominantly occurs in the Peronosporomycetes (and probably Hyphochytriomycota). The uninucleate zoospore initials are delimited by the progressive disposition of a system of narrow Golgi-derived cleavage vesicles/cisternae, occasionally with additional infurrowing of the plasma membrane as occurs in Albugo (Khan 1976, 1977), Phytophthora (Hemmes 1983; Hohl and Hammamoto 1967; Hyde et al. 1991a, b) and Pythium (Lunney and Bland 1976). This leads to the concurrent, rather than sequential, formation of zoospore initials and flagella (Hohl and Hammamoto 1967; Hyde et al. 1991a, b; Lunney and Bland 1976). As a consequence beating flagella can often be observed in differentiating sporangia or extrasporangial vesicles even before the formation of individual zoospores.

Zoospore Ultrastructure

The ultrastructure of motile cells has traditionally been widely used to provide taxonomically and phylogenetically informative characters in protists and is still important in helping to define clades of chytrid fungi (Powell and Letcher 2014). In the Hyphochytriomycota and Oomycota, zoospores are also a rich source of phylogenetically informative characters (reviewed by Beakes 1987, 1989). Hyphochytriomycota zoospore ultrastructure has been documented for both R. apophysatus (Fuller and Reichle 1965) and H. catenoides (Barr and Désaulniers 1989; Cooney et al. 1985; Lange and Olson 1979: see Fig. 7f). In common with other members of the stramenopile lineage (Cavalier-Smith and Chao 2006) there is a helically coiled double transitional helix (TH) located just above the basal plate of the flagellum (Fig. 7f). In the Hyphochytriomycota the anterior flagellum is associated with two microtubular rootlets consisting of single (AR1) and doublet (AR2) type, both of which have rib-like microtubules extending from them, providing a cytoskeletal framework for the zoospore (Fig. 7l; Barr and Désaulniers 1989; Beakes et al. 2014a; Dick 2001). In addition, there is a third doublet rootlet (designated as multistranded root, MS), which originates between the two basal bodies and extends to the spore posterior (Fig. 7l; Barr and Désaulniers 1989).

In the Hyphochytriomycota, the ribosomes in the zoospores are aggregated around the posterior region of the nucleus and are surrounded by a zone of mitochondria (Fig. 7f; Cooney et al. 1985; Fuller 1966; Fuller and Reichle 1965; Lange and Olson 1979). Lipid bodies and microbodies and assorted vesicles, including those containing mastigoneme tubules, are also scattered throughout peripheral zoospore cytoplasm (Fig. 7f). When Hyphochytriomycota zoospores encyst, the axoneme of the flagellum is retracted into the body of the cyst (Fuller and Reichle 1965; Wells 1982). The outer cyst coat is derived from the discharge of structured peripheral vesicles (Fuller 1966) which are similar to the encystment vesicles described in the Oomycota (Beakes 1987, 1989).

The structure and orientation of the four microtubular flagellar rootlets in Oomycota zoospores has been meticulously documented from serial section reconstructions in Saprolegnia (Fig. 7m; Barr and Allan 1985; Barr and Désaulniers 1987, 1989; Holloway and Heath 1977b) and Phytophthora (Barr and Allan 1985; Hardham 1987) and appears broadly similar to other biflagellate stramenopiles (Anderson et al. 1991; Barr 1981). Most Oomycota zoospores have the expected double TH in the flagellum base (Beakes et al. 2014a; Barr 1981; Dick 2001) although in Olpidiopsis saprolegniae it has only a single gyre (Bortnick et al. 1985), and it is apparantly absent in a few species, including the Peronosporomycete Lagena radicola (Barr and Désaulniers 1989). Zoospores contain an array of peripheral vesicles (Fig. 7g–j), which upon encystment are discharged to form both a ventral pad of adhesive and the outermost cyst coat layers (Beakes 1983, 1989, 1994; Gubler and Hardham 1988; Lehnen and Powell 1989). In Saprolegniomycetes, this system includes the larger kinetosome-associated (K-bodies) vesicles (Fig. 7h; Beakes 1989; Holloway and Heath 1977b; Randolph and Powell 1992) which upon encystment discharge to form a ventral pad of adhesive material (Burr and Beakes 1994; Lehnen and Powell 1989). In Peronosporomycetes the homologous vesicles are smaller and generally located along the rim of the ventral zoospore groove rather than immediately adjacent to the kinetosomes (Fig. 7j Gubler et al. 1990), and are often morphologically indistinguishable from the dorsal vesicle fraction. Saprolegniomycete genera also contain a second vesicle fraction, which in Saprolegnia ferax were called bar-bodies (Heath and Greenwood 1970b), although in other genera such as Apodachlya are spherical in profile (Randolph and Powell 1992). Upon discharge the peripheral component of these vesicles give rise to the thin outer electron-dense primary cyst coat (Beakes 1983, 1989; Randolph and Powell 1992). The corresponding vesicles in secondary zoospores of genera such as Dictyuchus and Saprolegnia contain, respectively, conspicuous tapered spines or boathook spines (Beakes 1983; Burr and Beakes 1994; Heath and Greenwood 1970b) that on release decorate the secondary cyst coat (Fig. 3j). In other genera such as Apodachlya, Aphanomyces, and Achlya the equivalent vesicles are spherical or ovoid in shape and have granular contents rather than tubules or spines and form only the thin outer electron-dense layer to the cyst wall (Beakes 1989). Morphologically similar encystment vesicles also occur in the zoospores of many of the early diverging oomycetes, including Eurychasma (Sekimoto et al. 2008a), Lagenisma (Schnepf et al. 1978c), Haliphthoros (Overton et al. 1983; Sekimoto 2008), Haptoglossa (Beakes and Glockling 2000), Olpidiopsis spp. (Sekimoto et al. 2008b, 2009), and Petersenia (Pueschel and van der Meer 1985). In contrast, in Peronosporomycetes, the homologous vesicle fraction are the so-called dorsal small vesicles (dsv), which are often morphologically indisguishable from the ventral vesicle fraction, and upon encystment form a structurally diffuse sticky glycoprotein coat (Gubler and Hardham 1988; Gubler et al. 1990).

Mature Oospore Ultrastructure

Following nuclear transfer and fusion (karyogamy) the fertilized oosphere matures into the thick-walled resting zygote, the oospore (Fig. 8g–p; Beakes 1980a; Beakes and Gay 1978a; Hemmes and Bartnicki-Garcia 1975; Tewari and Skoropad 1977). Following fertilisation a thick electron-dense wall layer is layed down (Fig. 8q–u), to which further wall layers may be added both internally from egg cytoplasm and externally from the periplasm (Fig. 8q–u; reviewed by Beakes 1981). This “epispore” layer appears to represent the transition from oosphere to oospore, and after its formation, the mature eggs are much more recalcitrant to TEM fixation (Fig. 8g, j). The overall organization of the cytoplasmic components in mature oospores was described by Dick (1969) and has proven to be a useful taxonomic character. In all species the oospore protoplasm contains a prominent ooplast vacuole (Dick 1969; Fig. 8g–m) derived from the fusion and expansion of the oosphere DBV system (Beakes 1980a; Beakes and Gay 1978a; Beakes et al. 1986; Hemmes and Bartnicki-Garcia 1975; Howard and Moore 1970). This vacuole is usually surrounded by the peripheral cytoplasm containing oil reserves, which may be organized into many small droplets (in centric, subcentric or plerotic oospores; Fig. 8g, h, j) or these may coalesce into a small number of large droplets (as in the eccentric oospores of Leptomitus; Fig. 8l). In the genus Saprolegnia the mature ooplast vacuole contains small granules which are in constant Brownian motion (granular ooplast; Fig. 8g, k) whereas in the Leptomitales (Fig. 8l; Dick 1969, 1973a) and Peronosporomycete species the ooplast vacuole usually has a uniform refractile appearance (Fig. 8i; Beakes et al. 1986) and appears as a homogenously electron-dense matrix in the transmission electron-microscope (Fig. 8j; Beakes 1981; Beakes et al. 1986).

Oospores are mostly not shed from the oogonium wall which provides an additional protective outer layer to the zygote. It is often thick and multilayered (Beakes and Bartnicki-Garcia 1989; Hemmes and Bartnicki-Garcia 1975) and in many genera can be papillate (e.g in Chlamydomyzium dictyuchoides: Fig. 8n; Sclerospora stellatus: Fig. 8o) or ornamented (e.g., Fig. 8p; Albugo ipomoeae-panduratae; Voglmayr and Riethmüller 2006). In Saprolegnia there are often thinner-walled pit regions through which the germ tube hyphae escape. Mature oospore walls are also thick multi-layered structures and contain a large amount of storage carbohydrates (and probably lipids) that are mobilized upon germination (Beakes and Bartnicki-Garcia 1989; Bartnicki-Garcia and Wang 1983). The thick (2–3 μm) innermost endospore wall layer may be multilayered as in the genus Saprolegnia (Fig. 8q Beakes and Gay 1978b) or relatively homogeneous as in Cornumyces (Fig. 8r) and most Peronosporomycete species (Fig. 8t, u; Beakes 1981; Beakes and Bartnicki-Garcia 1989; Hemmes and Bartnicki-Garcia 1975). In the Peronosporomycetes, the outermost oospore wall layer (the exospore layer; Beakes 1981) may at least be partially derived from the residual periplasm (Fig. 8s) and is particularly thick and complex in the Albuginales (Fig. 8h; Stevens 1901; Tewari and Skoropad 1977). In the Albuginales and many Peronosporales species (such as Peronospora tomentosa, Fig. 4l and Myzocytiopsis vermicola, Fig. 8o; Glockling and Beakes 2006a) the exospore is unevenly thickened, which gives the oospores their ornamented appearance (Fig. 8n–p).

The onset of germination is indicated by the rapid digestion and reabsorption of the thick inner endospore wall (Beakes 1980b; Beakes and Bartnicki-Garcia 1989) followed by the breakdown of the electron-dense ooplast globule material as the central vacuole expands. The broad germ tube hypha is often terminated by a zoosporangium (Ruben and Stangellini 1978). In Albugo also the swollen oospore may be converted directly into a zoosporangium, as depicted by Schröter (1893).

Genomic Studies

So far, there are no genome sequences for any Hyphochytriomycota in the public domain, although Hyphochytrium catenoides is being sequenced by Tom Richards, University of Exeter, and as part of the ATCC 18717 genome project. Some prelimary data for this organism has been included in publications, exploring horizontal gene transfer into the Oomycota (Richards et al. 2011; Savory et al. 2015). The top ten Oomycota pathogens, which genomes have been sequenced (even though some have not been released to the public domain so far) and which have been extensively studied in molecular plant pathology have recently been reviewed by Kamoun et al. (2015). Six are Phytophthora species, with the potato blight pathogen, Ph. infestans coming top of the list. The remaining places, were taken by two downy mildews (Hyaloperonospora arabidopsis and Plasmopara viticola), and a single Albugo and Pythium (Kamoun et al. 2015). The downy mildew Hyaloperonospora arabidopsidis and white blister rust Albugo laibachii both infect the model plant Arabidopsis, and have provided excellent systems in which to explore host pathogen interactions at the molecular level (Kemen and Jones 2012; Thines et al. 2009a). Much recent effort has been directed at unravelling the molecular basis of pathogenicity in economically important plant pathogenic oomycetes (see reviews by Jiang and Tyler 2012; Thines and Kamoun 2010). However, compared with the Fungi, genetic manipulation of stramenopiles has generally proven difficult and frustrating. With a few exceptions, such as Phytophthora capsici, it has been difficult to routinely transform Oomycota (Judelson and Ah-Fong 2009). Gene silencing techniques have often been the only tool available to explore gene functions (Whisson et al. 2009).

Representatives of the phytopathogenic genera Albugo (Kemen et al. 2011, Links et al. 2011), Hyaloperonospora (Baxter et al. 2010), Peronospora (Derevnina et al. 2015), Plasmopara (Sharma et al. 2015a), several Phytophthora species (e.g., Haas et al. 2009; Judelson 2012; Tyler et al. 2006), Pseudoperonospora (Tian et al. 2011) and Pythium ultimum (Cheung et al. 2008; Lévesque et al. 2010) and the fish pathogen, Saprolegnia parasitica, have had their full or partial genome sequences released. Comparative genomics is promising to unlock many interesting secrets about these organisms (see Greville-Briggs et al. 2011; Judelson 2012; Lamour et al. 2007; Pais et al. 2013; Seidl et al. 2012; Sharma et al. 2015a, b). Features of genome evolution in the Oomycota, has revealed repeat-driven expansions, deletions, gene fusions and horizontal gene-transfer (Judelson 2012; Haas et al. 2009; Savory et al. 2015; Tyler et al. 2006). One surprising discovery appears to be the extent to which the genomes of oomycetes contain genes derived from other prokaryotes and eukaryotes, suggesting horizontal gene transfer (HGT) from bacteria, fungi and red and green algal endosymbionts (Jiang and Tyler 2012; Maruyama et al. 2009; Richards et al. 2006; Soanes et al. 2007). Genes of green algal ancestry have been discovered in oomycetes (Richards et al. 2011; Jiang and Tyler 2012). This might suggest that the single plastid acquisition-multiple loss interpretation related to evolution of non-photosynthetic organisms, such as Oomycota, from a photosynthetic ancestor needs further evaluation (Dorrell and Smith 2011; Maruyama et al. 2009; Stiller et al. 2009).

Recent genomic studies on non-biotrophic pathogens in genera such as Aphanomyces (Gaulin et al. 2007; Krajaejun et al. 2011) , Saprolegnia (Torto-Alalibo et al. 2005; Wavra et al. 2012) and Pythium (Cheung et al. 2008; Lévesque et al. 2010) show these organisms contain a formidable array of glucanase and proteinase encoding genes, which have enabled them to so successfully exploit a wide range of plant and animal substrates (Jiang and Tyler 2012). Genomic studies have also revealed a startling array of pathogenicity factors and effector molecules, which presumably have enabled Phytophthora species (Judelson 2012; Lamour et al. 2007; Morgan and Kamoun 2007; Qutob et al. 2002; Sharma 2015a), downy mildew species (Baxter et al. 2010, Derevnina et al. 2015, Sharma et al. 2015a, b), and white blister rusts (Kemen et al. 2011; Links et al. 2011) to become such effective plant pathogens. The independent evolution of obligate biotrophy in the white blister rusts is also reflected by the fact that Albugo laibachii, the white blister rust pathogen of Arabidopsis thaliana (Thines et al. 2009c), has a much smaller genome compared with obligate parasites in the Peronosporales (Kemen and Jones 2012; Kemen et al. 2011) and has evolved a novel group of CHxC/CxHC effectors that are unique to this clade (Kemen et al. 2011; Links et al. 2011).

Classification

Karling (1977) presents what is probably the most realistic systematic treatment of the Hyphochytriomycota. He questioned Sparrow’s (1973) classification that placed emphasis on zoospore cleavage patterns and rejected Canteriomyces and Rhizidiomycopsis as independent genera. In this account the Hyphochytriomycota have been treated as a phylum in their own right, which may also include the phagotrophic protist, Pirsonia (Kühn et al. 2004), which we will consider to be of incertae sedis.

The most recent formal systematic account of the Oomycota was by Dick (2001) and is largely based on a critical and scholarly evaluation of morphological characters. Since this account was published there have been many molecular phylogenetic studies on oomycetes (see review by Beakes et al. 2014a). Most of these have compared genes such as those encoding the small (SSU) and large ribosomal subunits (LSU) and the intervening internal transcribed spacer region (ITS), beta-tubulin, NADH and the mitochondrially-encoded cytochrome c oxidase subunit II genes (cox2). Some studies have concentrated on higher level taxonomic boundaries and general phylogenic relationships (e.g.; Choi et al. 2015; Dick et al. 1999; Göker et al. 2007; Hudspeth et al. 2000; Lara and Belbahri 2011; Léclerc et al. 2000; Petersen and Rosendahl 2000; Riethmüller et al. 1999; Thines et al. 2008, 2015b), whilst others have been concerned with resolving species clades within the main genera (e.g., Albugo Choi et al. 2007, 2008; Ploch et al. 2010; Thines et al. 2009c: Aphanomyces Diéguez-Uribeonodo et al. 2009; Levenfors and Fatehi 2004; Lilley et al. 2003; Haliphthoros Sekimoto et al. 2007; Basidiophora Sökücü and Thines 2014; Hyaloperonospora Göker et al. 2004, Peronospora Voglmayr 2003; Peronosclerospora (Telle et al. 2011), Phytophthora Blair et al. 2008; Cooke et al. 2000; Förster et al. 2000; Runge et al. 2011; Pseudoperonospora Choi et al. 2005, Runge et al. 2011; Pythium Lévesque and de Cock 2004; Martin 2000; Saprolegnia Diéguez-Uribeondo et al. 2009; Hulvey et al. 2007; Inaba and Tokumasu 2002; Léclerc et al. 2000; Sandoval-Sierra et al. 2014; Steicow et al. 2013, 2014). As a result of these studies it is now clear that many of the taxonomic changes that were introduced by Dick (1997, 2001) are not supported by molecular data and require substantial revision. It is also becoming apparent that many of the ordinal, family and generic circumscriptions in Oomycota require re-evaluation and that many traditional morphological characters used in taxonomy (such as patterns of asexual spore formation in the Saprolegniceae, patterns of antheridium attachment in Phytophthora and conidiophore development in the downy mildews etc.) are not reliable indicators of genetic relatedness.

A revised taxonomic framework of the Hyphochytriomycota and Oomycota based on molecular data is summarised in Table 1. We have refrained from making formal taxonomic descriptions, but will use working names, indicated by “ ” when first used for likely new classes, orders and families. Those taxa that we consider not to be monophyletic and consider are in need of revision are indicated by the ~ before them. We have assumed that the Oomycota form a phylum in their own right and consequently have raised to full class rank the sub-orders proposed by Dick (2001). The placement of the taxa (Rhipidiales, Leptomitales and “Atkinsiellales”) which lie at the cusp of the divergence of the main groups, the Saprolegniomycetes and Peronosporomycetes, have proven particularly problematic and their taxon sampling under-represented, as is the case with many of the smaller marine and holocarpic genera (Table 1).

The majority of Oomycota genera listed in Table 1 fall into one of two major clades with a high degree of statistical support (Fig. 9b). These have been assigned as separate classes the Saprolegniomycetes and Peronosporomycetes (Beakes et al. 2014a, Thines et al. 2015a), which approximate to the galaxies proposed by Sparrow (1976) and assigned sub-class status by Dick (1997, 2001). Molecular studies have also revealed a number of early diverging basal clades, mostly encompassing marine species (Cook et al. 2001; Küpper et al. 2006; Sekimoto et al. 2007, 2008a, b). However, because of the limited or complete absence of molecular data for many genera in these early-diverging clades, we have refrained from assigning them to new classes at present and therefore they are placed under class(es) incertae sedis (Table 1).

Phylum Hyphochytriomycota

Class Hyphochytriomycetes

Order Hyphochytriales

Fuller (1990, 2001) considered that the Hyphochytriomycota consisted of one class (Hyphochytriomycetes), one order (Hyphochytriales), and three families (Anisolpidiaceae, Rhizidiomycetaceae, and Hyphochytriaceae). The Rhizidiomycetaceae have simple monocentric thalli and release their zoospores into a vesicle (Fig. 6b), consisting of 3 genera (Dick 2001; Fuller 2001). The Hyphochytriaceae have polycentric thalli and zoospores differentiate fully within the sporangium and are not released into a transient vesicle and at present also contains 3 genera (Dick 2001; Fuller 2001). Only two Hyphochytiomycota genera, Hyphochytrium and Rhizidiomyces , have so far been sequenced and together form a well supported clade that is well separated from the Oomycota (Fig. 1b). Recent molecular sequencing has shown that Anisolpidium belongs within the Oomycota (Gachon et al. 2015) and will be excluded from the Hyphochytiomycota in this account.

Phylum Oomycota Arx

Basal Class(es) – incertae sedis

Order “Eurychasmales”

The “Eurychasmales” (Table 1, Fig. 9b; Sparrow 1976) are a monotypic order of holocarpic parasites of seaweeds. Although three Eurychasma species have been described, most is known about E. dicksonii (Fig. 5c) a widespread parasite of filamentous brown seaweeds (Greville-Briggs et al. 2011; Küpper and Müller 1999). In all phylogenetic trees where it is included, Eurychasma is the earliest-diverging clade (Küpper et al. 2006; Sekimoto et al. 2008a; Strittmatter et al. 2013).

Order Haptoglossales M.W. Dick

The Haptoglossales (Dick 2001) forms a second early-diverging order (Table 1, Fig. 9b), which may ultimately form a new class together with the Eurychasmales as they both appear to share a common ancestor, but always with long branch separation (Beakes et al. 2006). This monotypic order and family contains a dozen or so species, all of which are parasites of bacterivorous nematodes and rotifers (Beakes and Glockling 1998, 2000, 2002; Glockling and Beakes 2000b, c; Hakariya et al. 2002, 2007). Haptoglossa (Figs. 2f, 3a, b, 5) is unusual amongst the genera in the early diverging clades of Oomycota in that it is a predominantly terrestrial genus, although H. heterospora has also been reported to infect marine nematodes (Newell et al. 1977). This genus produces unique infection ‘gun cells’ (Figs. 3b, 7q; Beakes and Glockling 1998; Robb and Barron 1982). Recent studies have revealed a number of species, such as H. erumpens (Beakes and Glockling 2002) and H. heteromorpha (Glockling and Beakes 2000c), which produce several morphological types of gun cells, which suggest they may have evolved to infect multiple hosts. Species within Haptoglossa clade also appear deeply diverging (Hakariya et al. 2007) and this genus will require revision.

Order ~Olpidiopsidales s. lat. M.W. Dick

The ~Olpidiopsidales (Fig. 5e–g) as currently defined is a paraphyletic or polyphyletic order of predominantly marine genera that are mostly parasites of marine algae (Fig. 5e–f). This order traditionally encompased three families, the Olpidiopsidaceae, Sirolpidiaceae and Pontismataceae (Dick 2001) but so far only representatives of the first family have been sequenced. The different species of marine Olpidiopsis for which sequence data have so far been published fall into two closely related clades, one with O. porphyrae and O. pyropiae (Klochclova et al. 2015; Sekimoto et al. 2008b) and the second with O. bostrychiae and O. feldmanni (Fletcher et al. 2015; Sekimoto et al. 2009) (Table 1). However, the type of the genus, O. saprolegniae, a freshwater endoparasite of saprolegniaceous water moulds (Bortnick et al. 1985), does not form a monophyletic clade with the marine species (Sekimoto and Inaba, unpublished sequences). This means the marine species will most likely have to be renamed. Recently, Gachon and colleagues (personal communication) have shown that two Anisolpidium species (A. ectocarp, A. rosenvingei) also forms a discrete clade nested between the marine Olpidiopsis spp. and the “Haliphthorales” clade. Therefore, it seems likely that as currently constituted even the genus Olpidiopsis is probably polyphyletic and will need significant revision, with new genera names required for the marine species.

Order “Haliphthorales”

The “Haliphthorales” (Figs. 2j–m, 5h) has not been formally described and among others contains the parasites of marine crustacea, Haliphthoros and Halocrusticida (renamed as Halodaphnea by Dick in 1998, but without supporting molecular data). These species can be cultured on agar media, have constricted segmented thalli (Hatai 2012; Hatai et al. 1980, 1992; Sekimoto et al. 2007), and form rather long (often >100 um) hyphal like discharge tubes (Fig. 5j). At present a single order (not as yet not formally described) and family (Haliphthoraceae) contains three or four poorly circumscribed genera (Sekimoto et al. 2007), including the recently described parasite of abalone, Halioticida (Maurosa et al. 2009). Haliphthoros as currently recognised appears to be a paraphyletic genus, with some “Haliphthoros-like” isolates apparently occuring within the crown Oomycota clade close to Atkinsiella (Sekimoto et al. 2007; Gachon, personal communication). Clearly much more research is required on this order.

It also seems possible that Petersenia and Pontisma in the Pontismataceae and Sirolpidium in the Sirolpidiacae will also turn out to be related to these two early-diverging marine orders or the basal lineages of the Saprolegniomycetes, currently they are placed as orders incertae sedis until sequence data become available (Taxonomic Summary; Table 1). The Ectrogellaceae (Dick 2001; Karling 1981) has been traditionally considered as part of the Saprolegniomycete line (Sparrow 1973, 1976) and also forms ‘naked’ plasmodial thalli in their diatom hosts similar to Lagenisma (Raghukumar 1980 – see below). However Ectogella has not yet been sequenced and therefore the Ectrogellaceae must also be considered as a family incertae sedis.

Class Saprolegniomycetes Thines et Beakes

The Saprolegniomycetes (Table 1; Fig. 9b), are characterized by the formation of two morphologically distinct generations of zoospore or aplanospore (Figs. 6c, 7a, d), a phenomenon usually referred to as diplanetism (see Dick 2001; Johnson et al. 2002). Fully differentiated zoospores or aplanospores are released directly from the sporangium (Fig. 6g, h). Both zoospores (Figs. 6f–h, 7b, d) and oospores are formed as a result of centrifugal cleavage (Fig. 8a) without the differentiation of a peripheral periplasmic layer of cytoplasm. Saprolegniomycetes are able to synthesize the sterols they require for oogenesis and generally utilize ammonium as a source of nitrogen and may also use organic sulphur (Gleason 1976). We have taken a conservative approach to their taxonomy, recognizing three orders within the class, the “Atkinsiellales”, Leptomitales s. lat., and Saprolegniales (Fig. 9, Table 1).

Order “Atkinsiellales” and closely related taxa.

The order Atkinsiellales contains a handful of relatively little studied parasites of marine crustaceans and terrestrial invertebrates and contains two families as defined by Dick (1998, 2001), the Atkinsiellaceae and Crypticolaceae. Atkinsiella dubia forms a highly distinct clade (Fig. 16) at the base of the Saprolegniomycetes (Cook et al. 2001; Sekimoto 2008; Sekimoto et al. 2007, Thines et al. 2015a). A second species, Atkinsiella entomophaga, a parasite of dipteran larvae described by Martin (1977), was transferred by Dick (1998) to the previously monotypic genus Crypticola. The latter had been created for C. clavulifera, a parasite of mosquito larvae described by Frances et al. (1989). C. clavulifera forms a clade with A. dubia in cox2 analyses (Deborah Hudspeth, personal communication), which suggests the Crypticolaceae should also be included in this order, although family cirumscriptions require more data.

The diatom pathogen Lagenisma coscinodisci, which Dick (2001) placed in its own family, the Lagenismataceae, has been shown to form an early diverging Saprolegniomycete clade with some affinity to Atkinsiella (Thines et al. 2015a). We have therefore included this family in the Atkinsiellales (Table 1). The paraphyletic genus Chlamydomyzium (Dick 2001), which has both Saprolegniomycete and Peronosporomycete characteristics (Glockling and Beakes 2006b; Beakes et al. 2014), also forms clades amongst these early diverging Saprolegniomycete genera (Beakes et al. 2006; Beakes et al. 2014a). Isolates of the genus Cornumyces obtained from keratin baits appears to be closely related to the nematode parasite Chlamydomyzium (Fig. 2o; Inaba unpublished trees) as well as to the Leptomitales clade (Inaba and Hariyama 2006). Dick (2001) also transferred Lagenidium pygmeaum to Cornumyces in absence of molecular data supporing this. He considered Cornumyces might belong in the Leptolegnielliaceae for which there is as yet no supporting sequence data. It is clear that much more work is required on these little studied basal Saprolegniomycetes before their formal taxonomy can be fully resolved.

Order Leptomitales Kanouse

The Leptomitales is a long-standing order that formerly included two families, the Leptomitaceae and Rhipidiacae (Dick 1973a; Sparrow 1960). These were separated into two orders by Dick (2001), and the Rhipidiales are now thought to be members of the Peronosporomycetes (Hudspeth et al. 2003; Thines et al. 2009c). The revised Leptomitales encompasses four small families, the most familiar of which are the Leptomitaceae, which are commonly known as sewage fungi. The Saprolegniomycete characteristics of Apodachlya and Leptomitus had long been been recognized (Beakes 1987) and sequence data confirms they form an early diverging clade within the class (Petersen and Rosendahl 2000). Recently the anamorphic genus Blastulidium paedophthorum, a parasite of freshwater cladocerans, has been confirmed to be in a clade close to Apodachlya and Leptomitus (Duffey et al. 2015), which confirms Dick’s placement in the Leptomitales. To date no sequence data exists for any member of the Ducellariaceae and Letolegnielliaceae that Dick (2001) also included in the Leptomitales. These families contain a number of rarely encountered, holocarpic genera (Aphanodictyon, Aphanomycopsis Brevilegniella, Ducellaria, Leptolegniella, and Nematophthora) that have been mainly been documented by Karling (1981).

Order Saprolegniales E. Fisch.

The Saprolegniales is one of the largest and longest-established orders (Sparrow 1960, Dick 1973b) and forms a well-supported monophyletic clade (Dick et al. 1999; Inaba and Tokumasu 2002; Léclerc et al. 2000; Petersen and Rosendahl 2000; Riethmüller et al. 1999; Spencer et al. 2002; Steicow et al. 2014). Beakes et al. (2014a) suggested this order should be divided into three family level clades: a redefined Verrucalvaceae, the “Achlyaceae” and a re-circumscribed Saprolegniaceae sensu stricto. Dick et al. (1999) had introduced the family Leptolegniaceae which encompassed the genera Aphanomyces, Plectospira and Leptolegnia. Unfortunately, the inclusion of Leptolegnia with these other two genera is not well supported by most molecular studies (e.g., Arcate et al. 2006; Léclerc et al. 2000; Petersen and Rosendahl 2000; Steicow et al. 2013, 2014). Furthermore subsequent molecular studies have also shown that the grass pathogens, Pachymetra and Verrucalvus, which Dick et al. (1988) had placed in their own family, the Verrucalvaceae, also fall within the Aphanomyces clade (Hudspeth et al. 2003; Riethmüller et al. 2002; Telle and Thines, unpublished data). Therefore the family name Verrucalvaceae should take precedence over Leptolegniaceae. This clade is characterized by having species with narrow hyphae and, when formed, relatively undifferentiated sporangia (Fig. 3f). Genera in this clade are predominantly soil-borne, root-infecting parasites, saprotrophs or animal parasites (Fig. 3e–g; Dick et al. 1984, 1988; Diéguez-Uribeondo et al. 2009; Johnson et al. 2002; Levenfors and Fatehi 2004; Lilley et al. 1998). The Verrucalvaceae also includes the nematode-trapping genus Sommerstorffia (Spies and Levesque, unpublished sequence data) as well as the recently described rotifer parasitic genus, Aquastella (Fig. 3d; Molloy et al. 2014). The genera Aphanomyces and Plectospira both form clusters (balls) of primary aplanospores (Fig. 6c), a feature shared with Somerstorffia (Johnson et al. 2002). All the genera form uni-oosporiate oogonia with more or less plerotic oospores, which in Verrucalvus have prominent verrucose ornamentation (similar to shown in Fig. 8n, o; Dick et al. 1988).

Although the branching order of the proposed family clades in the Saprolegniales is not well-resolved statistically, morphological and molecular evidence points to the recircumscribed Verrucalvaceae as the basal family in the Saprolegniales. A comprehensive molecular phylogenetic study of the genus Aphanomyces has shown that saprotrophic species, animal parasites and plant pathogens separate into three well supported sub-clades (Diéguez-Uribeondo et al. 2009). Dick et al. (1984) controversially also placed the graminicolus downy mildews in the Verrucalvaceae (Dick 2001) but this is not supported by molecular sequence data (Table 1; Hudspeth et al. 2000, 2003; Léclerc et al. 2000; Riethmüller et al. 1999, 2002; Thines et al. 2008).

The diverse genera of saprotrophic “water moulds” were traditionally all placed in a single family, the Saprolegniaceae containing a dozen or so genera (Table 1; Johnson et al. 2002; Sparrow 1960). Different genera were largely defined by their pattern of zoosporogenesis and asexual spore formation (Fig. 6d–h; Dick 2001; Johnson et al. 2002). However, it seems the best predictor of family-level relationships in the Saprolegniaceae is whether their mature oospores have centric/subcentric (as in Fig. 8k) or eccentric (as in Fig. 8l, m) organization (Léclerc et al. 2000; Spencer et al. 2002; Inaba and Tokumasu 2002). In some analyses (Inaba and Tokumasu 2002) genera with centric or subcentric oospores (Aplanes, Aplanopsis, Calyptralegnia, Protoachlya, Newbya and Saprolegnia , and possibly Leptolegnia) can be separated from those which produce strongly eccentric oospores (Achlya s. str., Brevilegnia, Dictyuchus, Isoachlya, and Thraustotheca). In the genus Saprolegnia, the mature ooplast often contains granules in Brownian motion as a result of the liquifaction of the matrix (Fig. 8k, g). However, even the archetypal water mould genus Saprolegnia is apparently not monophyletic, although molecular phylogeny is beginning to help resolve species boundaries (Diéguez-Uribeondo et al. 2007; Hulvey et al. 2007; Inaba and Tokumasu 2002; Sandoval-Sierra et al. 2014). Although we suggested a new family, the “Achlyaceae”, might be warranted for the clade containing genera with strongly eccentic oospores, recent publications suggest this may be an an oversimplistic solution (Steciow et al. 2013, 2014; Sandoval-Sierra et al. 2014). Therefore we have decided not to formally split the Saprolegniaceae in this account (Table 1, Fig. 9b). Clearly further work is required before this large and complex family is formally split into well supported families.

Class: Peronosporomycetes M.W. Dick

The Peronosporomycetes are predominantly a terrestrial class. Most have a mycelial fungus-like thallus, although there are holocarpic species and many of the Rhipidiaceae have constricted thalli of determinate growth. Peronosporomycetes have been reported to have a requirement for exogenous sterols to complete oogenesis (Kerwin and Washino 1983) and the non-obligate pathogens of plants are able to utilize sulphate and variable nitrogen sources (Gleason 1976; Dick 2001), while there seems to be a tendency that non-obligate animal parasites and obligate plant parasites have defects in the pathways for the acquisition of inorganic nitrogen and sulfur (Baxter et al. 2010; Kemen et al. 2011; Sharma et al. 2015b). Peronosporomycetes produce only secondary type zoospores (Fig. 7i), which are differentiated within or transiently released into an evanescent extrasporangial vesicle in several genera (Fig. 6m). They have mono-oosporic oogonia in which the single oosphere is surrounded by a layer of periplasm (Fig. 3c, e, i; Dick 2001). Mature oospores often have complex multilayered walls (Fig. 3h, s) and a homogeneous (ooplast) vacuole (Fig. 3i).

Dick (2001) included the orders Rhipidales, Pythiales and Peronsporales within his Peronosporomycotina sub-class. Subsequent molecular studies revealed the white-blister rusts, form a separate basal order (the Albuginales) in their own right (Thines and Spring 2005). Many molecular studies suggest that the order level separation of the Pythiales and the Peronsporales along the lines proposed by Dick (2001) is not supported statistically (see discussion in Beakes et al. 2014a) and some genera, such as Phytophthora, were incorrectly placed (Hulvey et al. 2010; Thines et al. 2009a,). Furthermore, unpublished multigene sequencing of genera, is revealing much more diversity amongst the lagenidiaceous and pythiaceous species than has hitherto been suspected (Spies et al. 2014, 2016). However, until more statistically robust multigene sequence data are publically available, as in our previous review, we have adopted the historical position of including all these genera, into a single all-encompassing Peronosporales s. lat. and not suggested new orders and families (Fig. 16, Table 1) to account for a probably paraphyletic Pythiaceae. However, we feel that the recognition of a broad Peronosporales might be preferable over the creation of several new ill-defined orders. At least one clade, that contains the unusual recently-described lagendiaceous mycopathogen of dogs, Paralagenidium karlingi (de Grooters et al. 2013), appears to be located between the Rhipidiales and Albuginales and will will probably need to be placed in its own Order and Family (Table 1).

Order Rhipidiales M.W. Dick.

The Rhipidiales consists of a single family, the Rhipidiaceae, containing a small number of saprotrophic genera (Table 1), which often grow on submerged twigs and fruits. Many have determinate, often segmented, thalli with only a few genera showing typical hyphal growth (e.g., Sapromyces, Fig. 2p). Some genera, such as Rhipidium, have thalli that are anchored to their substrate by rhizoid-like structures (Dick 2001; Sparrow 1960). They typically produce uni-oosporiate oogonia with a well differentiated periplasm (Sparrow 1960). To date only Sapromyces elongatus has been sequenced (Table 1). The phylogenetic placement of this species in phylogenetic trees has proven difficult and varies depending upon the gene sequenced and which other taxa are included in the analyses. Riethmüller et al. (1999) and Petersen and Rosendahl (2000) inferred a position basal to the ‘saprolegnian line’ in their LSU rDNA analyses, whereas Hudspeth et al. (2000) report it to form the basal clade to ‘peronosporalean line’. The COII amino acid sequence derived from from the cox2 gene, showed that Sapromyces has the same signature amino acid insertion-deletion (indel) sequence (LEF/T) to that found in members of the Peronosporales s.l., and not the YTD indel sequence found in members of the Leptomitaceae (Hudspeth et al. 2000, 2003; Cook et al. 2001). It is clear that much work still needs to be done to resolve the precise relationships between families and genera that appear at the base of both main classes.

Order Albuginales Thines

Traditionally, the white blister rusts, the Albuginales (Fig. 5), were placed together with the downy mildews in the Peronosporales (Beakes 1987; Dick 2001). They are obligate pathogens of angiospermae producing small stalked globose haustoria (Coffey 1975; Mims and Richardson 2002, Soylu et al. 2003). They form blister-like lesions on the leaves (Fig. 4f, i) below the host epidermis in which the basipetal chains of deciduous conidiosporangia are borne on club-shaped sporogenous hyphae (Fig. 4g, h; Heller and Thines 2009). Molecular phylogenetic studies revealed that the white blister rusts form a well supported clade basal to the Peronosporales s. lat. (Fig. 9b; Hudspeth et al.; 2003, Riethmüller et al. 2002; Thines et al. 2009c). This clade has been given its own order designation, the Albuginales (Thines and Spring 2005), containing just one family, the Albuginaceae (Table 1). Members of this family have exceptionally thick, multilayered oospore walls (Stevens 1901; Tewari and Skoropad 1977; Beakes 1981), the outer layers of which appear to be mainly derived from the periplasm. Recent molecular studies have also revealed an unsuspected genetic diversity within this order (Choi et al. 2007, 2008, 2011; Mizaee et al. 2013; Ploch et al. 2010; Ploch and Thines 2011; Rost and Thines 2012; Thines and Voglmayr 2009; Thines et al. 2009c; Voglmayr and Riethmüller 2006) and two new genera, Pustula and Wilsoniana, have been established based upon conidiosporangium and oospore characteristics (Thines and Spring 2005). These three genera appear to be restricted to specific host orders or subclasses (Thines and Voglmayr 2009). It is also expected that more comprehensive taxonomic re-arrangement of this family will be required as more species and isolates are sequenced.

Order Peronosporales E. Fisch. s. lat

The order Peronosporales s. lat. (Waterhouse 1973) contains a large number of often diverse taxa (Table 1), presently placed in three families, the Salispiliaceae, ~Pythiaceae s. lat. and Peronosporaceae s. lat. (Beakes et al. 2014a). This classification has to be considered provisional, as many lagenidiaceous species have not yet been included in published molecular phylogenies. Within the Peronsporales s. lat. There have been many published molecular phylogenetic studies on the important plant pathogenic genera (Pythium: de Cock et al. 2012; Lévesque and de Cock 2004; Phytophthora: Blair et al. 2008; Cooke et al. 2000; Kroon et al. 2004; Martin et al. 2014) and various downy mildew genera (Göker et al. 2003, 2004, 2007; Thines et al. 2009a, b; Voglmayr 2003; Voglmayr et al. 2004). The saprotrophic genera have been less well documented, but there have been accounts of the molecular phylogeny of Pythiogeton (Huang et al. 2012), Phytopythium (de Cock et al. 2015) and Halophytophthora (Nakagiri 2002), but molecular data for the “lagenidiaceaous” holocparic genera is sparse and incomplete (Beakes et al. 2006; Schroeder et al. 2012).

The Salispiliaceae is single genus family which forms a well-supported early-diverging clade in the Peronsporales s. lat. based on concatenated ITS and LSU sequences (Hulvey et al. 2010). They are saprotrophs isolated from salt marshes, with ovoid sporangia and smooth walled oogonia and oospores. However, unpublished trees based on an analysis of 16 genes do not support a basal phylogenetic position of this genus within the Peronsporales s.lat. (see Table 1; Spies et al. 2014 and personal communication). The ~Pythiaceae s. lat. as we have defined it (Beakes et al. 2014a) encompasses more than a dozen genera, including a many of holocarpic genera that were traditionally placed in the Lagenidiales (Table 1, Fig. 9b). However, a recent unpublished multigene analysis of a significant number of isolates identified as ~Lagenidium, ~Lagena, ~Myzocytiopsis, Pythiogeton, ~Pythium and Salilagenidium has revealed at least six clades that may ultimately justify family level designation (Spies et al. 2014, 2016, and unpublished trees - summarised in Table 1). There are still a number of Pythiaceous genera, such as Medusoides described by Voglmayr et al. (1999) and placed by Dick (2001) in his Pythiogetonaceae, for which no sequence data are publically available. Lagenidium, as currently recognised, is a particularly complex paraphyletic or polyphyletic genus, with isolates occuring in several different clades. However, until detailed phylogenies become available, we have retained all of these holocarpic species in a broadly defined ~Pythiaceae s. lat. (Table 1). The genus Pythium contains well over a hundred species, most of which have sequence data available (Bedard et al. 2006; Briard et al. 1995; Lévesque and de Cock 2004; Martin 2000; Schurko et al. 2004; Villa et al. 2006). Lévesque and de Cock (2004) recognised 8 clades (A-K) of Pythium, some of which are now assigned to new genera (Bala et al., 2010; de Cock et al. 2015; Usuhashi et al. 2010). However, as the relationships of these clades have not been fully resolved, most are subsumed under Pythium s. lat. in this review. Species which have simple more or less filamentous sporangia now constitute the genus Pythium s. str. (Usuhashi et al. 2010) although some genera, including the animal pathogen P. insidiosum cluster with Pythiogeton (Huang et al. 2012).

The Peronosporaceae s. lat. family (Table 1, Fig. 9b) includes not only the hyperdiverse downy mildews, but a number of genera that had been been previously included in the Pythiaceae (Dick 2001). These include the genus Phytopythium (syn. Ovatosporangium, Usuhashi et al. 2010; formerly known as the Pythium K-clade, Lévesque and de Cock 2004) described by Bala et al. (2010) and which has been recently monographed by de Cock et al. (2015). A recent multigene analysis also suggests that two other of the new pythiaceous genera introduced by Usuhashi et al. (2010), Elongisporangium and Globisporangium might also fall in the Peronosporaceae s. lat. clade (Spies et al. 2014, 2016). The polyphyletic marine genus ~Halophytophthora (Ho and Jong 1990; Ho et al. 1992; Nakagiri 2002) contains around 15 species many of which, including the type species, fall into a clade that sits between the Phytopythium and the Phytophthora/downy mildew assemblage. ~Halophytophthora spp. have ovoid to elongate sporangia, often with conspicuous papillar plugs (Nakagiri 2002, Nakagiri et al. 1994) and most show a transient vesiculate discharge of their zoospores (Fig. 6l). All have single-oospored oogonia with paragynous antheridia (Nakagiri 2002, Nakagiri et al. 1994). Phytophthora clades are probably paraphyletic with the hyperdiverse downy mildews, which appeared to have evolved from a clade of shoot- and leaf-infecting Phytophthora spp. (Cooke et al. 2000, Runge et al. 2011). Most Phytophthora taxa (Fig. 4a–e) have sequence data available (Blair et al. 2008; Brouwer et al. 2012; Cooke et al. 2001; Förster et al. 2000; Kroon et al. 2004; Martin and Tooley 2003a, b; Runge et al. 2011; Villa et al. 2006) and fall into 8 to 10 clades (usually referred to as groups). The clades can be broadly separated into two main evolutionary lines, encompassing those species (groups 6–8; Cooke et al. 2000) with non-papillate sporangia (e.g., Ph. cinnamomi; Fig. 4c) which are predominantly soil borne root or woody trunk infecting pathogens and those (Groups 1–5; Cooke et al. 2000) which have papillate sporangia (e.g., Ph. infestans) that often infect aerial foliage. Traditional morphological characters such as the morphology of the male antheridium and whether species are homo or heterothallic are not good markers of phylogenetic relatedness (Blair et al. 2008; Brouwer et al. 2012; Cooke et al. 2000; Kroon et al. 2004; Runge et al. 2011). In a recent phylogenetic analysis based upon whole genomes, albeit of the very restricted number of five taxa, Seidl et al. (2012) concluded that the downy mildews (represented by Hyaloperonospora) were sister to the Phytophthora clade rather than embedded within it, with the nonpapillate/semipapillate Ph. sojae and Ph. ramorum species forming a clade that was sister to the papillate Ph. infestans as in the analysis of Runge et al. (2011). In a recent phylogenomic analysis Sharma et al. (2015a) inferred again a sister-group relationship for Hyaloperonospora and Phytophthora, but also found that Plasmopara halstedii was embedded within the latter, highlighting the need for a an expanded taxon samping in future phylogenomic analyses, as the current taxon sampling is probably too low to infer robust phylogenomic trees, despite the generally high to maximum-support observed in these analyses.

The downy mildews (Fig. 4q–v) are a diverse, monophyletic, group currently encompassing 20 genera (Table 1) that are obligate parasites, predominantly of dicotyledons (Göker et al. 2007; Thines et al., 2009a, Thines 2014). Because of their importance as biotrophic plant pathogens they have been extensively studied and sequenced for phylogenetic analyses (Table 1; Göker et al. 2003, Göker et al. 2007; Riethmüller et al. 2002; Sökücü and Thines 2014; Telle and Thines 2012; Telle et al. 2011; Thines et al. 2008, 2009a; Voglmayr 2003). Downy mildews typically produce deciduous conidiosporangia (Fig. 4s) are that born on persistent conidiosporangiophores (Fig. 4u, s, v), although these may be evanescent in the graminicolous genera Baobabopsis, Eraphthora, Peronosclerospora, Sclerophthora, and Sclerospora (Fig. 4n–p; Thines 2006, 2009, Telle and Thines 2012, Thines et al. 2015b). Peronospora and Pseudoperonospora have pigmented conidia and consititute the most species-rich downy mildew clade (Table 1). Features such as haustorium morphology map well onto the molecular clades (Göker et al. 2007; Thines 2006; Voglmayr et al. 2004). Downy mildews with pyriform haustoria (DMPH) form a monophyletic lineage (Fig. 9). Digit-like (hyphal) haustoria (e.g., Peronospora viciae; Beakes et al. 1982; Hickey and Coffey 1977, 1978) probably represent the ancestral state and are similar to those formed in Phytophthora (Coffey and Wilson 1983). Molecular studies have confirmed that the graminicolous downy mildew (GDM; Fig. 4n–p) genera (Baobabopsis, Thines et al. 2015b; Eraphthora, Telle and Thines 2012; Peronosclerospora, Hudspeth et al. 2003; Shivas et al. 2012; Sclerophthora, Thines et al. 2008; Sclerospora, Riethmüller et al. 2003) are all related to other downy mildews in the Peronosporaceae sensu lato. Three monotypic GDM genera, Graminivora, Poakatesthia and Viennotia (Göker et al. 2003, Thines et al. 2006, Thines et al. 2007) appear to exhibit characteristics intermediate between Phytopththora and the downy mildews sensu stricto (Thines 2009).

Maintenance and Cultivation

Saprophytic or facultative parasitic species of Oomycota can be collected very easily from soil and water, and obligate hyperparasites are sometimes found at the same time. Useful sources of information on suitable methods for isolating and culturing aquatic fungi are given by Dick (2001), Fuller and Jaworski (1987), Johnson et al. (2002) and Sparrow (1960). Obligate parasitic downy mildews and white blister rusts must be sought on their known angiosperm hosts, but the less host-specific root parasites can be isolated using various plating and baiting techniques. Reference should be made to papers cited in Karling (1981) for information on the collection of the less-known species of Oomycota. A useful source of information for collecting and maintaining hemibiotrophic species is found in Erwin and Ribeiro (1998).

Typically many species of Saprolegniaceae and a variety of Pythium species can be isolated from samples of soil or exposed or submerged mud by placing suitable baits (e.g., 3 or 4 autoclaved hempseeds, sesame seeds, or snakeskin scales) added to sediment slurries diluted with sterile pond water (Dick 2001; Dick and Ali-Shtayeh 1986; Fuller and Jaworski 1987; Sparrow 1960). These dishes should be left undisturbed for 1–3 days at 10°–20 °C. The baits should then be transferred to clean dishes of water and incubated at 10°–20 °C for a further 4–14 days. A wide range (about 40 species) of Pythium species has been isolated from soil using a dilution plate procedure (Al-Shtayeh et al. 1986; Dick and Al-Shtayeh 1986). Several species of Phytophthora can be isolated by dilution plate techniques using P₁₀ PV hymexazol agar (for recipes see Erwin and Ribeiro 1998). Dilutions between 1:30 and 1:100 are recommended for infested soils. The same medium can be used for isolations from infected roots. Since Mortierella and Pythium are inhibited by hymexazol, the aliquots can be incorporated into the nutrient agar and the washing stage outlined above is not needed. Incubation is at 25 °C and scanning of plates is carried out after 1–3 days of incubation. Baiting, e.g., with Rhododendron and other leaves is a common procedure to isolate leaf-infecting Phytophthora species.

For the collection of Rhipidiaceae, in situ baiting techniques are essential. A cage of plastic-coated wire mesh containing fruits (e.g., apples, oranges, tomatoes) is suspended just below the water surface or just above the bottom mud in shallow stagnant or slow-moving water for about 10 days. The fruit is then removed and the fungal pustules examined with a dissecting microscope. Filamentous oomycete saprophytes will also be found. Using selective keratin and chitin baits, species that may be parasites of nematodes and other invertebrates are often selectively isolated (Sally Glockling and Shigeki Inaba, personal communication).

A wide variety of agars is used for culturing these oomycetes, including ones based on glucose, peptone and yeast extract (GYP); glucose, soluble starch, and yeast extract; potato dextrose; potatos and carrots; V8-juice; cornmeal, and others. Agars incorporating up to 10 mg/1 of cholesterol are also used: the carrier for the sterol may be chloroform, ether, or a 1% v/v aqueous solution of Tween 80. Axenic cultures are usually achieved by using several cleansing steps, such as by growing through a Raper’s ring. For more details, the reader is referred to Fuller and Jaworski (1987) and Tsoa (1970). Members of the Saprolegniaceae are often stored on infested hemp seeds in distilled water, or on infested hempseeds placed on sterilized dampened filter paper in sterile bottles (Clark and Dick 1974).

Obligate biotrophic species, like the downy mildews and the white blister rusts have so far not been grown on artificial media. There is an account of axenic cultures of graminicolous downy mildews (Sclerophthora and Sclerospora, cited in Thines 2009), which could apparently not be successfully repeated so far. Other downy mildews and white blister rusts can be maintained in the laboratory by using infected leaves to inoculate detached uninfected leaves or leaf disks of the host species with the spores from the former (e.g., by stamping onto moist leaves or spraying). After inoculation, leaves should be kept dark for 24 hours at moderate temperatures. After that, the inoculated leaves or leaf discs should be kept at 100% relative humidity and at moderate temperatures (10–20 °C depending upon the species) and light quality as close as possible to those encountered under natural field conditions and a regular day-night photoperiod cycle. White blister rusts usually have to be cultivated on whole plants and most do not tolerate high humidity during sporulation.

Evolutionary History

The Straminipila form a well-supported monophyletic clade that is sister to the alveolates (Keeling et al. 2005) within the larger SAR superkingdom (Burki et al. 2007, 2008; Burki and Keeling 2014). In analyses using multiple protein-encoding genes the Oomycota and Hyphochytiomycota appear to form a sister clade to the brown-pigmented photosynthetic algae, the Ochrophyta (Cavalier-Smith and Chao 2006; Rilsberg et al. 2009; Tsui et al. 2006). Together this monophyletic assemblage was sister to a second major heterokont clade which encompasses the fungal-like Thraustochytrids and Labyrinthulids and the bacteriotrophic bicoecid flagellates (Beakes et al. 2014; Yubuki et al. 2010). It has been estimated that the stem origin of the Ochrophyta was around 571 million years ago (mya) although with a large margin of error (Brown and Sorhannus 2010). The Oomycota and Hyphochytiomycota probably evolved after this, which is consistent with previous molecular clock estimates had suggested the origins of the Oomycota lay somewhere between 524 and 1000 mya (Bhattacharya et al. 2009). Recent molecular clock analyses by Matari and Blair (2014) proposes that the modern pathogenic oomycetes originated around the mid-Paleozoic, approximately 430–400 mya, although they did not include data from any early diverging genera in their analyses.

From earlier single gene analyses, the marine flagellate genus Developayella forms the sister clade to the Oomycota (Leipe et al. 1996: Tong 1995), although they have apparently little in common. When Sekimoto (2008) included the 18S sequences derived from assorted unknown stramenopiles from diverse marine ecosytems (Diéz et al. 2001; Massana and Pedró-Alió 2008; Massana et al. 2002, 2004, 2006) in his phylogenetic analyses the heterokont tree topography was markedly altered. An unknown stramenopile clade (lineage 3), consisting of a dozen or so rather deeply branched sequences, formed the sister clade to the Oomycota, although with little statistical support. Developayella, clustered in a clade with the flagellate parasitoid Pirsonia and the Hyphochytridiomycota and formed the immediate sister clade to the Ochrophyta rather than the oomycetes. Molecular studies have also revealed that most early diverging genera are marine and many are parasites of seaweeds or marine crustaceans (Beakes and Sekimoto 2009; Beakes et al. 2011). This, together with the fact that most of their closest relatives are also marine (Tsui et al. 2006), supports the current view, contrary to that of Dick (2001), that the Oomycota are marine in origin, as saprotrophs or facultative pathogens (Beakes and Sekimoto 2009; Beakes et al. 2012, 2014a).

Molecular studies have confirmed that the Oomycota are monophyletic and have provided a sound framework for hypothesising likely evolutionary pathways within the phylum. A simplified scheme is presented in Fig. 9a. This shows that the evolutionary scheme originally proposed by Bessey (1942), in which the holocarpic Olpidiopsidaceae were evolving prior to the split of the Saprolegniaceae and Peronsporaceae, was remarkably perceptive. We now know that the earliest-diverging clades contain predominantly small, non-mycelial, holocarpic oomycete genera (Beakes et al. 2014a; Karling 1981; Sparrow 1960), none of which have been successfully cultured on artificial media. This suggests this was the likely thallus form of the ancestral Oomycota. Genera in the Haliphthorales, Atkinsiellales s.lat. (Atkinsiella, Lagenisma), Leptomitales s.lat. (Apodachlya, Blastulidium, Chlamydomyzium, Leptomitus) and Rhipidiales (Araiospora, Rhipidium, Sapromyces) all produce extensive, bulbous or constricted thalli (Beakes et al. 2014a), which appears to be the intermediate stage in the evolution of a more-typical branched mycelial thallus that may have occurred about the time, or shortly after, of the Saprolegniomycete-Peronosporomycete divergence. It may have been the development of long, apically extending, hyphal-like discharge tubes in genera such as Haliphthoros (Fig. 5j) and Atkinsiella that led to the hyphal thallus form, at least in the Saprolegniomycete clade.

Analysis of the host preferences in basal Oomycota also raises the possibility that these organisms might have migrated from the sea to the terrestrial/freshwater environment with their invertebrate or algal hosts. Once on land they may have switched to plant hosts, as evidenced by the morphological similiarity between nematode-infecting species of the genus Myzocytiopsis. (Glockling and Beakes 2006a) and the closely related (Spies, personal communication) root-infecting genus Lagena (Barr and Désaulniers 1987, 1990). However, it should also be borne in mind that as long as the oomycete communities in marine and estuarian detritus remain largely unexplored (Nigrelli and Thines 2013; Marano et al. 2016), other evolutionary scenarios, such as the multiple independent development of a parasitic lifestyle from saprophytic genera cannot be ruled out. The same is also true for the likelihood of the repeated transition of oomycetes from land to the sea and vice versa (Richards et al. 2012), which has occurred several times within the Peronosporomycetes (Marano et al. 2016; Thines 2014). However, on balance it seems plausible that, at least initially, oomycetes evolved in the sea from holocarpic nutritionally-versatile organisms, many of which were facultative parasites of either invertebrates and or algae.

With the possible exception of the freshwater Olipidiopsis spp. (Martin and Miller 1986c), all basal genera lack oogamous sexual reproduction. However, recently a sexual cycle involving conjugation of adjacent cysts or thalli has been reported in Eurychasma, although only on some hosts (Gachon et al. 2015), and also occurs in Anisolpidium ectocarpi (Johnson 1957), a species now known to be a basal oomycote (Gachon et al. 2015). The recent finding that Lagenisma, which also reproduces by means of conjugating meiocysts (Schnepf et al. 1977, 1978a), is a basal Saprolegniomycete (Thines et al. 2015b), could mean that oogenesis may have evolved independently in the two classes of Oomycota. This may also explain the fundamentally different morphological patterns of oosphere formation in the two classes.

A critical evaluation of the fossil evidence for ancient terrestrial oomycetes is given in a recent review by Krings et al. (2011). Stidd and Consentino (1975) describe structures that they suggested represented Albugo oospores in the megagametophyte seed tissue of an ancient gymnosperm, Nucellangium glabrum, from around 310 mya. However the structures that were described were not conclusively Albugo oospores (Krings et al. 2011). A more convincing, though still controversial, Albugo-like microfossil appears to be Hassiella monosperma from the 412 mya lower Devonian Rhynie chert (Taylor et al. 2006). Structures purported to be small oogonia in Hansiella fossils look much more like the small globose haustoria that are typical of the genus Albugo. If this fossil is accepted as representing an obligately biotrophic Albugo-like pathogen of Rhyniophyte plants, it would mean that the evolution of obligate biotrophy can be traced back nearly 400 mya, which accords with recent molecular clock deductions (Matari and Blair 2014). Obligate symbiotrophy exemplified by the Albuginales, is therefore of ancient origin and must have evolved independently at least twice in the oomycete lineage (Kemen and Jones 2012; Kemen et al. 2011; Thines and Kamoun 2010). All extant white blister rusts are obligate parasites of angiosperms and the latter only diversified from a common ancestor about 150 mya, even though they can probably be traced back into the Permian. This implies that the white blister rusts have evolved on hosts other than those we know them on today.

Another fossil genus, Combresomyces, with spiny papillate oogonia with paragynus antheridia, resembling current-day Pythium species, has been recently described associated with the remains of a 300 mya seed fern, Lygniopteris (Strullu-Derrien et al. 2010). Galteriella biscalitheceae associated with a sporangium of a fern Biscallitheca, also from around ca 300 mya, has Phytophthora-like amphigynous and paragynous smooth-walled oogonia. Papillate multi-oospored oogonia, reminscent of those found in some present day genera in the Saprolegniaceae have also been found in Rhynie chert deposits from the same time period (Krings et al. 2010). Therefore by the early Mesozoic era, about 300 mya, fossils showing the complete range of oogonium morphologies found in present day genera in the Albuginales, Peronosporales, and Saprolegniales have all been documented and implies that most of the known oomycete diversity had already evolved by then, likely with the exception of the hyperdiverse downy mildews.

The hyperdiverse obligate parasitic downy mildews are thought to have evolved relatively recent from an ancestor belonging to one of the more derived shoot- and foliage-infecting Phytophthora clades with papillate sporangia (for an in depth discussion see Runge et al. 2011) and represent the pinnacle of oomycete diversity. Thines (2009) has also discussed a number of traits (indeterminate sporangiosphore development, intracellular hyphal development) in rare graminicolous downy mildew genera, such as Viennotia and Poakatesthia, that are shared with Phytophthora and suggests these may represent relicts of the evolution of downy mildews from Phytophthora-like ancestors on Poales.

Finally there appear to be a number of interesting evolutionary parallels between Fungi and Oomycota (Sharma et al. 2015b). The two earliest-diverging oomycete genera Eurychasma and Haptoglossa, have endobiotic plasmodial thalli and injecting infection mechanism, respectively. These features are mirrored in the early diverging cryptomycete Rozella and by microsporidia, respectively (Jones et al. 2011; Lara et al. 2009). The clade (MAST-1) of unknown marine stramenopiles that are the closest to the oomycetes (Sekimoto 2008; Yubuki et al. 2010) may be analogous to the recently described cryptofungal clade that appears to be the sister clade to the Fungi (Jones et al. 2011). This highlights that many phylogenetically critical organisms still remain to be described and we still have little idea what sort of organisms make up unknown stramenopile clades. They are probably being sampled from their zoospores, and it seems possibly that many are parasitoids or parasites. In the future, the systematic application of both genomics and multigene molecular phylogenetic studies should help resolve many of the unresolved evolutionary questions both within oomycetes and to their closest relatives.

References

Adl, S. M., Simpson, A. G. B., Lane, C. E., Lukeš, J., Bass, D., Bowser, S. S., Brown, M. W., Burki, F., Hampl, V., Heiss, A., Hoppenrath, M., Lara, E., Le Gall, L., Lynn, D. H., McManus, H., Mitchell, E. A. D., Mozley-Stanridge, S. E., Parfrey, L. W., Pawlowski, J., Rueckert, S., Shadwick, L., Schoch, C. L., Smirnov, A., & Spiegel, F. W. (2012). A revised classification of eukaryotes. Journal of Eukaryotic Microbiology, 59, 429–493.
Article PubMed PubMed Central Google Scholar
Ali-Shtayeh, M. S., Lim-Ho, C. L., & Dick, M. W. (1986). An improved method and medium for quantitative estimates of populations of Pythium species from soil. Transactions of the British Mycological Society, 86, 39–47.
Article Google Scholar
Andersen, R. A., Barr, D. J. S., Lynn, D. H., Melkonian, M., Moestrup, O., & Sleigh, M. A. (1991). Terminology and nomenclature of the cytoskeletal elements associated with the flagellar/ciliary apparatus in protists. Protoplasma, 164, 1–8.
Article Google Scholar
Arcate, J. M., Karp, M. A., & Nelson, E. B. (2006). Diversity of peronosporomycete (oomycete) communities associated with the rhizosphere of different plant species. Microbial Ecology, 51, 36–50.
Article PubMed Google Scholar
Artemchuk, N. V., & Zelezinskaya, L. M. (1969). The sea fungus Hyphochytrium peniliae n.sp. affecting planktonic crawfish Penilia avirostris (Dana). Mikologiya i Fitopatologiya, 3, 356–358.
Google Scholar
Ayers, W. A., & Lumsden, R. D. (1977). Mycoparasitism of oospores of Pythium and Aphanomyces species by Hyphochytrium catenoides. Canadian Journal of Microbiology, 23, 38–44.
Article Google Scholar
Badreddine, I., Lafitte, C., Heux, L., Skandalis, N., Spanou, Z., Martinez, Y., Esquerré-Tugayé, M.-T., Bulone, V., Dumas, B., & Bottin, A. (2008). Cell wall chitosaccharides are essential components and exposed patterns of the phytopathogenic oomycete Aphanomyces euteiches. Eukaryotic Cell, 7, 1980–1993.
Article CAS PubMed PubMed Central Google Scholar
Bala, K., Robideau, G. P., Levésque, C. A., de Cock, A. W. A. M., Abad, G., Lodhi, A. M., Shazad, S., Ghaffer, A., & Coffey, M. D. (2010). Phytopythium sindham Lodi, Shazad & Levesque sp. Nov. Persoonia, 24, 127–139.
Article Google Scholar
Barr, D. J. S. (1981). The phylogenetic and taxonomic implications of flagellar rootlet morphology among zoosporic fungi. Biosystems, 14, 359–370.
Article CAS PubMed Google Scholar
Barr, D. J. S., & Allan, P. M. E. (1985). A comparison of the flagellar apparatus in Phytophthora, Saprolegnia, Thraustochytrium, and Rhizidiomyces. Canadian Journal of Botany, 63, 138–154.
Article Google Scholar
Barr, D. J. S., & Désaulniers, N. L. (1987). The ultrastructure of Lagena radicola zoospores, including a comparison with the primary and secondary Saprolegnia zoospores. Canadian Journal of Botany, 65, 2161–2176.
Article Google Scholar
Barr, D. J. S., & Désaulniers, N. L. (1989). The flagellar apparatus of the oomycetes and hyphochriomycetes. In J. P. Green, B. S. C. Leadbeater, & W. L. Diver (Eds.), The chromophyte algae: Problems and perspectives (pp. 343–355). Oxford: Clarendon Press.
Google Scholar
Barr, D. J. S., & Désaulniers, N. L. (1990). The life cycle Lagena radicola, an oomycetous parasite of wheat roots. Canadian Journal of Botany, 68, 2112–2118.
Article Google Scholar
Barstow, W. E., Freshour, G. D., & Fuller, M. S. (1989). The ultrastructure of mitosis during zoosporgenesis in Rhizidiomyces apophysatus. Canadian Journal of Botany, 67, 3401–3409.
Article Google Scholar
Bartinicki-Garcia, S. (1970). Cell wall composition and other biochemical markers in fungal phylogeny. In J. G. Harborne (Ed.), Phytochemical phylogeny (pp. 81–103). Academic: New York.
Google Scholar
Bartnick-Garcia, S., & Wang, M. C. (1983). Biochemical aspects of morphogenesis in Phytophthora. In D. C. Erwin, S.Bartnicki-Garcia, & P. H. Tsoa (Eds.), Phytophthora. Its biology,taxonomy, ecology and pathology (pp. 121–137). St Paul: American Phytopathological Society.
Google Scholar
Bartnicki-Garcia, S. (1996). The hypha: The unifying thread of the fungal kingdom. In B. C. Sutton (Ed.), A century of mycology (pp. 105–133). Cambridge: Cambridge University Press.
Google Scholar
Baxter, L., Tripathy, S., Ishaque, N., Boot, N., Cabral, A., Kemen, E., Thines, M., Ah-Fong, A., Anderson, R., Badejoko, W., Bittner-Eddy, P., Boore, J. L., Chibucos, M. C., Coates, M., Dehal, P., Delehaunty, K., Dong, S., Downton, P., Dumas, B., Fabro, G., Fronick, C., Fuerstenberg, S. I., Fulton, L., Gaulin, E., Govers, F., Hughes, L., Humphray, S., Jiang, R. H., Judelson, H., Kamoun, S., Kyung, K., Meijer, H., Minx, P., Morris, P., Nelson, J., Phuntumart, V., Qutob, D., Rehmany, A., Rougon-Cardoso, A., Ryden, P., Torto-Alalibo, T., Studholme, D., Wang, Y., Win, J., Wood, J., Clifton, S. W., Rogers, J., Van den Ackerveken, G., Jones, J. D., McDowell, J. M., Beynon, J., & Tyler, B. M. (2010). Signatures of adaptation to obligate biotrophy in the Hyaloperonospora genome. Science, 330, 1549–1551.
Article CAS PubMed PubMed Central Google Scholar
Beakes, G. W. (1980a). Electron microscopic study of oospore maturation and germination in an emasculate isolate of Saprolegnia ferax. 3. Changes in organelle status and associations. Canadian Journal of Botany, 58, 209–227.
Article Google Scholar
Beakes, G. W. (1980b). Electron microscopic study of oospore maturation and gemination in an emasculate isolate of Saprolegnia ferax. 4. Nuclear cytology. Canadian Journal of Botany, 58, 228–240.
Article Google Scholar
Beakes, G. W. (1980c). Ultrastructure of the phycomycete nucleus. In S. Oliver & K. Gull (Eds.), The fungal nucleus (pp. 1–35). Cambridge: Cambridge University Press.
Google Scholar
Beakes, G. W. (1981). Ultrastructural aspects of oospore differentiation. In H. Hohl & G. Turian (Eds.), The fungal spore: Morphogenetic controls (pp. 71–94). London/New York: Academic Press.
Google Scholar
Beakes, G. W. (1983). A comparative account of cyst coat ontogeny in saprophytic and fish-lesion isolates (pathogenic) of the Saprolegnia diclina-parasitica complex. Canadian Journal of Botany, 61, 603–625.
Article Google Scholar
Beakes, G. W. (1987). Oomycete phylogeny: Ultrastructural perspectives. In A. D. M. Rayner, C. M. Brasier, & D. Moore (Eds.), Evolutionary biology of the fungi (pp. 405–421). Cambridge: Cambridge University Press.
Google Scholar
Beakes, G. W. (1989). Oomycete fungi: Their phylogeny and relationship to chromophyte algae. In J. C. Green & B. S. C. Leadbeater (Eds.), The chromophyte algae: Problems and perspectives (pp. 325–342). Oxford: Clarendon Press.
Google Scholar
Beakes, G. W. (1994). Sporulation of lower fungi. In N. A. R. Gow & G. M. Gadd (Eds.), The growing fungus (pp. 337–366). London: Chapman and Hall.
Google Scholar
Beakes, G. W., & Bartnicki-Garcia, S. (1989). Ultrastructure of mature oogonium-oospore wall complexes in Phytophthora megasperma: A comparison of in vivo and in vitro dissolution of the oospore wall. Mycological Research, 93, 321–234.
Article Google Scholar
Beakes, G. W., & Gay, J. L. (1977). Gametangial nuclear division and fertilization in Saprolegnia furcata as observed by light and electron microscopy. Transactions of the British Mycological Society, 69, 459–471.
Article Google Scholar
Beakes, G. W., & Gay, J. L. (1978a). A light and electron microscopic study of oospore maturation in Saprolegnia furcata 1. Cytoplasmic changes. Transactions of the British Mycological Society, 71, 11–24.
Article Google Scholar
Beakes, G. W., & Gay, J. L. (1978b). A light and electron microscopic study of oospore maturation in Saprolegnia furcata 2. Wall changes. Transactions of the British Mycological Society, 71, 25–35.
Article Google Scholar
Beakes, G. W., & Glockling, S. L. (1998). Injection tube differentiation in gun cells of a Haptoglossa species which infects nematodes. Fungal Genetics and Biology, 24, 45–68.
Article CAS PubMed Google Scholar
Beakes, G. W., & Glockling, S. L. (2000). An ultrastructural analysis of organelle arrangement during gun (infection) cell differentiation in the nematode parasite Haptoglossa dickii. Mycological Research, 104, 1258–1269.
Article Google Scholar
Beakes, G. W., & Glockling, S. L. (2002). A comparative fine-structural study of dimorphic infection cells in the nematophagous parasite, Haptoglossa erumpens. Fungal Genetics and Biology, 37, 250–262.
Article PubMed Google Scholar
Beakes, G. W., & Sekimoto, S. (2009). The evolutionary phylogeny of oomycetes – Insights gained from studies of holocarpic parasites of algae and invertebrates. In K. Lamour & S. Kamoun (Eds.), Oomycete genetics and genomics: Diversity, interactions and research tools (pp. 1–24). New York: Wiley.
Google Scholar
Beakes, G. W., Singh, H., & Dickinson, C. H. (1982). Ultrastructure of the host-pathogen interface of Peronospora viciae in cultivars of pea which show different susceptibilities. Plant Pathology, 31, 343–354.
Article Google Scholar
Beakes, G. W., El-Hamalawi, Z. A., & Erwin, D. C. (1986). Ultrastructure of mature oospores of Phytophthora megasperma f.sp. medicaginis: Preparation protocols and effects of MTT vital staining and permanganate pre-treatment. Transactions of the British Mycological Society, 86, 195–206.
Article Google Scholar
Beakes, G. W., Glockling, S. L., & James, T. Y. (2006). The diversity of oomycete pathogens of nematodes and its implications to our understanding of oomycete phylogeny. In W. Meyer & C. Pearce (Eds.), Proceedings 8th international mycological congress (pp. 7–12). Bologna: Medimond.
Google Scholar
Beakes, G. W., Glockling, S. L., & Sekimoto, S. (2012). The evolutionary phylogeny of the oomycete “fungi”. Protoplasma, 249, 3–19.
Article PubMed Google Scholar
Beakes, G. W., Honda, D., & Thines, M. (2014a). Systematics of the Straminipila: Labyrinthulomycota, Hyphochytriomycota, and Oomycota. In D. J. McLaughlin & J. W. Spatafora (Eds.), The mycota VII Part A. Systematics and evolution (2nd ed., pp. 39–97). Springer: Berlin/Heidelberg.
Google Scholar
Beakes, G. W., Glockling, S. L., & James, T. Y. (2014b). A new oomycete species parasitic in nematodes, Chlamydomyzium dictyuchoides sp. nov.: Developmental biology and phylogenetic studies. Fungal Biology, 118, 527–543.
Article PubMed Google Scholar
Bedard, J. E. J., Schurko, A. M., de Cock, A. W. A. M., & Klassen, G. R. (2006). Diversity and evolution of 5S rRNA gene family and organization in Pythium. Mycological Research, 110, 86–95.
Article CAS PubMed Google Scholar
Berkeley, M. J. (1846). Observations, botanical and physiological on the potato murein. Journal of the Horticultural Society of London, 1, 9–34.
Google Scholar
Bessey, E. A. (1942). Some problems in fungus phylogeny. Mycologia, 34, 355–376.
Article Google Scholar
Bhattacharya, D., Yoon, H. S., Hedges, S. B., & Hackett, D. (2009). Eukaryotes. In S. B. Hedges & S. Kumar (Eds.), The timetree of life (pp. 116–120). New York: Oxford University Press.
Google Scholar
Blair, J. E., Coffey, M. D., Park, S.-Y., Geiser, D. M., & Kang, S. (2008). A multi-locus phylogeny for Phytophthora utilizing markers derived from complete genome sequences. Fungal Genetics and Biology, 45, 266–277.
Article CAS PubMed Google Scholar
Bock, C. H., Jeger, M. J., Mughogho, L. K., Cardwell, K. F., Mtisi, E., Kaula, G., & Mukansabimana, D. (2000). Variability of Peronoscleropsora sorghi isolates from different geographic locations and hosts in Africa. Mycological Research, 104, 61–68.
Article Google Scholar
Bortnick, R. N., Powell, M. J., & Bangert, T. N. (1985). Zoospore fine-structure of the parasite Olpidiopsis saprolegniae (Oomycetes, Lagenidiales). Mycologia, 77, 861–879.
Article Google Scholar
Briard, M., Dutertre, M., Rouxel, F., & Brygoo, Y. (1995). Ribosomal DNA sequence divergence within the Pythiaceae. Mycological Research, 99, 1119–1127.
Article CAS Google Scholar
Brouwer, H., Govers, F., Kroon, L. P. N. M., & de Cock, A. W. A. M. (2012). The genus Phytophthora anno 2012. Phytopathology, 102, 348–364.
Article PubMed Google Scholar
Brown, J. W., & Sorhannus, U. (2010). A molecular genetic timescale for the diversification of autotrophic stramenopiles (Ochrophyta): Substantive underestimation of putative fossil ages. PloS One, 5, e12759. doi:10.1371/journal.pone.0012759.
Article PubMed PubMed Central CAS Google Scholar
Bruno, D. W., Wan West, P., & Beakes, G. W. (2011). Saprolegnia. In P. T. K. Woo & D. W. Bruno (Eds.), Fish diseases and disorders, Viral, bacterial and fungal infections (Vol. 3, 2nd ed., pp. 669–720). Wallingford/Oxon: CABI Publishing.
Google Scholar
Burki, F., & Keeling, P. (2014). Rhizaria. Current Biology, 24, R103–R107. doi:10.1016/j.cub.2013.12.025.
Article CAS PubMed Google Scholar
Burki, F., Shalchian-Tabrizi, K., Minge, M., Skjaeveland, A., Nikolaev, S. I., Jakobsen, K. S., & Pawlowski, J. (2007). Phylogenetics reshuffles the eukaryote supergroups. PloS One, 2, e790. doi:10.1371/journal.pone.0000790.
Article PubMed PubMed Central CAS Google Scholar
Burki, F., Shalchian-Tabrizi, K., & Pawlowski, J. (2008). Phylogenomics reveals a new ‘megagroup’ including most photosynthetic eukaryotes. Biology Letters, 4, 366–369.
Article PubMed PubMed Central Google Scholar
Burr, A. W., & Beakes, G. W. (1994). Characterization of zoospore and cyst surface structure in saprophytic and fish pathogenic Saprolegnia species (oomycete fungal protists). Protoplasma, 181, 142–163.
Article Google Scholar
Canter, H. M. (1950). Studies on British chytrids IX. Anisolpidium stigeoclonii (De Wildeman) n. comb. Transactions of the British Mycological Society, 33, 335–344.
Article Google Scholar
Cavalier-Smith, T., & Chao, E. E. Y. (2006). Phylogeny and megasystematics of phagotrophic heterokonts (Kingdom Chromista). Journal of Molecular Evolution, 62, 388–420.
Article CAS PubMed Google Scholar
Cerenius, L., Soderhall, K., Persson, M., & Ajaxon, R. (1988). The crayfish plague fungus Aphanomyces astaci – Diagnosis, isolation and pathobiology. Freshwater Crayfish, 7, 131–144.
Google Scholar
Cheung, F., Win, J., Lang, J. H., Hamilton, J., Vuong, H., Leach, J. F., Kamoun, S., Lévesque, C. A., Tisserat, N., & Bruell, C. R. (2008). Analysis of the Pythium ultimum transcriptome using Sanger and Pyrosequencing approaches. BMC Genomics, 9, 542. doi:10.1186/1471-2164-9-542.
Article PubMed PubMed Central CAS Google Scholar
Choi, S.-Y., & Thines, M. (2015). Host jumps and raditaion, not co-divergence, drives diversification of obligate pathogens. A case study in downy mildews and Asteraceae. PLOS One. doi:10.1371/journal.pone.0133655.
Google Scholar
Choi, Y.-J., Jong, S.-B., & Shin, H.-D. (2005). A reconsideration of Pseudoperonospora cubensis and P. humuli based on molecular and morphological data. Mycological Research, 109, 842–848.
Article CAS Google Scholar
Choi, Y.-J., Jong, S.-B., & Shin, H.-D. (2006). Genetic diversity within the Albugo candida complex (Peronosporales, Oomycota) inferred from phylogenetic analysis of ITS rDNA and COX2 mt DNA sequences. Molecular Phylogenetics and Evolution, 40, 400–409.
Article CAS PubMed Google Scholar
Choi, Y.-J., Shin, H.-D., Hong, S.-B., & Thines, M. (2007). Morphological and molecular descrimination among Albugo candida materials infecting Capsella bursa-pastoris world-wide. Fungal Diversity, 27, 11–34.
Google Scholar
Choi, Y.-J., Shin, H.-D., Ploch, S., & Thines, M. (2008). Evidence for uncharted biodiversity in the Albugo candida complex, with the description of a new species. Mycological Research, 112, 1327–1334.
Article CAS PubMed Google Scholar
Choi, Y.-J., Shin, H.-D., Ploch, S., & Thines, M. (2011). Three new phylogenetic lineages are the closest relatives of the widespread species Albugo candida. Fungal Biology, 115, 598–607.
Article PubMed Google Scholar
Choi, Y.-J., Beakes, G., Glockling, S., Kruse, J., Nam, B., Nigrelli, L., Ploch, S., Shin, H. D., Shivas, R. G., Telle, S., Voglmayr, H., & Thines, M. (2015). Towards a universal barcode of oomycetes - a comparison of cox1 and cox2 loci. Molecular Ecology Resources, 15, 1275–1288.
Article CAS PubMed Google Scholar
Clark, G., & Dick, M. W. (1974). Long-term storage and viability of aquatic oomycetes. Transactions of the British Mycological Society, 63, 611–612.
Article Google Scholar
Clay, R. P., Benhamou, N., & Fuller, M. S. (1991). Ultratructural detection of polysaccharides in the cell walls of two members of the Hyphochytriales. Mycological Research, 95, 1057–1064.
Article CAS Google Scholar
Coffey, M. D. (1975). Ultrastructural features of the haustorial apparatus of the white blister rust Albugo candida. Canadian Journal of Botany, 53, 1285–1299.
Article Google Scholar
Coffey, M. D., & Wilson, U. (1983). An ultrastructural stidy of the late-blight fungus Phytophthora infestans and its itnereaction with the foliage of two potato cultivars prossing different levels of general (field) resistance. Canadian Journal of Botany, 61, 2669–2685.
Article Google Scholar
Coker, W. C. (1923). The saprolegniaceae with notes on other water molds. Chapel Hill: University of North Carolina Press.
Book Google Scholar
Constantinescu, O. (1991). An annotated list of Peronospora names. Thumbergia, 15, 1–110.
Google Scholar
Contantinescu, O., & Fatehi, J. (2002). Peronospora-like fungi (Chromista, Peronosporales) parasitic on Brassicaceae and related hosts. Nova Hedwigia, 74, 291–338.
Article Google Scholar
Cook, K. L., Hudspeth, D. S. S., & Hudspeth, M. E. S. (2001). A cox2 phylogeny of representative marine peronosporomycetes (Oomycetes). Nova Hedwigia. Beiheft, 122, 231–243.
Google Scholar
Cooke, D. E. L., Drenth, A., Duncan, J. M., Wagels, G., & Brasier, C. M. (2000). A molecular phylogeny of Phytophthora and related oomycetes. Fungal Genetics and Biology, 30, 17–32.
Article CAS PubMed Google Scholar
Cooney, E. W., Barr, D. J. S., & Barstow, W. E. (1985). The ulstrastructure of the zoospore of Hyphochytrium catenoides. Canadian Journal of Botany, 63, 497–505.
Article Google Scholar
Corda, A. J. K. (1837). Icones Fungorum Hucusque Cognitorum (Vol. 1). Czechoslovakia: Praha.
Google Scholar
Cornu, M. (1872). Monographie des Saprolegniales. Etude physiolique et systematique. Annales des Sciences Naturelles, Botanique Serie V, 15, 1–198.
Google Scholar
Davidson, J. M., Werres, S., Garbelotto, M., Hansen, E. M., & Rizzo, D. M. (2003). Sudden oak death and associated diseases caused by Phytophthora ramorum. Online Plant Health Progress. doi:10.1094/PHP-2003-0707-01-DG.
Google Scholar
de Bary, A. (1876). Researches into the nature of the potato-fungus - Phytophthora infestans. Journal of the Royal Agricultural Society of England, 12, 239–269.
Google Scholar
de Bary, A. (1881). Untersuchungen über die Peronsporeen und Saprolegnieen und der Grundlagen eins natürlichen Systems der Pilz. Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft, 12, 225–370.
Google Scholar
de Cock, A.W.A.M., Abad, G., Lévesque, A., Robideau, G., & Brouwer, H. (2012). Pythium: Morphological taxonomy after the molecular revision. www.phytopthoradb.org/pdf/O31DeCock.pdf.
de Cock, A. W. A. M., Lodhi, A. M., Rintoul, T. L., Bala, K., Robideau, G. P., Abad, Z. G., Coffey, M. D., Shahzad, S., & Lévesque, C. A. (2015). Phytopythium: Molecular phylogeny and systematics. Persoonia, 34, 35–39.
Google Scholar
de Grooters, A. M., Spies, C. F. J., Chen, C., Glockling, S. L., Lévesque, A., & de Cock, A. W. A. M. (2013). Nomenclature novelites. Index Fungorum, 34, 1.
Google Scholar
Derevima, L., Chin-Wo-Reyes, S., Martin, F., Wood, K., Froenicke, L., Spring, O., & Michelmore, R. (2015). Genome sequence and architecture of the tobacco downy mildew pathogen Peronospora tabacina. Molecular Plant-Microbe Interactions, 11, 1198–1215.
Article CAS Google Scholar
Dick, M. W. (1969). Morphology and taxonomy of the Oomycetes, with special reference to Saprolegniaceae, Leptomitaceae and Pythiaceae I. Sexual reproduction. New Phytologist, 68, 751–755.
Article Google Scholar
Dick, M. W. (1972). Morphology and taxonomy of the Oomycetes, with special reference to Saprolegniaceae, Leptomitaceae, and Pythiaceae II. Cytogenetic systems. New Phytologist, 71, 1151–1159.
Article Google Scholar
Dick, M. W. (1973a). Leptomitales. In C. G. Ainsworth, F. K. Sparrow, & A. L. Sussman (Eds.), The fungi, an adanced treatise (Vol. IVb, pp. 145–158). New York: Academic.
Google Scholar
Dick, M. W. (1973b). Saprolegniales. In C. G. Ainsworth, F. K. Sparrow, & A. L. Sussman (Eds.), The fungi, an adanced treatise (Vol. IVb, pp. 113–144). New York: Academic.
Google Scholar
Dick, M. W. (1976). The ecology of aquatic phycomycetes. In E. B. G. Jones (Ed.), Recent advances in aquatic mycology (pp. 513–542). London: Elek Press.
Google Scholar
Dick, M.W. (1990). Phylum Oomycota. In Margulis, L. Corliss, J.O Melkonian M., Chapman D. (eds) Handbook of protoctista. pp. 661–685. Boston, Jones and Bartlett.
Google Scholar
Dick, M. W. (1995). Sexual reproduction in the Peronosporomycetes (chromistan fungi). Canadian Journal of Botany, 73(Supplement 1), S712–S724.
Article Google Scholar
Dick, M. W. (1997). The Myzocytiopsidaceae. Mycological Research, 101, 878–882.
Article Google Scholar
Dick, M. W. (1998). The species and systematic position of Crypticola in the Peronosporomycetes, and new names for the genus Halocrusticida and species therein. Mycological Research, 102, 1062–1066.
Article Google Scholar
Dick, M. W. (2001). Straminipilous fungi (p. 670). Dordrecht: Kluwer.
Book Google Scholar
Dick, M. W., & Ali-Shtayeh, M. S. (1986). Distribution and frequency of Pythium species in parkland and farmland soils. Transactions of the British Mycological Society, 86, 49–62.
Article Google Scholar
Dick, M. W., & Win-Tin. (1973). The development of cytological theory in the Oomycetes. Biological Reviews, 48, 133–158.
Google Scholar
Dick, M. W., Wong, P. T. W., & Clark, G. (1984). The identity of the oomycete causing “Kikuyu Yellows”, with a reclassification of the downy mildews. Botanical Journal of the Linnean Society, 89, 171–197.
Article Google Scholar
Dick, M. W., Croft, B. J., Magary, R. C., de Cock, A. W. A. M., & Clark, G. (1988). A new genus of the Verrucalvaceae (Oomycetes). Botanical Journal of the Linnean Society, 99, 97–113.
Article Google Scholar
Dick, M. W., Vick, M. C., Gibbings, J. G., Hedderson, T. A., & Lopez Lastra, C. C. (1999). 18S rDNA for species of Leptolegnia and other Peronosporomycetes: Justification of the subclass taxa Saprolegniomycetidae and Peronosporomycetidae and division of the Saprolegniaceae sensu lato into the Leptolegniaceae and Saprolegniaceae. Mycological Research, 103, 1119–1125.
Article CAS Google Scholar
Diéguez-Uribeondo, J., Fregeneda-Grandes, J. M., Cerenius, L., Perez-Iniesta, M., Aller-Gancedo, J. M., Tellerıa, M. T., Soderhall, K., & Martın, M. P. (2007). Re-evaluation of the enigmatic species complex Saprolegnia diclina–Saprolegnia parasitica based on morphological, physiological and molecular data. Fungal Genetics and Biology, 44, 585–601.
Article PubMed CAS Google Scholar
Diéguez-Uribeondo, J., Garcia, M. A., Cerenius, L., Kozubikova, E., Ballesteros, I., Windels, C., Weiland, J., Kator, H., Soderhall, K., & Martın, M. P. (2009). Phylogenetic relationships among plant and animal parasites, and saprotrophs in Aphanomyces (Oomcyetes). Fungal Genetics and Biology, 46, 365–376.
Article PubMed CAS Google Scholar
Diéz, B., Pedrós-Alió, C., & Massana, R. (2001). Study of genetic diversity of eukaryotic picoplankton in different oceanic regions by small-subunit rRNA gene cloning and sequencing. Applied and Environmental Microbiology, 67, 2932–2941.
Article PubMed PubMed Central Google Scholar
Domergue, F., Abbadi, A., & Heinz, E. (2005). Relief for fish stocks: Oceanic fatty acids in transgenic oilseeds synthesis. Trends in Plant Science, 10, 112–116.
Article CAS PubMed Google Scholar
Dorrell, R. G., & Smith, A. G. (2011). Do red and green make brown? Perspectives on plastid acquisitions within Chromalveolates. Eukaryotic Cell, 10, 856–868.
Article CAS PubMed PubMed Central Google Scholar
Duffey, M. A., James, T. Y., & Longworth, A. (2015). Ecology, virulence, and phylogeny of Blastulidium paedophthorum, a widespread brood parasite of Daphnia sp. Applied and Environmental Microbiology, 81, 5486–5496.
Article CAS Google Scholar
Duncan, J. M. (1990). Phytophthora species attacking strawberry and raspberry. EPPO Bulletin, 20, 107–115.
Article Google Scholar
Edgerton, B.F., Henttonen, P., Jussila, J., Mannonen,A., Paasonen, P, Taugbil, T., Edsman, L., & Souty-Grosset, C. (2004). Understanding the cause of disease in European freshwater crayfish. Conservation Biology 18 1466–1474.
Google Scholar
Emerson, R., & Natvig, D. O. (1981). Adaptation of fungi to stagnant waters. In D. T. Wicklow & G. C. Carroll (Eds.), The fungal community, its organization and role in the ecosystem (pp. 109–128). New York: Marcel Dekker.
Google Scholar
Erwin, D. C., & Ribeiro, O. K. (1998). Phytophthora diseases worldwide (p. 592). St Paul: The American Phytopathological Society.
Google Scholar
Fletcher, K., Zuljevic, A., Tsirigoti, A., Antolic, B., Katsaros, C., Nikolic, V., van West, P., & Küpper, F. (2015). New record and phylogenetic affinities of the oomycete Olpidiopsis feldmanni infecting Asparagopsis sp. (Rhodophyta). Diseases of Aquatic Organisms, 117, 45–57.
Article PubMed Google Scholar
Förster, H., Coffey, M. D., Elwood, H., & Sogin, M. L. (1990). Sequence analysis of the small ribosomal subunit RNAs of three zoosporic fungi and implications for fungal evolution. Mycologia, 82, 306–312.
Article Google Scholar
Förster, H., Cummings, M. P., & Coffey, M. D. (2000). Phylogenetic relationships of Phytophthora species based on ribosomal ITS I DNA sequence analysis with emphasis on Waterhouse groups V and VI. Mycological Research, 104, 1055–1061.
Article Google Scholar
Frances, S. P., Sweeney, A. W., & Humber, R. A. (1989). Crypticola clavulifera gen. et sp. nov and Lagenidium giganteum: Oomycetes pathogenic for dipterans infesting leaf axils in Australian rain forest. Journal of Invertebrate Pathology, 54, 103–111.
Article CAS PubMed Google Scholar
Fuller, M. S. (1960). Biochemical and microchemical study of the cell walls of Rhizidiomyces sp. American Journal of Botany, 47, 838–842.
Article CAS Google Scholar
Fuller, M. S. (1966). The flagellated fungal spore. In M. F. Madelin (Ed.), The fungus spore (pp. 67–84). London: Butterworths.
Google Scholar
Fuller, M. S. (1990). Phylum Hyphochytriomycota. In L. Margulis, J. O. Corliss, M. Melkonian, & D. J. Chapman (Eds.), Handbook of Protoctista (pp. 380–387). New York: Jones and Bartlett.
Google Scholar
Fuller, M. S. (2001). Hyphochytriomycota. In D. McLaughlin, E. McLaughlin, & C. A. Lemke (Eds.), The mycota VII Part A. Systematics and evolution (pp. 74–80). Berlin: Springer.
Google Scholar
Fuller, M. S., & Jaworski, A. (Eds.). (1987). Zoosporic fungi in teaching and research. Athens: Southeastern Publishing Corporation.
Google Scholar
Fuller, M. S., & Reichle, R. (1965). The zoospore and early development of Rhizidiomyces apophysatus. Mycologia, 57, 946–961.
Article Google Scholar
Gachon, C. M. M., Fletcher, K. I., Badis, Y., van West, P., & Muller, D. G. (2015). The pathogens of brown algae Anisolpidium ectocarpii and Anisolpidium rosenvingei define a new class marine anteriorly uniciliate oomycetes. European Journal of Phycology, 50, 25–26 (abstract).
Google Scholar
García-Blázquez, G., Göker, M., Voglmayr, H., Martin, M. P., Telleria, M. T., & Oberwinkler, F. (2008). Phylogeny of Peronospora parasitic on Fabaceae, based on ITS sequences. Mycological Research, 112, 502–512.
Article PubMed CAS Google Scholar
Gaulin, E., Jacquet, C., Bottin, A., & Dumas, B. (2007). Root rot disease of legumes caused by Aphanomyces euteiches. Molecular Plant Pathology, 8, 539–548.
Article PubMed Google Scholar
Gay, J. L., & Greenwood, A. D. (1966). Structural aspects of zoospore production in Saprolegnia ferax with particular reference to the cell and vacuolar membranes. In M. F. Madelin (Ed.), The fungus spore (pp. 95–100). London: Butterworths.
Google Scholar
Gleason, F. (1976). The physiology of lower freshwater fungi. In E. B. G. Jones (Ed.), Recent advances in aquatic mycology (pp. 543–572). London: Elek Press.
Google Scholar
Gleason, F. H., Letcher, P. M., Evershed, N., & McGee, P. A. (2009). Recovery of growth of Hyphochytrium catenoides after exposure to environmental stess. Journal of Eukaryotic Microbiology, 55, 351–354.
Article Google Scholar
Glockling, S. L., & Beakes, G. W. (2000a). A review of the biology and infection strategies of biflagellate zoosporic parasites of nematodes. Fungal Diversity, 4, 1–20.
Google Scholar
Glockling, S. L., & Beakes, G. W. (2000b). An ultrastructural study of sporidium formation during infection of a rhabditid nematode by large gun cells of Haptoglossa heteromorpha. Journal of Invertebrate Pathology, 76, 208–215.
Article CAS PubMed Google Scholar
Glockling, S. L., & Beakes, G. W. (2000c). The ultrastructure of the dimorphic infection cells of Haptoglossa heteromorpha illustrates the developmental plasticity of infection apparatus structures in a nematode parasite. Canadian Journal of Botany, 78, 1095–1107.
Article Google Scholar
Glockling, S. L., & Beakes, G. W. (2006a). An ultrastructural study of development and reproduction in the nematode parasite. Myzocytiopsis vermicola Mycologia, 98, 7–21.
Google Scholar
Glockling, S. L., & Beakes, G. W. (2006b). Structural and developmental studies of Chlamydomyzium oviparasiticum from Rhabditis nematodes in culture. Mycological Research, 110, 1119–1126.
Article PubMed Google Scholar
Gmelin, J. F. (1792). Caroli a Linné, Systema Naturae per Regna Tria Naturae, Secundum Classes, Ordines, Genera, Species, cum Characteribus, Differentiis, Synonymis, Locis, 2.
Google Scholar
Göker, M., Voglmayr, H., Riethmüller, A., Weiß, M., & Oberwinkler, F. (2003). Taxonomic aspects of Peronosporaceae inferred from Bayesian molecular phylogenetics. Canadian Journal of Botany, 81, 672–683.
Article Google Scholar
Göker, M., Riethmüller, A., Voglmayr, H., Weiss, M., & Oberwinkler, F. (2004). Phylogeny of Hyaloperonospora based on nuclear ribosomal internal transcribed spacer sequences. Mycological Progress, 3, 83–94.
Article Google Scholar
Göker, M., Voglmayr, H., Riethmüller, A., & Oberwinkler, F. (2007). How do obligate parasites evolve? A multi-gene phylogenetic analysis of downy mildews. Fungal Genetics and Biology, 44, 105–122.
Article PubMed CAS Google Scholar
Gotelli, D. (1974). The morphology of Lagenidium callinectes II. Zoosporogenesis. Mycologia, 66, 846–858.
Article Google Scholar
Grenville-Briggs, L., Gachon, C. M., Strittmater, M., Sterck, L., Kupper, F. C., & van West, P. (2011). A molecular insight into algal-oomycete warfare: cDNA analysis of Ectocarpus siliculosus infected with the basal oomycete Eurychasma dicksonii. PloS One, 6, e24500.
Article CAS PubMed PubMed Central Google Scholar
Gubler, F., & Hardham, A. R. (1988). Secretion of adhesive material during encystement of Phytophthora cinnamomi zoospores characterized by immunogold labeling with monoclonal antibodies to components of peripheral vescicles. Journal of Cell Science, 90, 225–235.
Google Scholar
Gubler, F., Hardham, A. R., & Duniec, J. (1990). Characterizing adhesiveness of Phytophthora cinnamomi zoospores during encystment. Protoplasma, 149, 24–30.
Article Google Scholar
Gunderson, J. H., Elwood, H., Ingold, A., Kindle, K., & Sogin, M. (1987). Phylogenetic relationships between chlorophytes, chrysophytes and oomycetes. Proceedings of the National Academy of Sciences of the United States of America, 84, 5823–5827.
Article CAS PubMed PubMed Central Google Scholar
Haas, B. J., Kamoun, S., Zody, M. C., Jiang, R. H. Y., Handsaker, R. E., Cano, L. M., Grabherr, M., Kodira, C. D., Raffaele, S., Torto-Alalibo, T., Bozkurt, T. O., Ah-Fong, A. M. V., Alvarado, L., Anderson, V. L., Armstrong, M. R., Avrova, A., Baxter, L., Beynon, J., Boevink, P. C., Bollmann, S. R., Bos, J. I. B., Bulone, V., Cai, G., Cakir, C., Carrington, J. C., Chawner, M., Conti, L., Costanzo, S., Ewan, R., Fahlgren, N., Fischbach, M. A., Fugelstad, J., Gilroy, E. M., Gnerre, S., Green, P. J., Grenville-Briggs, L. J., Griffith, J., Grünwald, N. J., Horn, K., Horner, N. R., Hu, C.-H., Huitema, E., Jeong, D.-H., Jones, A. M. E., Jones, J. D. G., Jones, R. W., Karlsson, E. K., Kunjeti, S. G., Lamour, K., Liu, Z., Ma, L. J., MacLean, D., Chibucos, M. C., McDonald, H., McWalters, J., Meijer, H. J. G., Morgan, W., Morris, P. F., Munro, C. A., O’Neill, K., Ospina-Giraldo, M., Pinzón, A., Pritchard, L., Ramsahoye, B., Ren, Q., Restrepo, S., Roy, S., Sadanandom, A., Savidor, A., Schornack, S., Schwartz, D. C., Schumann, U. D., Schwessinger, B., Seyer, L., Sharpe, T., Silvar, C., Song, J., Studholme, D. J., Sykes, S., Thines, M., van de Vondervoor, P. J. I., Phuntumart, V., Wawra, S., Weide, R., Win, J., Young, C., Zho, S., Fry, W., Meyers, B. C., van West, P., Ristaino, J., Govers, F., Birch, P. R. J., Whisson, S. C., Judelson, H. S., & Nusbaum, C. (2009). Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature, 461, 393–398.
Article CAS PubMed Google Scholar
Hakariya, M., Masuyama, N., & Saikawa, M. (2002). Shooting of sporidium by “gun” cells in Haptoglossa heterospora and H. zoospora and secondary zoospore formation in H. zoospora. Mycoscience, 43, 119–125.
Article Google Scholar
Hakariya, M., Hirose, D., & Tokumasu, S. (2007). A molecular phylogeny of Haptoglossa species, terrestrial peronosporomycetes (oomycetes) endoparasitic on nematodes. Mycoscience, 48, 169–175.
Article CAS Google Scholar
Hardham, A. R. (1987). Microtubules and the flagellar apparatus in zoospores and cysts of the fungus Phytophthora cinnamomi. Protoplasma, 137, 109–124.
Article Google Scholar
Hatai, K. (2012). Diseases of fish and shellfish caused by marine fungi. In C. Raghukumar (Ed.), Biology of marine fungi (pp. 15–52). Berlin/Heidelberg: Springer-Verlag.
Chapter Google Scholar
Hatai, K., Bian, B. Z., Baticados, M. C. L., & Egusa, S. (1980). Studies on the fungal diseases in crustaceans. II Haliphthoros phillippinensis sp. nov. isolated from cultivated larvae of the jumbo tiger prawn (Penaseus monodon). Transactions of the Mycological Society of Japan, 21, 47–55.
Google Scholar
Hatai, K., Rhoobunjongde, W., & Wada, S. (1992). Haliphthoros milfordensis isolated from gills of juvenile kuruma prawn (Penaeus japonicus) with black gill disease. Transactions of the Mycological Society of Japan, 33, 185–192.
Google Scholar
Hausner, G., Belkhiri, A., & Klassen, G. R. (2000). Phylogenetic analysis of the small ribosomal subunit RNA gene of the hyphochytrid Rhizidiomyces apophysatus. Canadian Journal of Botany, 78, 124–128.
CAS Google Scholar
Heath, I. B., & Greenwood, A. D. (1970a). Centriole replication and nuclear division in Saprolegnia. Journal of General Microbiology, 62, 139–289.
Article Google Scholar
Heath, I. B., & Greenwood, A. D. (1970b). Wall formation in the Saprolegniales II. Formation of cysts by the zoospores of Saprolegnia and Dictyuchus. Archives für Mikrobiologie, 75, 67–79.
Article Google Scholar
Heller, A., & Thines, M. (2009). Evidence for the importance of enzymatic digestion of epidermal walls during subepidermal sporulation and pustule opening in white blister rusts (Albuginaceae). Mycological Research, 113, 657–667.
Article PubMed Google Scholar
Hemmes, D. E. (1983). Cytology of Phytophthora. In D. C. Erwin, S. Bartnicki-Garcia, & P. H. Tsoa (Eds.), Phytophthora: Its biology, taxonomy, ecology and pathology (pp. 9–40). St Paul: The American Phytopathological Society.
Google Scholar
Hemmes, D. E., & Bartnick-García, S. (1975). Electron microscopy of gametangial interaction and oospore development in Phytophthora capsici. Archives of Microbiology, 103, 91–112.
Article Google Scholar
Hemmes, D. E., & Hohl, H. R. (1973). Mitosis and nuclear degeneration: Simultaneous events during secondary sporangia formation in Phytophthora palmivora. Canadian Journal of Botany, 51, 1671–1675.
Article Google Scholar
Heuhauser, S., Bulman, S., & Kirschmair, M. (2010). Plasmodiophorids: The challenge to understand soil-borne, obligate biotrophs with multiphasic life cycle. In Y. Gherbawy & K. Voight (Eds.), Molecular identification of fungi (pp. 51–78). Berlin: Springer-Verlag.
Chapter Google Scholar
Hickey, E. L., & Coffey, M. D. (1977). A fine-structural study of the pea downy mildew fungus, Peronspora pisi in its host Pisum sativum. Canadian Journal of Botany, 55, 2845–2858.
Article Google Scholar
Hickey, E. L., & Coffey, M. D. (1978). A cyto-chemical investigation of the host-parasite interface in Pisum sativum infected by the downy mildew fungus Peronospora pisi. Protoplasma, 97, 201–220.
Article Google Scholar
Ho, H. H., & Jong, S. C. (1990). Halophytophthora gen. nov., a new member of the family Pythiaceae. Mycotaxon, 19, 377–382.
Google Scholar
Ho, H. H., Nakagiri, A., & Newell, S. Y. (1992). A new speceies of Halophytophthora form Atlantic and Pacific subtropical islands. Mycologia, 84, 548–554.
Article Google Scholar
Hoch, H. C., & Mitchell, J. E. (1972). A continuous flow system for inducing and observing asexual spore formation in Aphanomyces euteiches. Canadian Journal of Botany, 50, 681–682.
Article Google Scholar
Hohl, H. R., & Hammamoto, S. T. (1967). Ultrastructural changes during zoospore formation in Phytophthora parasitica. American Journal of Botany, 54, 1131–1139.
Article CAS PubMed Google Scholar
Holloway, S. A., & Heath, I. B. (1977a). An ultrastructural analysis of the changes in organelle arrangement and structure between the various spore types of Saprolegnia. Canadian Journal of Botany, 55, 1328–1339.
Article Google Scholar
Holloway, S. A., & Heath, I. B. (1977b). Morphogenesis and the role of microtubules in synchronous populations of Saprolegnia zoospores. Experimental Mycology, 1, 9–29.
Article Google Scholar
Howard, K. L., & Moore, R. T. (1970). Ultrastructure of oogenesis in Saprolegnia terrestris. Botanical Gazette, 131, 311–336.
Article Google Scholar
Huang, J.-H., Chen, C.-Y., Lin, Y.-H., Ann, P.-J., Huang, H.-C., & Chung, W.-H. (2012). Six new species of Pythiogeton in Taiwan, with an account of the molecular phylogeny of this genus. Mycoscience, 54, 130–147.
Article Google Scholar
Hudspeth, D. S. S., Nadler, S. A., & Hudspeth, M. E. S. (2000). A cox II molecular phylogeny of the Peronosporomycetes. Mycologia, 92, 674–684.
Article CAS Google Scholar
Hudspeth, D. S. S., Stenger, D., & Hudspeth, M. E. S. (2003). A cox2 phylogenetic hyphothesis for the downy mildews and white rusts. Fungal Diversity, 13, 47–57.
Google Scholar
Hughes, G. C. (1994). Saprolegniasis: Then and now. A retrospective. In G. J. Mueller (Ed.), Salmon Saprolegniasis (pp. 8–21). Portland Oregon: US Department of Energy, Bonneville Power Administration.
Google Scholar
Huizar, H. E., & Aronson, J. M. (1986). Aspects of cellulin deposition and chitin biosynthesis in the Leptomitaceae. Mycologia, 78, 489–492.
Article CAS Google Scholar
Hulvey, J. P., Padgett, D. E., & Bailey, J. C. (2007). Species boundaries within the Saprolegnia (Saprolegniales, Oomycota) based on morphological and DNA sequence data. Mycologia, 99, 421–429.
Article CAS PubMed Google Scholar
Hulvey, J. P., Telle, S., Nigrelli, L., Lamour, K., & Thines, M. (2010). Salisapiliaceae – A new family of oomycetes from marsh grasss litter of southeastern North America. Persoonia, 25, 109–116.
Article CAS PubMed PubMed Central Google Scholar
Hyde, G. J., Gubler, F., & Hardham, A. R. (1991a). Ultrastructure of zoosporogenesis in Phytophthora cinnamomi. Mycological Research, 95, 577–591.
Article Google Scholar
Hyde, G. J., Lancelle, S. A., Hepler, P. A., & Hardham, A. R. (1991b). Freeze substitution reveals a new model for sporangial cleavage in Phytophthora, a result with implications for cytokinesis in other eukaryotes. Journal of Cell Science, 100, 735–746.
PubMed Google Scholar
Inaba S., & Hariyama, S. (2006).The phylogenetic studies on the genus Cornumyces (Oomycetes) based on the nucleotide sequences of the nuclear large subunit ribosomal RNA and the mitochondrially-encoded cox2 genes. 8th International Mycological Congress Handbook and Abstracts (p. 330) Cairns: IMC.
Google Scholar
Inaba, S., & Tokumasu, S. (2002). Phylogenetic relationships between the genus Saprolegnia and related genera inferred from ITS sequences. Abstracts 7th International Mycological Congress (p. 687). Oslo: IMC7.
Google Scholar
Jee, H.-J., & Ko, W.-H. (1997). Stimulation of sexual reproduction in Phytophthora cactorum and P. parasitica by fatty acids and related compounds. Mycological Research, 101, 1140–1144.
Article CAS Google Scholar
Jiang, R. H. Y., & Tyler, B. M. (2012). Mechanisms and evolution of virulence in oomycetes. Annual Review of Phytopathology, 50, 295–318. doi:10.1146/annrev-phyto-081211-172912.
Article CAS PubMed Google Scholar
Johnson, T. W. (1956). The genus Achlya: Morphology and taxonomy. Ann Arbor: University of Michigan Press.
Google Scholar
Johnson, T. W. (1957). Resting spore development in the marine phycomycete Anisolpidium. American Journal of Botany, 44, 875–878.
Article Google Scholar
Johnson, T.W., Seymour, R.L., & Padgett, D.E. (2002). Biology and systematics of the Saprolegniaceae. http://dl.uncw.edu/digilib/biology/fungi/taxonomy%20and%20systematics/padgett%20book/
Johnson, R. A., Zebrechy, J., Kiryu, Y., & Shields, J. D. (2004). Infection experiments with Aphanomyces invadans in four species of estuarine fish. Journal of Fish Diseases, 27, 287–295.
Article CAS PubMed Google Scholar
Jones, M. D. M., Forn, I., Gadelha, C., Egan, M. J., Bass, D., Massana, R., & Richards, T. A. (2011). Discovery of novel intermediate forms redefines the fungal tree of life. Nature, 474, 200–203.
Article CAS PubMed Google Scholar
Judelson, H. S. (2012). Dynamics and innovations within oomycete genomes: Insights into biology, pathology, and evolution. Eukaryotic Cell, 11, 1304–1324.
Article CAS PubMed PubMed Central Google Scholar
Judelson, H. S., & Ah-Fong, A. M. V. (2009). Progress and challenges in oomcete transformation. In K. Lamour & S. Kamoun (Eds.), Oomycete genetics and genomics: Diversity, interactions and research tools (pp. 435–453). New York: Wiley.
Chapter Google Scholar
Kamoun, S., Furzer, O., Jones, J.D.G., Judelson, H.S., Ali, G.S., Dalio, R.J.D., Roy, S.G., Schena, L., Zambounis, A., Panabières, F., Cahill, D., Ruocco, M., Figueiredo, A., Chen, X.-R.., Hulvey, J., Stam, R., Lamour, K., Gijzem, M., Tyler, B.M., Grüwald, N.J, Mukhtar, M.S., Tomé, F.A., Tör, M., Van den Ackerveken, G., McDowell, J., Daayf, F., Fry, W.E., Lindqvist-Kreuze, H., Meijer, H.J., Petre, B., Ristaino, J., Yoshida, K., Birch, P.R.J., & Govers, F. (2015). The top 10 oomycete pathogens in molecular plant pathology. Molecular Plant Pathology, 16, 413–435.
Google Scholar
Karling, J. S. (1939). A new fungus with anteriorly uniciliate zoosproes: Hyphochytrium catenoides. American Journal of Botany, 26, 512–519.
Article Google Scholar
Karling, J. S. (1942). The simple holocarpic biflagellate phycomycetes. New York: Columbia University Press.
Book Google Scholar
Karling, J. S. (1943). The life history of Anisolpidium ectocarpii gen. nov. et sp. nov., and a synopsis of classification of other fungi with anteriorly flagellate zoospores. American Journal of Botany, 30, 637–648.
Article Google Scholar
Karling, J. S. (1977). Chytridiomycetarum Iconographia (2nd ed.). Vaduz: Cramer.
Google Scholar
Karling, J. S. (1981). Predominantly holocarpic and eucarpic simple biflagellate phycomycetes (2nd ed.). Vaduz: Cramer.
Google Scholar
Keeling, P. J., Burger, G., Dunford, D. G., Lang, B. F., Lee, R. W., Pearlman, R. E., Roger, A. J., & Gray, M. W. (2005). The tree of eukaryotes. Trends in Microbial Ecology, 41, 670–676.
Article Google Scholar
Kemen, E., & Jones, J. D. G. (2012). Obligate biotroph parasitism: Can we link genomes and lifestyles. Trends in Plant Science, 17, 448–457.
Article CAS PubMed Google Scholar
Kemen, E., Gardiner, A., Schultz-Larsen, T., Kemen, A. C., Balmuth, A. L., Robert-Seilaniantz, A., Bailey, K., Holub, E., Studholme, D. J., McLean, D., & Jones, J. D. G. (2011). Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana. PLoS Biology, 9, e1001094. doi:10.1371/journal.pbio.1001094.
Article CAS PubMed PubMed Central Google Scholar
Kenneth, R. G. (1981). Downy mildews of graminaceous crops. In D. M. Spencer (Ed.), The downy mildews (pp. 367–394). London: Academic Press.
Google Scholar
Kerwin, J. L. (2007). Oomycetes: Lagenidium giganteum. Journal of the American Mosquito Control Association, 23, 50–57.
Article PubMed Google Scholar
Kerwin, J. L., & Washino, R. K. (1983). Sterol induction of sexual reproduction in Lagenidium giganteum. Experimental Mycology, 7, 109–115.
Article CAS Google Scholar
Khan, S. R. (1976). Ultrastructural changes in maturing sporangia of Albugo candida. Annals of Botany, 40, 1285–1292.
Article Google Scholar
Khan, S. R. (1977). Light and electron microscopic observations of sporangium formation in Albugo candida (Peronosporales; Oomycetes). Canadian Journal of Botany, 55, 730–739.
Article Google Scholar
Klochkova, T., Shin, Y., Moon, K. H., Motomura, T., & Kim, G. (2015). New species of unicellular obligate parasite, Olpidiopsis pyropiae sp. nov., that plagues Pyropia sea farms in Korea. Journal of Applied Phycology, 27, 1–11.
Article CAS Google Scholar
Ko, W.-H. (1988). Hormonal heterothallism and homothallism in Phytophthora. Annual Review of Phytopathology, 26, 57–74.
Article Google Scholar
Krajaejun, T., Khositnithikul, R., Lerksuthirat, T., Lowhnoo, T., Rujirawat, T., Petchthong, T., Yingyong, W., Suriyaphol, P., Smittipat, N., Juthayothin, T., Phuntumart, V., & Sullivan, T. D. (2011). Expressed sequence tags reveal genetic diversity and putative virulence factors of the pathogenic oomycete Pythium insidiosum. Fungal Biology, 115, 683–696.
Article CAS PubMed Google Scholar
Krings, M., Dotzler, N., Taylor, T. N., & Galtier, J. (2010). A fungal community in plant tissue from the Lower Coal Measures (Langsettian, Lower Pennsylvanian) of Great Britain. Bulletin of Geosciences, 85, 679–690.
Article Google Scholar
Krings, M., Taylor, T. N., & Dotzler, N. (2011). The fossil record of the Peronosporomycetes (Oomycota). Mycologia, 103, 445–457.
Article Google Scholar
Kroon, L. M. M., Bakker, F. T., van den Bosch, G. B. M., Bonants, P. J. M., & Flier, W. G. (2004). Phylogenetic analysis of Phytophthora species based on mitochondrial and nuclear DNA sequences. Fungal Genetics and Biology, 41, 766–782.
Article CAS PubMed Google Scholar
Kühn, S. (1997). Infection of Coscinodiscus spp. by the parasitoid nanoflagellate Pirsonia diadema: I. Behavioural studies on the infection process. Journal of Plankton Research, 19, 791–804.
Article Google Scholar
Kühn, S. F., Medlin, L. K., & Eller, G. (2004). Phylogenetic position of the parasitoid nanoflagellate Pirsonia inferred from nuclear-encoded small subunit ribosomal DNA and a description of Pseudopirsonia n. gen. and Pseudopirsonia mucosa (Drebes) comb. nov. Protist, 155, 143–156.
Article PubMed Google Scholar
Küpper, F. C., & Müller, D. G. (1999). Massive occurrence of the heterokont and fungal parasites Anisolpidium, Eurychasma and Chytridium in Pylaiella litoralis (Ectocarpales, Phaeophyceae). Nova Hedwigia, 69, 381–389.
Google Scholar
Küpper, F. C., Maier, I., Müller, D. G., Loiseaux-de Goer, S., & Guillou, L. (2006). Phylogenetic affinities of two eukaryotic pathogens of marine macroalgae, Eurychasma dicksonii (Wright) Magnus and Chytridium polysiphoniae Cohn. Cryptogamie Algologie, 27, 165–184.
Google Scholar
Lamour, K. H., Win, J., & Kamoun, S. (2007). Oomycete genomics: new insights and future directions. FEMS Microbiology Letters, 274, 1–8.
Article CAS PubMed Google Scholar
Lange, L. L., & Olson, L. W. (1979). The uniflagellate phycomycete zoospore. Dansk Botanisk Arkiv, 33, 1–95.
Google Scholar
Lara, E., & Belbahri, L. (2011). SSU rRNA reveals major trends in oomycete evolution. Fungal Diversity, 49, 93–100.
Article Google Scholar
Lara, E., Moreira, D., & Lόpez-García, P. (2009). The environmental clade LKM11 and Rozella form the deepest branching clade of fungi. Protist, 161, 116–121. doi:10.1016/j.protis.2009.06.005.
Article PubMed CAS Google Scholar
Lebeda, A., & Spencer-Phillips, P. T. N. (Eds.). (2007). Advances in downy mildew research Vol.3. v.o.s. in Kostelec na Hane: Palacky University in Olomouc and JOL.
Google Scholar
Léclerc, M. C., Guillot, J., & Deville, M. (2000). Taxonomic and phylogenetic analysis of Saprolegniaceae (Oomycetes) inferred from LSU rDNA and ITS sequence comparisons. Antonie Van Leeuwenhoek, 77, 369–377.
Article PubMed Google Scholar
Lehnen, L. P., & Powell, M. J. (1989). The role of kinetosome-associated organelles in the attachment of encysting secondary zoospores of Saprolegnia ferax to substrates. Protoplasma, 149, 163–174.
Article Google Scholar
Leipe, D. D., Tong, S. M., Goggin, C. L., Slemenda, S. B., Pieniazek, N. J., & Sogin, M. L. (1994). 16S-like rDNA sequences from Developayella elegans, Labyrinthuloides haliotidis, and Proteromonas lacertae confirm that the stramenopiles are a primarily heterotrophic group. European Journal of Protistology, 33, 369–377.
Google Scholar
Léveillé, J.-H. (1847). Sur la disposition méthodique des Urédinées. Annales des Sciences Naturelles Botanique, Série III 8, 369–376.
Google Scholar
Levenfors, J. P., & Fatehi, J. (2004). Molecular characterization of Aphanomyces species associated with legumes. Mycological Research, 108, 682–689.
Article CAS PubMed Google Scholar
Lévesque, C. A., & de Cock, A. W. (2004). Molecular phylogeny and taxonomy of the genus Pythium. Mycological Research, 108, 1363–1383.
Article PubMed CAS Google Scholar
Lévesque, C.A., Brouwer, H., Cano, L., Hamilton, J.P., Holt, C., Huitema, E., Raffaele, S., Robideau, G.P., Thines, M., Win, J., Zerillo, M.M., Beakes, G.W., Boore, J.L., Busam, D., Dumas, B., Ferriera, S., Furstenberg, S.I., Gachon, C.M.M., Gaulin, E., Govers, F., Grenville-Briggs, L., Horner, N., Hostetle,, J., Jiang, R.H.Y., Johnson, J., Krajaejun, T., Lin, H., Meijer, H.J.G., Moore, B., Morris, P., Phuntmart, V., Puiu, D., Shetty, J., Stajich, J.E., Tripathy, S., Wawra S., van West, P., Whitty, B.R., Coutinho, P.M., Henrissat, B., Martin, F., Thomas, P.D., Tyler, B.M., De Vries, R.P., Kamoun, S., Yandell, M., Tisserat, N., & Buell, C.R. (2010). Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenecity mechanisms and effector repertoire. Genome Biology 11, R73.
Google Scholar
Lilley, J. H., Callinan, R. B., Chinabut, S., Kanchanakhan, S., MacRae, I. H., & Phillips, M. J. (1998). Epizootic ulcerative syndrome (EUS) technical handbook. Bangkok: The Aquatic Animal Health Research Institute.
Google Scholar
Lilley, J. H., Hart, D., Panywachira, V., Kanchanakhan, S., Chinabut, S., Soderhall, K., & Cerenius, L. (2003). Molecular characterization of the fish-pathogenic fungus Aphanomyces invadans. Journal of Fish Diseases, 26, 263–275.
Article CAS PubMed Google Scholar
Links, M. G., Holub, E., Jiang, R. H. Y., Sharpe, A. G., Hegedus, D., Beynon, E., Sillito, D., Clarke, W. E., Uzuhashi, S., & Borhan, M. H. (2011). De novo sequence assembly of Albugo candida reveals a small genome relative to other biotrophic oomycetes. BMC Genomics, 12, 503. doi:10.1186/1471-2164-12-503.
Article CAS PubMed PubMed Central Google Scholar
Lunney, C. Z., & Bland, C. E. (1976). An ultrastructural stidy of zoosporogenesis in Pythium proliferum de Bary. Protoplasma, 88, 85–100.
Article Google Scholar
Manton, I., Clarke, B., & Greenwood, A. D. (1951). Observations with the electron microscope on a species of Saprolegnia. Journal of Experimental Botany, 2, 321–331.
Article Google Scholar
Marano, A. V., Jesus, A. L., De Souza, J. I., Jerônimo, G. H., Gonçalves, D. R., Boro, M. C., Rocha, S. C. O., & Pires-Zottarelli, C. L. A. (2016). Ecological roles of saprotrophic Peronosporales (Oomycetes, Straminipila) in natural environments. Fungal Ecology, 19, 77–88.
Google Scholar
Martin, W. W. (1977). The development and possible relationships of a new Atkinsiella parasitic in insect eggs. American Journal of Botany, 64, 760–769.
Article Google Scholar
Martin, F. N. (2000). Phylogenetic relationships among some Pythium species inferred from sequence analysis of the mitochondrially encoded cytochrome oxidase II gene. Mycologia, 92, 711–727.
Article CAS Google Scholar
Martin, R. W., & Miller, C. E. (1986a). Ultrastructure of mitosis in the endoparasite Olpidiopsis varians. Mycologia, 78, 11–21.
Article Google Scholar
Martin, R. W., & Miller, C. E. (1986b). Ultrastructure of zoosporogenesis in the endoparasite Olpidiopsis varians. Mycologia, 78, 230–241.
Article Google Scholar
Martin, R. W., & Miller, C. E. (1986c). Ultrastructure of sexual reproduction in Olpidiopsis varians. Mycologia, 78, 359–370.
Article Google Scholar
Martin, F. N., & Tooley, P. W. (2003a). Phylogenetic relationships among Phytophthora species inferred from sequence analysis of mitochondrially encoded cytochrome oxidase I and II genes. Mycologia, 95, 269–284.
Article CAS PubMed Google Scholar
Martin, F. N., & Tooley, P. W. (2003b). Phylogenetic relationships of Phytophthora ramorum, P. nemorosa and P. pseudosyringe, three species recovered from areas in California with sudden oak death. Mycological Research, 107, 1379–1391.
Article CAS PubMed Google Scholar
Martin, F. N., Blair, J. E., & Coffey, M. D. (2014). A combined mitochondrial and nuclear multilocus phylogeny of the genus Phytophthora. Fungal Genetics and Biology, 66, 19–32.
Article CAS PubMed Google Scholar
Maruyama, S., Matsuzaki, M., Misawa, K., & Nozaki, H. (2009). Cyanobacterial contribution to the genomes of the plastid lacking protists. BMC Evolutionary Biology, 9, 197. doi:10.1186/1471-2148-9-197.
Article PubMed PubMed Central CAS Google Scholar
Massana, R., & Pedró-Alió, C. (2008). Unveiling new microbial eukaryotes in the surface ocean. Current Opinion in Microbiology, 11, 213–218.
Article PubMed Google Scholar
Massana, R., Guillou, L., Diez, B., & Pedró-Alió, C. (2002). Unveiling the organisms behind novel eukaryotic ribosomal DNA sequences from the ocean. Applied and Environmental Microbiology, 68, 4554–4558.
Article CAS PubMed PubMed Central Google Scholar
Massana, R., Castresana, J., Balagué, V., Guillou, L., Romari, K., Groisillier, A., Valentin, K., & Pedró-Alió, C. (2004). Phylogenetic and ecological analysis of novel marine stramenopiles. Applied and Environmental Microbiology, 70, 3528–3534.
Article CAS PubMed PubMed Central Google Scholar
Massana, R., Terrado, R., Forn, I., Lovejoy, C., & Pedró-Alió, C. (2006). Distribution and abundance of uncultured heterotrophic flagellates in the world oceans. Environmental Microbiology, 8, 1515–1522.
Article CAS PubMed Google Scholar
Matari, N. H., & Blair, J. E. (2014). A multilocus timescale for oomycete evolution estimated under three distinct molecular clock models. BMC Evolutionary Biology, 14, 101. doi:10.1186/1471-2148-14-101.
Article PubMed PubMed Central Google Scholar
Maurosa, Y., Morimoto, K., Sano, A., Nishimura, K., & Hatai, K. (2009). A new peronosporomycete, Halioticida noduliformans gen.et sp. nov., isolated from white nodules in the abalone, Haliotis spp. from Japan. Mycoscience, 50, 106–115.
Article Google Scholar
McMorris, T. C., & Barksdale, A. W. (1967). Isolation of a sex hormone from the water mould Achlya bisexualis. Nature, 215, 320–321.
Article CAS PubMed Google Scholar
Mendoza, L. (2005). Pythiosis. In R. J. Hay & W. G. Merz (Eds.), Medical mycology, topley and Wilson’s microbiology and microbial infections (10th ed., pp. 412–429). London: Arnold.
Google Scholar
Mims, C. W., & Richardson, E. A. (2002). Ultrastructure of the zoosporangia of Albugo ipomoeae-panduratae as revealed by conventional chemical fixation and high pressure freezing followed by freeze substitution. Mycologia, 95, 1–10.
Article Google Scholar
Mizaee, M. R., Ploch, S., Runge, F., Telle, S., Nigrelli, L., & Thines, M. (2013). A new presumably widespread species of Albugo parasitic to Strigosella spp. (Brassicaceae). Mycological Progress, 12, 45–52.
Article Google Scholar
Molina, F. I. (1981). Petersenia polygaster (oomycetes), an invasive pathogen of Chondrus crispus (Rhodophyta), Ph.D. thesis, University of British Columbia, Vancouver.
Google Scholar
Molloy, D. P., Glockling, S. L., Siegfried, C. A., Beakes, G. W., James, T. Y., Mastitsky, S. E., Wurdak, E., Giamberini, L., Gaylo, M. J., & Nemeth, M. J. (2014). Aquastella gen. nov.: A new genus of saprolegniaceaous oomycete rotifer parasites related to Aphanomyces, with unique sporangial outgrowths. Fungal Biology, 118, 544–558.
Article PubMed Google Scholar
Money, N. P. (1998). Why the oomycetes have not stopped being fungi. Mycological Research, 102, 767–768.
Article Google Scholar
Morgan, W., & Kamoun, S. (2007). RXLR effors of plant pathogenic oomycetes. Current Opinion in Microbiology, 10, 332–338.
Article CAS PubMed Google Scholar
Nakagiri A. (2002). Diversity and phylogeny of Halophytophthora (Oomycetes). Abstracts 7th International Mycological Congress (p. 19). Oslo: International Mycological Society.
Google Scholar
Nakagiri, A., Newell, S. Y., & Ito, T. (1994). Two new Halophytophthora species, H. tartarea and H. masteri, from intertidal decomposing leaves in salt marsh and mangrove regions. Mycoscience, 35, 223–232.
Article Google Scholar
Newell, S. Y., & Fell, J. W. (1995). Distribution and experimental responses to substrate of marine oomycetes (Halophytophthora spp.) (Oomycota) from decomposing mangrove leaves. Canadian Journal of Botany, 73, 761–765.
Article Google Scholar
Newell, S. Y., Cefalu, R., & Fell, J. W. (1977). Myzocytium, Haptoglossa, and Gonimochaete (fungi) in littoral marine nematodes. Bulletin of Marine Science, 27, 177–207.
Google Scholar
Newhook, F. J., & Podger, F. D. (1972). The role of Phytophthora cinnamomi in Australian and New Zealand forests. Annual Review of Phytopathology, 10, 299–325.
Article Google Scholar
Nigrelli, L., & Thines, M. (2013). Tropical oomycetes in the German Bight – Climate warming or overlooked diversity? Fungal Ecology, 6, 152–160.
Article Google Scholar
Overton, S. V., Tharp, T. P., & Bland, C. E. (1983). Fine structure of swimming, encysting, and germinating spores of Haliphthoros milfordensis. Canadian Journal of Botany, 61, 1165–1177.
Article Google Scholar
Pais, M., Win, J., Kentaro, Y., Etherington, G. J., Cano, L. M., Raffael, S., Banfield, M. J., Jones, A., Kamoun, S., & Saunders, D. G. O. (2013). From pathogen genomes to host plant processes: the power of plant parasitic oomycetes. Genome Biology, 14, 211. doi:10.1186/gb-2013-14-6-211.
Article PubMed PubMed Central Google Scholar
Petersen, A. B., & Rosendahl, S. (2000). Phylogeny of the Peronosporomycetes (Oomycota) based on partial sequences of the large ribosomal subunit (LSU rDNA). Mycological Research, 104, 1295–1303.
Article CAS Google Scholar
Phillips, A. J., Anderson, V. L., Robertson, E. J., Secombes, C. J., & van West, P. (2008). New insights into animal pathogenic oomycetes. Trends in Microbiology, 16, 13–19.
Article CAS PubMed Google Scholar
Ploch, S., & Thines, M. (2011). Obligate biotrophic pathogens of the genus Albugo are widespread asymptomatic endophytes in natural populations of Brassicaceae. Molecular Ecology, 20, 3692–3699.
PubMed Google Scholar
Ploch, S., Choi, Y.-J., Rost, C., Shin, H.-D., Schilling, E., & Thines, M. (2010). Evolution of diversity in Albugo is driven by high host specificity and multiple speciation events on closely related Brassicaceae. Molecular Phylogenetics and Evolution, 57, 812–820.
Article PubMed Google Scholar
Podger, F. D. (1972). Phytophthora cinnamomi, a cause of lethal disease in indigenous plant communities in Western Australia. Phytopathology, 62, 972–981.
Article Google Scholar
Powell, M. J., & Bracker, C. E. (1977). Isolation of organelles from Phytophthora palmivora. Second International Mycological Congress Abstracts (p. 533). Tampa: International Mycological Association.
Google Scholar
Powell, M. J., & Letcher, P. M. (2014). Chytriomycota, Monoblepharidomycota, and Neocallismastigomycota. In D. J. McLaughlin & J. W. Spatafora (Eds.), The mycota VII Part A. Systematics and evolution (2nd ed., pp. 141–175). Springer: Berlin/Heidelberg.
Google Scholar
Pueschel, C. M., & van der Meer, J. P. (1985). Ultrastructure of the fungus Petersenia palmariae (Oomycota) parasitic on the alga Palmaria molis (Rhodophyceae). Canadian Journal of Botany, 63, 409–418.
Article Google Scholar
Qutob, D., Kamoun, S., & Gijzen M. (2002). Expression of Phytophthora sojae necrosis-inducing proteins occurs during transition from biotrophy to necrotrophy. The Plant Journal. doi: 10.1046/j.1365-313X.2002.01439.x.
PubMed Google Scholar
Ragukumar, C. (1980). An ultrastructural study of the marine diatom Licmophora hyalina and its parasite Ectrogella perforans. II. Development of the fungus in its host. Canadian Journal of Botany, 58, 2557–2574.
Article Google Scholar
Randolph, L. R., & Powell, M. J. (1992). Ultrastructure of zoospores of the oomycete Apodachlya pyrifera. Mycologia, 84, 768–780.
Article Google Scholar
Raper, J. R. (1939). Role of hormones in the sexual reaction of heterothallic Achlyas. Science, 89, 321–322.
Article CAS PubMed Google Scholar
Regel, E. (1843). Beitrage zur Kenntnis einiger Blattpilze. Botanische Zeitung. 1 Jahrgang, 39, 665–667.
Google Scholar
Richards, T. A., Dacks, J. B., Jenkinson, J. M., Thornton, C. R., & Talbot, N. J. (2006). Evolution of filamentous pathogens: Gene exchange across eukaryote kingdoms. Current Biology, 16, 1857–1864.
Article CAS PubMed Google Scholar
Richards, T. A., Soanes, D. M., Jones, M. D. M., Vasieva, O., Leonard, G., Paszkiewicz, K., Foster, P. G., Hall, N., & Talbot, N. J. (2011). Horizontal gene transfer facilitated the evolution of plant parasitic mechanisms in the oomycetes. Proceedings of the National Academy of Sciences of the United States of America, 108, 15258–15263.
Article CAS PubMed PubMed Central Google Scholar
Richards, T. A., Jones, M. D., Leonard, G., & Bass, G. (2012). Marine fungi their ecology and molecular diversity. Annual Review of Marine Science, 4, 495–522.
Article PubMed Google Scholar
Riethmüller, A., & Langer, E. (2004). Seasonal occurrence of species of Saprolegniales and Leptomitales in Lake Aue and the River Fulda in Kassel (Hesse) with special consideration of fish pathogenic species. Acta Hydrochimica et Hydrobiologica, 33, 622–634.
Article CAS Google Scholar
Riethmüller, A., Weiss, M., & Oberwinkler, F. (1999). Phylogenetic studies of Saprolegniomycetidae and related groups based on nuclear large subunit ribosomal DNA sequences. Canadian Journal of Botany, 77, 1790–1800.
Article Google Scholar
Riethmüller, A., Voglmayr, H., Göker, M., Weiss, M., & Oberwinkler, F. (2002). Phylogenetic relationships of the downy mildews (Peronosporales) and related groups based on nuclear large subunit ribosomal DNA sequences. Mycologia, 94, 834–849.
Article PubMed Google Scholar
Rilsberg, I., Orr, R. J., Kluge, R., Shalchian-Tabrizi, K., Bowers, H. A., Patil, V., Edvardsen, B., & Jakobsen, K. S. (2009). Seven gene phylogeny of heterokonts. Protist, 160, 191–204.
Article CAS Google Scholar
Robb, E. J., & Barron, G. L. (1982). Nature’s ballistic Missile. Science, 218, 1221–1222.
Article CAS PubMed Google Scholar
Rost, C., & Thines, M. (2012). A new species of Pustula (Oomycetes, Albuginales) is the causal agent of sunflower white rust. Mycological Progress, 11, 351–359.
Article Google Scholar
Roze, E., & Cornu, M. (1869). Sur deux nouveux types generiques pour les families des Saprolegniales et Peronosporales. Annales des Sciences Naturelles, Botanique. Serie V, 11, 72–91.
Google Scholar
Ruben, D. M., & Stanghellini, M. E. (1978). Ultrastructure of oospore germination in Pythium aphanidermatum. American Journal of Botany, 65, 491–501.
Article Google Scholar
Runge, F., Telle, S., Ploch, S., Savory, E., Day, B., Sharma, R., & Thines, M. (2011). The inclusion of downy mildews in a multi-locus-dataset and its reanalysis reveals a high degree of paraphyly in Phytophthora. IMA Fungus, 2, 163–171.
Article PubMed PubMed Central Google Scholar
Sandoval-Sierra, J. V., Martin, M. P., & Diéguez-Uribeondo, J. (2014). Species identification in the genus Saprolegnia (Oomycetes): Defining DNA-based molecualr operational units. Fungal Biology, 118, 559–578.
Article CAS PubMed Google Scholar
Savory, F., Leonard, G., & Richards, T. A. (2015). The role of horizontal gene transfer in the evolution of the oomycetes. PLoS Pathogens. doi:10.1371/journal.ppat.1004805.
PubMed PubMed Central Google Scholar
Schenck, N. C., & Nicolson, T. H. (1977). A zoosporic fungus occurring on species of Gigaspora margarita and other vesicular-arbuscular mycorrhizal fungi. Mycologia, 69, 1049–1053.
Article Google Scholar
Schnepf, E., Deichgräber, G., & Drebes, G. (1977). Development and ultrastructure of the marine, parasitic oomcete, Lagenisma coscinodisci (Lagenidiales): Sexual reproduction. Canadian Journal of Botany, 56, 1315–1325.
Article Google Scholar
Schnepf, E., Deichgräber, G., & Drebes, G. (1978a). Development and ultrastructure of the marine parasitic oomycete Lagenisma coscinodisci Drebes (Lagenidiales) Thallus, zoosporangium, mitosis and meiosis. Archives of Microbiology, 116, 121–132.
Article Google Scholar
Schnepf, E., Deichgräber, G., & Drebes, G. (1978b). Development and ultrastructure of the marine, parasitic oomycete, Lagenisma coscinodisci Drebes (Lagenidiales). The infection. Archives of Microbiology, 116, 133–139.
Article Google Scholar
Schnepf, E., Deichgräber, G., & Drebes, G. (1978c). Development and ultrastructure of the marine, parasitic Oomycete, Lagenisma coscinodisci Drebes (Lagenidiales): Formation of the primary zoospores and their release. Protoplasma, 94, 263–280.
Article Google Scholar
Schnepf, E., Drebes, G., & Elbrächter, M. (1990). Pirsonia guinardiae, gen. et spec. nov.: A parasitic flagellate on the marine diatom Guinardia flaccida with an unusual mode of food uptake. Helogoländer Meersesunters, 44, 275–293.
Article Google Scholar
Schroeder, K. L., Martin, F. N., de Cock, A. W. A. M., Lévesque, C. A., Spies, C. D. J., Okubara, P. A., & Paulitz, T. C. (2012). Molecular detection and quantification of Pythium species – Evolving taxonomy, new tools and challenges. Plant Disease, 97, 4–20.
Article CAS Google Scholar
Schröter, J. (1893). Peronsporinae. In A. Engler (Ed.), Die naturlichen Pfanzenfamilien nebst ihren Gattungen und wichtigeren Arten, insbesondere den Nutzpflanzen, unter Mitwirkung zahlreicher hervorragender Fachgelehrter begründet von A. Engler und K. Prantl. I. Teil (pp. 108–119). Abteilung 4.
Google Scholar
Schurko, A. M., Mendoza, L., Lévesque, C. A., Désaulniers, N. L., de Cock, A. W. A. M., & Klassen, G. R. (2004). A molecular phylogeny of Pythium insidiosum. Mycological Research, 107, 537–544.
Article CAS Google Scholar
Scott, W. W. (1961). A monograph of the genus Aphanomyces, Station Technical Bulletin (Vol. 151, pp. 1–95). Blacksburg: Virginia Agricultural Experimental.
Google Scholar
Seidl, M. F., Van den Ackerveken, G., Govers, F., & Snel, B. (2012). Reconstruction of oomycete genome evolution identifies differences in evolutionary trajectories leading to present-day large gene families. Genome Biology and Evolution, 4, 199–211.
Article PubMed PubMed Central CAS Google Scholar
Sekimoto, S. (2008). The taxonomy and phylogeny of the marine holocarpic oomycetes. Ph.D. Thesis, Kobe Graduate School of Natural Sciences, Konan University.
Google Scholar
Sekimoto, S., Hatai, K., & Honda, D. (2007). Molecular phylogeny of an unidentified Haliphthoros-like marine oomycete and Haliphthoros milfordensis inferred from nuclear-encoded small and large subunit rDNA genes and mitochondrial-encoded cox2 gene. Mycoscience, 48, 212–221.
Article CAS Google Scholar
Sekimoto, S., Beakes, G. W., Gachon, C. M. M., Müller, D. G., Küpper, F. C., & Honda, D. (2008a). The development, ultrastructural cytology, and molecular phylogeny of the basal oomycete Eurychasma dicksonii, infecting the filamentous phaeophyte algae Ectocarpus siliculosus and Pylaiella littoralis. Protist, 159, 401–412.
Article CAS Google Scholar
Sekimoto, S., Yokoo, K., Kawamura, Y., & Honda, D. (2008b). Taxonomy, molecular phylogeny, and ultrastructural morphology of Olpidiopsis porphyrae sp. nov. (Oomycetes, stramenopiles), a unicellular obligate endoparasite of Porphyra spp. (Bangiales, Rhodophyta). Mycological Research, 112, 361–374.
Article CAS PubMed Google Scholar
Sekimoto, S., Kochkova, T. A., West, J. A., Beakes, G. W., & Honda, D. (2009). Olpidiopsis bostychiae: A new species endoparasitic oomycete that infects Bostrychia and other red algae. Phycologia, 48, 460–472.
Article Google Scholar
Seymour, R. L. (1970). The genus Saprolegnia. Nova Hedwigia, 19, 1–124.
Google Scholar
Sharma, R., Xia, X., Cano, L. M., Evangelisti, E., Kemen, E., Judelson, H., Oome, S., Sambles, C., van den Hoogen, D. J., Kitner, M., Klein, J., Meijer, H. J., Spring, O., Win, J., Zipper, R., Bode, H. B., Govers, F., Kamoun, S., Schornack, S., Studholme, D. J., van den Ackerveken, G., & Thines, M. (2015a). Genome analyses of the sunflower pathogen Plasmopara halstedii provide insights into effector evolution in downy mildews and Phytophthora. BMC Genomics, 16, 741.
Article PubMed PubMed Central CAS Google Scholar
Sharma, R., Xia, X., Riess, K., Bauer, R., & Thines, M. (2015b). Comparative genomics including the early diverging smut fungus Ceraceosorus bombacis reveals parallel evolution within plant and animal pathogens of fungi and oomycetes. Genome Biology and Evolution, 7, 2781–2798.
Article CAS PubMed PubMed Central Google Scholar
Schenk, A. (1858). Über das Vorkommen contractiler Zellen im Pflanzenreiche. Würzburg: F.E. Thein.
Google Scholar
Shivas, R. G., Ryley, M. J., Telle, S., Liberato, J. R., & Thines, M. (2012). Peronosclerospora australiensis sp. nov. and Peronosclerospora sargae sp. nov., two newly recognised downy mildews in northern Australia, and their biosecucurity implications. Australasian Plant Pathology, 41, 125–130.
Article Google Scholar
Sneh, B., Humble, S. J., & Lockwood, J. L. (1977). Parasitism of oospores of Phytophthora megasperma var. sojae, P. cactorum, Pythium sp. and Aphanomyces euteiches in soil by Oomycetes, Chytridiomycetes, Hyphomycetes, Actinomycetes, and bacteria. Phytopathology, 67, 622–628.
Article Google Scholar
Soanes, D. M., Richards, T. A., & Talbot, N. J. (2007). Insights from sequencing fungal and oomycete genomes: What can we learn about plant diseases and the evolution of pathogenecity? The Plant Cell, 19, 3318–3326.
Article CAS PubMed PubMed Central Google Scholar
Sökücü, A., & Thines, M. (2014). A molecular phylogeny of Basidiophora reveals apparently host-specific lineages on Asteraceae. Mycological Progress, 13, 1137–1143.
Article Google Scholar
Soylu, E. M., Soylu, S., Keshavarzi, M., Brown, I., & Mansfield, J. W. (2003). Ultrastructural characterization of the intereactions between Arabidopsis thaliana and Albugo candida. Physiological and Molecular Plant Pathology, 63, 201–211.
Article CAS Google Scholar
Sparrow, F. K. (1960). Aquatic phycomycetes, 2nd revised edn. Ann Arbor: University of Michigan Press.
Google Scholar
Sparrow, F. K. (1973). Chytridiomycetes. Hyphochytridiomycetes. In G. C. Ainsworth, F. K. Sparrow, & A. S. Sussman (Eds.), The fungi (Vol. 4b, pp. 85–110). New York/London: Academic.
Google Scholar
Sparrow, F. K. (1976). The present status of classification in biflagellate fungi. In E. B. G. Jones (Ed.), Recent advances in aquatic mycology (pp. 213–222). London: Elek Press.
Google Scholar
Sparrow, F. K. (1977). Rhizidiomycopsis on azygospores of Gigaspora margarita. Mycologia, 69, 1053–1058.
Article Google Scholar
Spencer, D. M. (Ed.). (1981). The downy mildews. London: Academic.
Google Scholar
Spencer, M. A., & Dick, M. W. (2001). Aspects of graminicolous downy mildew biology: Perspectives for tropical plant pathology and Peronosporomycetes phylogeny. In R. Watling (Ed.), Tropical mycology, vol 2. Micromycetes (pp. 63–81). Wallingford: CABI Publishing.
Google Scholar
Spencer, M. A., Vick, M. C., & Dick, M. W. (2002). Revision of Aplanopsis, Pythiopsis, and ‘subcentric’ Achlya species (Saprolegniaceae) using 18S rDNA and morphological data. Mycological Research, 106, 549–560.
Article CAS Google Scholar
Spies, C., Lévesque, C.A., de Cock, A.W.A.M., Glockling, S.L., Chen, C.-Y., & de Grooters, A. M. (2014). Untangling Pythium, Lagenidium and their relatives. Abstracts of 10th International Mycological Congress, Bangkok, August 2014.
Google Scholar
Spies, C. F. J., Grooters, A. M., Lévesque, C. A., Rintoul, T. L., Redhead, S. A., Glockling, S. L., Chen, C.-Y., & de Cock, A. W. A. M. (2016). Molecular phylogeny and taxonomy of Lagenidium-like oomycetes pathogenic to mammals. Fungal Biology, 120, 931–947.
Article CAS PubMed Google Scholar
Steciow, M. M., Lara, E., Paul, C., Pillonel, A., & Belhahri, L. (2014). Multiple barcode assessment within the Saprolegnia-Achlya clade (Saprolegniales, Oomycota, Straminipila) brings order in a neglected group of pathogens. IMA Fungus, 5, 439–448.
Article PubMed PubMed Central Google Scholar
Steicow, M. M., Lara, E., Pillonel, A., Pelizza, S. A., Lestani, E. A., Rossi, G. C., & Belbahri, L. (2013). Incipient loss of flagella in the genus Geolegnia. the emergence of a new clade within Leptolegnia? IMA Fungus, 4, 169–175.
Article Google Scholar
Stevens, F. L. (1901). Gametogenesis and fertilization in Albugo. I. Botanical Gazette, 32, 77–98.
Article Google Scholar
Stidd, B. M., & Consentino, K. (1975). Albugo-like oogonia from the American carboniferous. Science, 190, 1092–1093.
Article Google Scholar
Stiller, J. W., Huang, J., Ding, W., Trian, J., & Goodwillie, C. (2009). Are algal genes in nonphotosynthetic protists evidence of historical plastid endosymbioses. BMC Genomics, 10, 484.
Article PubMed PubMed Central CAS Google Scholar
Strittmatter, M., Gachon, C. M. M., Müller, D. G., Kleinteich, J., Heesch, S., Tsirigoti, A., Katsaros, C., Kostopoulou, M., & Küpper, F. C. (2013). New records of intracellular eukaryotic pathogens challenging brown macroalgae in the East Mediterranean Sea, with emphasis on LSU rRNA data of the oomycete pathogen Eurychasma dicksonii. Diseases of Aquatic Organisms, 104, 1–11.
Article CAS PubMed Google Scholar
Strullu-Derrien, C., Kenrick, P., Rioult, J. P., & Strullu, D. G. (2010). Evidence of parasitic oomycetes (Peronosporomycetes) infecting the stem cortex of the Carboniferous seed fern Lygniopteris odlhamia. Proceedings of the Royal Society B. doi:10.1098/rspb.2010.1603.
PubMed PubMed Central Google Scholar
Taylor, T. N., Krings, M., & Keri, H. (2006). Hassiella monspora gen. et sp. nov., a microfungus from the 400 million year old Rhynie chert. Mycological Research, 110, 628–632.
Article PubMed Google Scholar
Telle, S., & Thines, M. (2012). Reclassification of an enigmatic downy mildew species on lovegrass (Egrostis) to the new genus Eraphthora, with a key to the genera of the Peronosporaceae. Mycological Progress, 11, 121–129.
Article Google Scholar
Telle, S., Shivas, R. G., Ryley, M. J., & Thines, M. (2011). Molecular phylogenetic analysis of Peronosclerospora (Oomycetes) reveals cryptic species and genetically distinct species parasitic to maize. European Journal of Plant Pathology, 130, 520–528.
Article Google Scholar
Tewari, J. P., & Skoropad, W. P. (1977). Ultrastructure of oospore development in Albugo candida on rape seed. Canadian Journal of Botany, 55, 2348–2357.
Article Google Scholar
Thines, M. (2006). Evaluation of characters available from herbarium vouchers for the phylogeny of downy mildew genera (Chromista, Peronasporales), with a focus on scanning electron-microscopy. Mycotaxon, 97, 195–218.
Google Scholar
Thines, M. (2009). Bridging the gulf: Phytophthora and downy mildews are connected by rare grass parasites. PloS One, 4, e4790.
Article PubMed PubMed Central CAS Google Scholar
Thines, M. (2014). Phylogeny and evolution of plant pathogenic oomycetes – A global overview. European Journal of Plant Pathology, 138, 431–447.
Article Google Scholar
Thines, M., & Choi, Y. J. (2016). Evolution, diversity, and taxonomy of the Peronosporaceae, with focus on the genus Peronospora. Phytopathology. doi:10.1094/PHYTO-05-15-0127-RVW.
Google Scholar
Thines, M., & Kamoun, S. (2010). Oomycete-plant coevolution: Recent advances and future prospects. Current Opinion in Biotechnology, 13, 427–433.
Google Scholar
Thines, M., & Spring, O. (2005). A revision of Albugo (Chromista, Peronosporomycetes). Mycotaxon, 92, 443–458.
Google Scholar
Thines, M., & Voglmayr, H. (2009). An introduction to the white bilster rusts (Albuginales). In K. Lamour & S. Kamoun (Eds.), Oomycete genetics and genomics: Diversity, interactions, and research tools (pp. 77–92). Ann Arbor: Wiley-Blackwell.
Chapter Google Scholar
Thines, M., Göker, M., & Oberwinkler, F. (2006). A revision of Bremia graminicola. Mycological Research, 110, 646–656.
Article PubMed Google Scholar
Thines, M., Göker, M., Oberwinkler, F., & Spring, O. (2007). A revision of Plasmopara penniseti, with implications for the host range of the downy mildews with pyriform haustoria. Mycological Research, 111, 1377–1385.
Article CAS PubMed Google Scholar
Thines, M., Göker, M., Telle, S., Ryley, M., Mathur, K., Narayana, Y. D., Spring, O., & Thakur, R. P. (2008). Phylogenetic relationships in graminicolous downy mildews based on cox2 sequence data. Mycological Research, 112, 345–351.
Article CAS PubMed Google Scholar
Thines, M., Telle, S., Ploch, S., & Runge, F. (2009a). Identity of the downy mildew pathogens of basil, coleus, and sage with implications for quarantine measures. Mycological Research, 113, 532–540.
Article PubMed Google Scholar
Thines, M., Voglmayr, H., & Göker, M. (2009b). Taxonomy and phylogeny of the downy mildews. In K. Lamour & S. Kamoun (Eds.), Oomycete genetics and genomics: Diversity, interactions, and research tools (pp. 47–75). Ann Arbor: Wiley-Blackwell.
Chapter Google Scholar
Thines, M., Choi, Y.-J., Kemen, E., Ploch, S., Holub, E. B., Shin, H.-D., & Jones, J. D. G. (2009c). A new species of Albugo parasitic to Arabidopsis thaliana reveals new evolutionary patterns in white blister rusts (Albuginaceae). Persoonia, 22, 123–128.
Article CAS PubMed PubMed Central Google Scholar
Thines, M., Nam, B., Nigrelli, L., Beakes, G., & Kraberg, A. (2015a). The diatom parasite Lagenisma coscinodisci (Lagenismatales, Oomycota) is an early diverging lineage of the Saprolegniomycetes. Mycological Progress, 14, 75. doi:10.1007/s11557-015-1099-y.
Article Google Scholar
Thines, M., Telle, S., Choi, Y., Tan, P. Y., & Shivas, R. G. (2015b). Baobabopsis, a new genus of graminicolous downy mildews from tropical fungi, with an updated key to the genera of downy mildews. IMA Fungus, 6, 483–491.
Article PubMed PubMed Central Google Scholar
Tian, M., Win, J., Savory, R., Burkhart, A., Held, M., Brandizzi, F., & Day, F. (2011). 454 Genome sequencing of Pseudoperonospora cubensis revleals effector proteins with a QXLR translocation motive. Molecular Plant-Microbe Interactions, 24, 543–553.
Article CAS PubMed Google Scholar
Tong, S. M. (1995). Developayella elegans nov. gen., nov. spec., a new type of heterotrophic flagellate from marine plankton. European Journal of Protistology, 31, 24–31.
Article Google Scholar
Torto-Alalibo, T., Tian, M., Gajendran, K., Waugh, M. E., van West, P., & Kamoun S. (2005). Expressed sequence tags from the oomycete fish pathogen Saprolegnia parasitica reveal putative virulence factors. BMC Microbiology, 5, 46. doi:10.1186/1471-2180-5-46.
Article PubMed PubMed Central CAS Google Scholar
Tsao, P. H. (1970). Selective media for isolation of pathogenic fungi. Annual Review of Phytopathology, 8, 157–186.
Article Google Scholar
Tsui, C. K. M., Marshall, W., Yokoyama, R., Honda, D., Lippmeier, J. C., Craven, K. D., & Berbee, M. L. (2009). Labryinthulomycetes phylgeneny and its implications for the evolutionary loss of chloroplasts and gain of ectoplasmic gliding. Molecular Phylogenetics and Evolution, 50, 129–140.
Article CAS PubMed Google Scholar
Tyler, B. M., Tripathy, S., Zhang, X., Dehal, P., Jiang, R. H., Aerts, A., Arredondo, F. D., Baxter, L., Bensasson, D., Beynon, J. L., Chapman, J., Damasceno, C. M., Dorrance, A. E., Dou, D., Dickerman, A. W., Dubchak, I. L., Garbelotto, M., Gijzen, M., Gordon, S. G., Govers, F., Grunwald, N. J., Huang, W., Ivors, K. L., Jones, R. W., Kamoun, S., Krampis, K., Lamour, K. H., Lee, M. K., McDonald, W. H., Medina, M., Meijer, H. J., Nordberg, E. K., Maclean, D. J., Ospina-Giraldo, M. D., Morris, P. F., Phuntumart, V., Putnam, N. H., Rash, S., Rose, J. K., Sakihama, Y., Salamov, A. A., Savidor, A., Scheuring, C. F., Smith, B. M., Sobral, B. W., Terry, A., Torto-Alalibo, T. A., Win, J., Xu, Z., Zhang, H., Grigoriev, I. V., Rokhsar, D. S., & Boore, J. L. (2006). Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science, 313, 1261–1266.
Article CAS PubMed Google Scholar
Usuhashi, S., Motoaki, T., & Kakishima, M. (2010). Phylogeny of the genus Pythium and description of new genera. Mycoscience, 51, 337–365.
Article Google Scholar
Van der Auwera, G., Da Baere, R., Van der Peer, Y., Rijk, P. D., Van den Broeck, I., & De Wachter, R. (1995). The phylogeny of the Hyphochytriomycota as deduced from ribosomal RNA sequences of Hyphochytrium catenoides. Molecular Biology and Evolution, 12, 671–678.
CAS PubMed Google Scholar
van der Plaats-Niterink, A. J. (1981). Monograph of the genus Pythium. Baarn: Centraalbureau voor Schimmelcultures.
Google Scholar
Van West, P. (2006). Saprolegnia parasitica, an oomycete pathogen with a fishy appetite; new challenges for an old problem. Mycologist, 20, 99–104.
Article Google Scholar
Van Wyk, P. S., Jones, B. L., Vilgoen, A., & Rong, I. H. (1995). Early lodging, a novel manifestation of Albugo tragopogonis infection on sunflower in South Africa. Helia, 18, 83–90.
Google Scholar
Vilgoen, A., van Wyk, P. S., Nowell, D. C., & Gulya, T. J. (1997). Occurrence of downy mildew on sunflower in South Africa. Plant Disease, 81, 111.
Article Google Scholar
Villa, N. O., Kageyama, K., Asano, T., & Suga, H. (2006). Phylogenetic relationships of Pythium and Phytophthora species based on ITS, rDNA, cytochrome oxidase II and β-tubulin gene sequences. Mycologia, 98, 410–422.
CAS PubMed Google Scholar
Vlk, W. (1939). Uber die Geisselstructur der Saprolegniaceenschwärmer. Archiv für Protistenkunde, 92, 157–160.
Google Scholar
Vogel, H. J. (1960). Two modes of lysine synthesis among lower fungi: Evolutionary significance. Biochimica et Biophysica Acta, 41, 172–173.
Article CAS Google Scholar
Voglmayer, H. (2003). Phylogenetic study of Peronospora and related genera based on nuclear ribosomal ITS sequences. Mycological Research, 107, 1132–1142.
Article CAS Google Scholar
Voglmayr, H. (2008). Progress and challenges in systematics of downy mildews and white blister rusts: New insights from genes and morphology. European Journal of Plant Pathology, 22, 3–18.
Article Google Scholar
Voglmayr, H., & Constantinescu, O. (2008). Revision and reclassification of three Plasmopara species based on morphological and molecular phylogenetic data. Mycological Research, 112, 487–501.
Article CAS PubMed Google Scholar
Voglmayr, H., & Riethmüller, A. (2006). Phylogenetic relationships of Albugo species (white blister rusts) based on LSU rDNA sequence and oospore data. Mycological Research, 110, 75–85.
Article CAS PubMed Google Scholar
Voglmayr, H., Bonner, L., & Dick, M. W. (1999). Taxonomy and oogonial ultrastructure of a new aero-aquatic peronosporomycete, Medusoides gen nov. (Pythiogetonaceae fam nov). Mycological Research, 103, 591–606.
Article Google Scholar
Voglmayr, H., Riethmüller, A., Göker, M., Weiß, M., & Oberwinkler, F. (2004). Phylogenetic relationships of Plasmopara, Bremia and other genera of downy mildews with pyriform haustoria based on Bayesian analysis of partial LSU rDNA sequence data. Mycological Research, 108, 1011–1024.
Article CAS PubMed Google Scholar
Wang, M. C., & Bartnicki-Garcia, S. (1974). Mycolaminarans. Storage (l→3)-β-D-glucans from the cytoplasm of the fungus Phytophthora palmivora. Carbohydrate Research, 37, 331–338.
Article CAS Google Scholar
Waterhouse, G. M. (1970). The genus Phytophthora de Bary: Diagnoses (or descriptions) and figures from the original papers, 2nd edition. Mycological Papers, 122, 1–59.
Google Scholar
Waterhouse, G. M. (1973). Peronosporales. In G. C. Ainsworth, F. K. Sparrow, & A. S. Sussman (Eds.), The Fungi: An advanced treatise IVB (pp. 165–183). New York/London: Academic.
Google Scholar
Wavra, S., Bain J., Durward, E., Bruijn, I. D., Minor, K., Matena, A., Lobach, L., Whisson, S. C., Bayer P., Birch, P. R. J., Seccombes, C. J., & van West, P. (2012). Host-targeting protein 1 (SpHtp1) from the oomycete Saprolegnia parasitica translocates specifically into fish cells in a tyrosine-O-sulphate dependent manner. Proceedings of the National Academy of Sciences USA, 109, 2096–2101.
Article Google Scholar
Wells, E. A. (1982). A developmental study of the aquatic fungus Hyphochytrium catenoides Karling. MS Thesis, University of Georgia, Athens, pp. i–xi, 1–115.
Google Scholar
Whisson, S. C., Avrova, A., Grenville-Briggs, L., & van West, P. (2009). Mechanisms and applications of gene silencing in oomycetes. In K. Lamour & S. Kamoun (Eds.), Oomycete genetics and genomics: Diversity, interactions and research tools (pp. 493–515). New York: Wiley.
Chapter Google Scholar
Willoughby, L. G. (1962). The occurrence of reproductive spores of Saprolegniaceae in freshwater. Journal of Ecology, 50, 733–759.
Article Google Scholar
Win-Tin, & Dick, M. W. (1975). Cytology of the oomycetes: Evidence for meiosis and multiple chromosome associations in Saprolegniaceae and Pythiaceae, with an introduction to the cytotaxonomy of Achlya and Pythium. Archives of Microbiology, 105, 283–293.
Article Google Scholar
Wood, S. E., & Willoughby, L. G. (1986). Ecological observations on the fungal colonization of fish by Saprolegniaceae in Windermere. Journal of Applied Biology, 23, 737–749.
Google Scholar
Wynn, A. R., & Epton, H. A. S. (1979). Parasitism of oospores of the Phytophthora erythroseptica in soil. Transactions of the British Mycological Society, 73, 255–259.
Article Google Scholar
Yoshida, K., Schuenemann, V. J., Cano, L. M., Pais, M., Mishra, B., Sharma, R., Lanz,. C., Martin, F. N., Kamoun, S., Krause,. J., Thines, M., Weigel, D., & Burbano, H. A. (2013). The rise and fall of the Phytophthora infestans lineage that triggered the Irish potato famine. eLife, 2, e00731.
Google Scholar
Yubuki, N., Leander, B. S., & Silberan, J. D. (2010). Ultrastructure and molecular phylogenetic position of a novel phagotrophic position of a novel phagotrophic stramenopile from low oxygen environments, Rictus lutensis gen. et sp. nov. (Biocoecida, incertae sedis). Protist, 161, 264–278.
Article CAS PubMed Google Scholar
Zopf, W. (1884). Zur Kenntniss der Phycomyceten. 1. Zur Morphologie und Biologie der Ancylisteen und Chytridiaceen, zugleich ein Beitrag zur Kaiserlichen Leopoldinisch-coralinischen. Akademie der Naturforscher, 47, 141–236.
Google Scholar

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Acknowledgments

We would like to acknowledge the contribution made by the many colleagues who work on Oomycota for their helpful advice, discussions and sharing of phylogenetic data and illustrative material. In particular we would like to thank Satoshi Sekimoto, Sally Glockling, André Lévesque, Shigeke Inaba, Markus Göker, David Cooke, Nicholas Money, Claire Gachon, Deborah Huspeth, Young-Joon Choi, Hermann Voglmayr, Sabine Telle, Sebastian Ploch, late Ovidiu Constantinescu. Funding by the German Science Foundation, the Landesstiftung Baden-Württemberg (Elite Programm for Postdocs), the Max-Planck-Society and support by LOEWE in the framwork of IPF and BiK-F to M.T. are gratefully acknowledged.

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Department of Biology, School of Biology, Newcastle University, Newcastle upon Tyne, NE1 7RU, Newcastle upon Tyne, UK
Gordon W. Beakes
Department of Biological Sciences, Institute of Ecology, Evolution and Diversity, LOEWE Excellence Cluster for Integrative Fungal Research (IPF) and Biodiversity and Climate Research Centre (BiK-F), Senckenberg Gesellschaft für Naturforschung, Goethe University Frankfurt am Main, Senckenberganlage 25, D-60325, Frankfurt am Main, Germany
Marco Thines

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Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Nova Scotia, Canada
John M. Archibald
Department of Biology, Dalhousie University, Halifax, Nova Scotia, Canada
Alastair G.B. Simpson
Department of Biochemistry and Molecular Biology, Dalhousie University , Halifax, Nova Scotia, Canada
Claudio H. Slamovits

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Beakes, G.W., Thines, M. (2017). Hyphochytriomycota and Oomycota. In: Archibald, J., Simpson, A., Slamovits, C. (eds) Handbook of the Protists. Springer, Cham. https://doi.org/10.1007/978-3-319-28149-0_26

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DOI: https://doi.org/10.1007/978-3-319-28149-0_26
Published: 01 August 2017
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-28147-6
Online ISBN: 978-3-319-28149-0
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Hyphochytriomycota and Oomycota

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Hyphochytriomycota and Oomycota

Chytridiomycota

3 Systematics of the Straminipila: Labyrinthulomycota, Hyphochytriomycota, and Oomycota

Keywords

Summary Classification

Introduction

General Characteristics

Occurrence

Literature and History of Knowledge

Economic and Practical Importance

Habitats And Ecology

Characterization and Recognition

Thallus Organization

Sporogenesis

Sexual Reproduction

Ultrastructure

Zoospore Ultrastructure

Mature Oospore Ultrastructure

Genomic Studies

Classification

Phylum Hyphochytriomycota

Class Hyphochytriomycetes

Order Hyphochytriales

Phylum Oomycota Arx

Basal Class(es) – incertae sedis

Order “Eurychasmales”

Order Haptoglossales M.W. Dick

Order ~Olpidiopsidales s. lat. M.W. Dick

Order “Haliphthorales”

Class Saprolegniomycetes Thines et Beakes

Order “Atkinsiellales” and closely related taxa.

Order Leptomitales Kanouse

Order Saprolegniales E. Fisch.

Class: Peronosporomycetes M.W. Dick

Order Rhipidiales M.W. Dick.

Order Albuginales Thines

Order Peronosporales E. Fisch. s. lat

Maintenance and Cultivation

Evolutionary History

References

Acknowledgments

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