Keywords

Introduction

Some 30 or so virus and virus-like diseases of grapevines are recognized (Martelli 2014), which are characterized by a wide array of symptoms, i.e., malformations of leaves and twigs, foliar discolorations (reddening, yellowing, chlorotic or bright yellow mottling, ringspots, and line patterns ), grooving and/or pitting of the woody cylinder, delayed bud break, stunting, and decline. The productive lifespan of the vineyards can be shortened and the quantity and quality of the crop badly affected. Prevailing agents of the three major disease complexes (infectious degeneration /decline, leafroll , and rugose wood) are either viruses with isometric particles, the most relevant of which are transmitted by nematodes (nepoviruses ), or viruses with filamentous particles, transmitted by pseudococcid mealybugs and soft scale insects (closteroviruses and vitiviruses ). No vectors are known for the viruses of a fourth complex (fleck ). Infected propagation materials (nursery productions) are the major responsible for the long-distance dissemination of the viral diseases and related agents, several of which have now a worldwide distribution and have entered areas where the grapevine industry is expanding. This is, in summary, the extant situation. However, how was it in the past, and when and where did the sanitary problems began?

The first descriptions of an alarming degenerative condition (infectious degeneration ) of grapevines date back to the second half of the nineteenth century. These early records were from European countries: France (Cazalis-Allut 1865), Austria (Rathay 1882), Germany (Cholin 1896), and Italy (Baccarini 1902). In a few decades, evidence was gathered that this disease had a patchy distribution in the field and was graft transmissible and no infection occurred when the soil was heated at 120 °C (Schiff-Giorgini 1906; Pantanelli 1910, 1917; Petri 1918). Based on these evidences and his own observations, Petri (1929) endorsed Baccarini’s (1902) early suggestion of the putative viral origin of the disease in question.

Notwithstanding the relevance of infectious degeneration, and after the early 1900s upsurge of interest for it, there was no much action in Europe and elsewhere up to the mid-1950s. Then, the studies carried out in California (Hewitt 1954) revealed that grapevines are affected by a number of different virus and viruslike diseases and provided a detailed description of their symptomatology. This was soon followed by the demonstration that fanleaf (i.e., the same disease as the European infectious degeneration) is indeed a soilborne disorder transmitted by the longidorid nematode Xiphinema index (Hewitt et al. 1958) and, shortly afterward, that the putative agent of fanleaf is a mechanically transmissible Nepovirus (Cadman et al. 1960). These papers revived the attention for the long-neglected viral problems of the viticultural industry, first in Europe and then in the rest of the world.

In May 1962, a group of American and European plant pathologists decided to establish a study group denoted “International Council for the Study of Virus and Virus-like Diseases of the Grapevine” [ICVG (Bovey and Gugerli 2003)], an organization which has given a tremendous impulse to virological studies. In fact, since the early 1960s, nearly 70 different viruses have been identified in grapevines (Vitis and Muscadinia), many of which (31 viruses) are associated with the four major disease complexes that, as stated above, are known as (1) infectious degeneration (12 European/Mediterranean nepoviruses) and decline (four American nepoviruses), (2) leafroll (five viruses), (3) rugose wood (six viruses) and (4) fleck (four viruses) (Table 2.1).

Table 2.1 Grapevine-infecting viruses
Full size table

Infectious Degeneration /Decline

Recognized as putative agents of infectious degeneration/decline are viruses with isometric particles classified in the genus Nepovirus (except for Strawberry latent ringspot virus, which is an unassigned member of the family Secoviridae), many of which (eight of those infecting vines) have a recognized nematode vector. These viruses have a bipartite, single-stranded, positive-sense RNA genome. The complete sequence of 12 of them has been determined (Martelli 2014): Arabis mosaic virus (ArMV), Cherry leafroll virus (CLRV), grapevine Anatolian ringspot virus (GARSV), Grapevine Bulgarian latent virus (GBLV), Grapevine chrome mosaic virus (GCMV), Grapevine deformation virus (GDefV), Grapevine fanleaf virus (GFLV) , Raspberry ringspot virus (RpRSV), Strawberry latent ringspot virus (SLRSV), Tomato black ring virus (TBRV), Tobacco ringspot virus (TRSV) , and Tomato ringspot virus (ToRSV). A comparative analysis of these sequences disclosed that recombination at the level of RNA-2 is an efficient evolutionary mechanism of these viruses, which results in the emergence of interspecific hybrids (Olivier et al. 2010) and novel viral species. The latter is the case of (1) Grapevine chrome mosaic virus, a recombinant between Tomato black ring virus and Grapevine Anatolian ringspot virus (Digiaro et al. 2015), and (2) Grapevine deformation virus, a recombinant between Grapevine fanleaf virus and Arabis mosaic virus (Elbeaino et al. 2012).

Viruses involved in degenerative diseases (fanleaf and the like) are referred to as Old World nepoviruses because, except for GFLV, which has a man-fostered worldwide distribution, they occur in this geographical area and have vectors sharing the same territorial distribution (Martelli and Taylor 1990). Thus, degenerative diseases and relative agents prevail in Continental and Mediterranean Europe where they are likely to have originated, whereas with other diseases denoted “grapevine decline”, the eliciting viruses and vectors are found primarily in North America .

Based on the above, it can be hypothesized that degenerative diseases occurred in Europe before the arrival of phylloxera, thus are native to the Old World. This likelihood is supported by additional evidence:

  1. 1.

    Old records in the European literature describing the symptoms of the disease.

  2. 2.

    Discovery in a Sicilian herbarium of the second half of the nineteenth century of dried grapevine leaves with symptoms identical to those currently visible in vines infected by chromogenic and distorting strains of GFLV (Martelli and Piro 1975).

  3. 3.

    Old paintings, [e.g., Pompeii frescos (79 AD) and a painting by Caravaggio (1600)] depicting distorted grapevine leaves resembling those from fanleaf-diseased plants.

  4. 4.

    GFLV, the major causal agent of degeneration, is serologically related to ArMV, a European Nepovirus with which it can recombine to give rise either to new “pathotypes” [e.g., chromogenic virus strains (Elbeaino et al. 2014)] or to novel grapevine-infecting viral species [e.g., Grapevine deformation virus (Elbeaino et al. 2012)].

  5. 5.

    Tolerance to GFLV infection is widespread in European grapes, likely due to their long-lasting association with and adaptation to the virus. In fact, a high level of the “host plant resistance ” type was found in V. vinifera accessions from the Near East (Walker and Meredith 1990), one of the areas of domestication of the grapevine (Arroyo-Garcia et al. 2006).

  6. 6.

    Xiphinema index, the vector of fanleaf, is a nematode thought to be native of Asia minor (ancient Persia) (Hewitt 1968; Mojtahedi et al. 1980). Its eastern origin was confirmed through the analysis of mitochondrial genes and microsatellite loci (Villate 2008).

  7. 7.

    GFLV occurs in phylloxera-free countries (e.g., Cyprus, Armenia, parts of southern Turkey, some Aegean Greek islands) (Martelli 2014), where American rootstocks have not been introduced.

Evidence of the American roots of decline syndromes rests on (1) their almost exclusive occurrence in Vitis vinifera and V. labrusca grown in the Northern United States and Canada; (2) the origin of the eliciting viruses [ToRSV, TRSV, and Peach rosette mosaic virus (PRMV) ], whose presence in other geographical areas is due to accidental introductions; and (3) the distribution of their vectors, which are largely restricted to North America (Martelli and Taylor 1990; Martelli and Uyemoto 2011).

Leafroll

Graft transmission of leafroll from grape to grape was first obtained in Germany by Scheu (1936). A decade later, Harmon and Snyder (1946) described in California a graft-transmissible disease of cv. Emperor called “White Emperor” which, after an additional decade, and again in California, was shown to be the same as leafroll (Goheen et al. 1958). Thus, in the early 1960, the infectious nature of leafroll was established, but its etiological agent was still unknown. The importance of the discovery of filamentous viruslike particles in the sieve tubes of German vines affected by yellows (Mendgen 1971) was overlooked, notwithstanding the fact that the similarity with citrus plants infected by the Closterovirus Citrus tristeza virus (CTV) was striking. The breakthrough came a few years later when Closterovirus-like particles were recovered in Japan from vines with leafroll symptoms and their presence was linked with the disease (Namba et al. 1979).

The first partial characterization of two serologically different leafroll-associated closteroviruses came from Switzerland in 1984. These viruses were referred to as “type I” and “type II” (Gugerli et al. 1984). This was the beginning of the nomenclature based on the use of numbers. In the years that followed, the putatively new Closterovirus species found in leafroll-diseased vines increased in a disorderly way, so as to call for a revision of their status and nomenclature. The number of bona fide virus species was reduced to six, and their name was determined to be Grapevine leafroll -associated virus (GLRaV) followed by an Arabic numeral, e.g., GLRaV-1, GLRaV-2, GLRaV-3, and so on (Boscia et al. 1995).

For many years, leafroll was thought not to be spreading in the field, and the reports from different countries (e.g., Dimitrijevic 1973) that this was not the case were not paid much attention. A leap forward was made when Grapevine virus A (GVA), which at that time was classified as a “short Closterovirus ,” was transmitted by the mealybug Pseudococcus longispinus (Rosciglione et al. 1983). In this paper it was stated that:

These observations are consistent with the notion that mealybugs could be vectors of grapevine leafroll as indicated some 20 years ago by the late Dr. H.F. Dias, then by Dr. L. Chiarappa who, in trials with an unidentified species of Pseudococcus carried out in California in 1961, obtained the reproduction of the leafroll syndrome on virus-free Mission vines exposed to mealybugs that had previously fed on grapevine with natural leafroll infection. (Rosciglione et al. 1983)

These findings were not published, but the information and the positive results of GVA transmission by a mealybug species (Rosciglione et al. 1983) prompted a study, which showed that Grapevine leafroll-associated virus 3 (GLRaV-3) is vectored by Planococcus ficus (Rosciglione and Gugerli 1989). It was later established that the transmission is nonspecific (multiple vectors) and semi-persistent (Krüger et al. 2006; Almeida et al. 2013).

Recognized vectors of leafroll agents are as follows: Heliococcus bohemicus, Phenacoccus aceris, Ps. affinis, Ps. calceolariae, Ps. viburni, Ps. maritimus, Ps. comstocki, Ph. aceris, Pulvinaria vitis, Neopulvinaria innumerabilis and Parthenolecanium corni (GLRaV-1); Planococcus ficus, Pl. citri, Pseudococcus longispinus, Ps. calceolariae, Ps. maritimus, Ps. affinis, Ps. viburni, Ps. comstocki, Phenacoccus aceris, Parthenolecanium corni, Neopulvinaria innumerabilis, Pulvinaria vitis, Coccus hesperidium, C. longulus, Saissetia sp., Parasaissetia sp., and Ceroplastes sp. (GLRaV-3); Ps. longispinus, Pl. ficus, and Ph. aceris (GLRaV-4 and several of its strains).

Closteroviruses have very flexuous filamentous particles with distinct cross-banding, are members of the family Closteroviridae , and are classified in four genera: Closterovirus (vectored by aphids), Ampelovirus (vectored by mealybugs and soft scale insects ), Crinivirus (vectored by whiteflies), and Velarivirus (vector unknown). Grapevine-infecting closteroviruses belong in the genera Closterovirus, Ampelovirus, and Velarivirus and possess genomes differing in size (from 13,700 to 18,500 nucleotides) and structure (from 6 to 12 genes) (Martelli et al. 2012). These differences are thought to derive from the modular evolution of a primigenial replicating viral sequence that underwent a series of successive modifications, i.e., loss of sequences due to deletion, acquisition of sequences from foreign sources, gene duplication followed by diversification, and genome bipartition (Dolja et al. 2006).

Although leafroll is now one of the most widespread virus disorders of the grapevine in the world, its origin seems to hail from the Old World where the disease is likely to have occurred long before the arrival of phylloxera. Supporting evidence is: (1) old records in the Italian and French literature describing an abnormal condition of grapevines called “rossore” and “rougeau” (reddening), respectively; (2) presence in a Sicilian herbarium of the second half of the nineteenth century of dried grapevine leaves reported as being affected by “rossore.” These specimens show unmistakable signs of a leafroll condition, i.e., downward rolled, very heavy, thick, fractured, and blackish blades (Martelli and Piro 1975); (3) occurrence of some of the leafroll-associated viruses (especially GLRaV-1 and GLRaV-3 ) in countries like Cyprus, Armenia, Yemen, China (Sinkiang), parts of southern Turkey, and some Aegean Greek islands which are still phylloxera-free; thus, the vines grow on their own roots (Martelli et al. 1994; Pio Ribeiro et al. 2004); and (4) leafroll-infected vines were present among the original grape stocks imported in 1890 from Europe by the University of California (Luhn and Goheen 1970).

There is, however, a puzzling case which is not in line with the above reconstruction. It so happens that GLRaV-2 infections have recently been recorded in American native species: (1) Vitis californica and its natural hybrids with Vitis vinifera in California (Klaassen et al. 2011); and (2) Muscadinia rotundifolia and summer grape (Vitis aestivalis) in Southeastern United States, i.e., Mississippi and the Great Smoky Mountains National Park (GSMNP) (Aboughanem-Sabanadzovic and Sabanadzovic 2015). The virus isolate from GSMNP is the same as the Californian graft incompatibility inducer GLRaV-2RG (Alkowni et al. 2011) which is not known to occur in Europe, whereas the isolate from Mississippi is an ordinary leafroll-inducing strain (Meng et al. 2005). It ensues that the presence of GLRaV-2 in V. aestivalis growing in a natural ecosystem (GSMNP), in muscadines in an area with a small V. vinifera industry (Mississippi), and in the riparian vegetation of the Napa Valley (California) seems difficult to reconcile with an European origin of this virus, unless in the USA there is a vector (e.g., an aphid, as with other members of the genus Closterovirus in which GLRV-2 belongs?) able to acquire the virus from infected European grapevines (V. vinifera) and transfer it to native Vitis species. Should this not be the case, the notion that GLRaV-2 may be a virus native to North America gains strength.

Rugose Wood

Rugose wood, a graft-transmissible disease first reported from Italy (Graniti and Martelli 1965) and soon afterward from Hungary (Martelli et al. 1967), is a complex disorder within which, based on the differential reactions of the indicators V. rupestris, LN33, and Kober 5BB (Savino et al. 1987), four different syndromes have been identified: Rupestris stem pitting (RSP) , Kober stem grooving (KSG), Corky bark (CB), and LN-33 stem grooving (LNSG).

The etiology of rugose wood remained uncertain for many years, until the recovery by mechanical inoculation from a symptomatic vine of a virus with particles resembling those of closteroviruses (Conti et al. 1980) provided support to its supposed viral nature. The name of this virus, which was originally denoted Grapevine stem pitting-associated virus, was later changed into Grapevine virus A (GVA) (Milne et al. 1984). Other similar viruses were soon identified in infected vines, four of which, i.e., Grapevine virus B (GVB), Grapevine virus D (GVD), Grapevine virus E (GVE), and Grapevine virus F (GVF), have found a taxonomic allocation in the genus Vitivirus along with GVA, the type species of the genus (Martelli et al. 1997). An additional virus, called Grapevine rupestris stem pitting-associated virus (GRSPaV) (Meng et al. 1998), was classified in the novel genus Foveavirus (Martelli and Jelkmann 1998).

The extant relationship between the rugose wood syndromes and their putative agents can be summarized as follows: (1) GRSPaV (Meng et al. 1999), (2) GVA/Kober stem grooving (Garau et al. 1994), (3) GVB and GVD/Corky bark (Bonavia et al. 1996), and (4) no specific virus is associated with LNSG. As yet, there is no evidence of a cause-effect relationship for two additional vitiviruses recently found in vines showing either stem pitting (GVE) or a graft incompatibility condition (GVF) (Martelli 2014).

A breakthrough in rugose wood epidemiology came when GVA was experimentally transmitted by Pseudococcus longispinus (Rosciglione et al. 1983). This represented the first evidence that pseudococcid mealybugs , till then known as DNA virus vectors, were able to transmit also RNA viruses. It was later ascertained that, the same as with closteroviruses, Vitivirus transmission is nonspecific and semi-persistent (La Notte et al. 1997).

Recognized vectors are the same as those reported for ampeloviruses , with which vitiviruses are often transmitted together: Planococcus citri, Pl. ficus, Pseudococcus longispinus, Ps. affinis, Heliococcus bohemicus, Phenacoccus aceris, and Neopulvinaria innumerabilis (GVA); Ps. longispinus, Ps. affinis, Pl. ficus, and Ph. aceris (GVB); Pseudococcus comstocki (GVE). The vector of GVD is still unknown, so is the vector of GRSPaV (Martelli 2014).

Vitiviruses and foveaviruses possess very flexuous filamentous particles with a morphology resembling that of closteroviruses , with which they may share a comparable evolutionary scenario (Martelli et al. 2007), the same as representatives of the genus Trichovirus . These latter viruses, however, are not involved in any of the rugose wood syndromes , but two different species, Grapevine berry inner necrosis virus (GINV) and Grapevine pinot gris virus (GPGV), which have eriophyid mite vectors, are pathogenic to grapevines (Giampetruzzi et al. 2012; Yoshikawa et al. 1997).

Rugose wood also appears to be an “Old World” disease based on the following evidence: (1) wood symptoms described in the French literature of the early twentieth century and (2) occurrence of the disease and some of the rugose wood-associated viruses in phylloxera-free countries like Cyprus, Armenia, Yemen, parts of southern Turkey, and some Aegean Greek islands where American rootstocks have not yet been introduced (Martelli et al. 1994).

Admittedly, this historical evidence is less substantiated than that gathered for infectious degeneration and leafroll, and it may apply only in part to GRSPaV, a definitive species of the genus Foveavirus and the most widespread of the rugose wood-associated viruses. In fact, GRSPaV is (1) nonmechanically transmissible, (2) may not be seed transmitted notwithstanding its presence in pollen grains and has no known vector, (3) may have evolved from an ancient recombination event between a Carlavirus and a Potexvirus (Meng and Gonsalves 2003), and (4) may have gained entrance in different Vitis species in the past, and, while adapting to them, its genome has diverged, producing several groups of variants. Two of the four major groups of variants may be specific to V. riparia and V. rupestris (American species), whereas two other groups may be linked with V. sylvestris and, perhaps, V. vinifera (Old World species) (Meng and Gonsalves 2007; Meng and Rowhani, Chap. 12, this book).

Fleck

Fleck , a disease with a worldwide distribution, is latent in European grape cultivars and in most American rootstocks. Symptoms are expressed in V. rupestris and consist of clearing of the veins of third and fourth order resulting in localized translucent spots. Leaves with intense flecking are wrinkled, twisted, and may curl upward (Hewitt et al. 1962, 1972). The causal agent is Grapevine fleck virus (GFkV), the type species of the genus Maculavirus (Martelli et al. 2002). It has isometric particles with rounded contour and a prominent surface structure containing a single-stranded, positive-sense RNA genome (Boscia et al. 1991). These properties are shared by three additional viruses, i.e., Grapevine asteroid mosaic -associated virus (GAMaV), Grapevine rupestris vein feathering virus (GRVFV), and Grapevine redglobe virus (GRGV), which, together with GFkV, constitute the “fleck complex” (Martelli 2014).

Whereas historical data and other hints have allowed to hypothesize the geographical area of origin of the viruses involved in other disease complexes (infectious degeneration /decline, leafroll, and rugose wood ), such exercise does not seem applicable to the agents of the fleck complex. However, one can speculate that the substantial latency of these viruses in European grape cultivars may be indicative of their longer-lasting association with V. vinifera than with V. rupestris, an American species.

The Emergence of a DNA Virus and Pararetroviruses

Notwithstanding the intensive studies conducted in the major viticultural areas of the world, no virus other than those with a RNA genome had been detected up to a few years ago, although it had been known for some time that the genome of a clone of cv. Pinot noir incorporated fragments of DNA sequences of six different pararetroviruses, mostly of the genus Caulimovirus (Bertsch et al. 2009). The breakthrough came when next-generation sequencing revealed that vines affected by vein clearing and decline in the Midwest region of the USA hosted a Badnavirus (family Caulimoviridae) denoted Grapevine vein clearing virus (GVCV) (Zhang et al. 2011). This was soon followed by the discovery of (1) a putative member of the family Geminiviridae (Grapevine red blotch-associated virus, GRBaV) in vines showing a patchy discoloration of the leaves (red blotch ), first in the USA (12 different States throughout the country) and Canada (Krenz et al. 2012; Al Rawhanih et al. 2013; Poojari et al. 2013; Sudarshana et al. 2015; Xiao et al. 2015) and then in Switzerland (Reynard and Gugerli 2015), and (2) another badnavirus (Grapevine roditis leaf discoloration-associated virus, GRLDaV) in Greek vines affected by a foliar discoloration (Maliogka et al. 2015) and in a symptomless wine grape from southern Italy (Chiumenti et al. 2015). Not much is known on the epidemiology of these viruses, except for the claim that GRBaV is transmitted by the Virginia creeper leafhopper (Erythroneura ziczac) (Poojari et al. 2013) and more recently by the three-cornered alfalfa treehopper (Spissistilus festinus) (Bahder et al. 2016). The latter vector is likely of epidemiological importance. In fact, there is circumstantial evidence that GRBaV is spreading, as shown by its detection in free-living Vitis species, e.g., V. californica x V. vinifera hybrids (Perry et al. 2016). There is also evidence of the detrimental impact of GRLDaV and GRBaV on infected vines (Rumbos and Avgelis 1989; Qiu et al. 2007; Reynard and Gugerli 2015; Sudarshana et al. 2015).

GVCV, GRBaV, and GRLDaV are three of the 85 novel plant viruses discovered up to mid-2015 using a metagenomic approach (Roossinck et al. 2015).

Viroids

Viroids are subviral pathogens endowed with autonomous replication in their hosts. They are made up of a non-encapsidated circular RNA of 246–375 nts, a size much smaller than that of the smallest viral genome. Like viruses, viroids are classified in families, genera, and species. Two families are known, Pospiviroidae and Avsunviroidae, whose discriminating traits are the presence of a central conserved region in the secondary structure and nuclear replication (Pospiviroidae) or a branched secondary structure lacking the central conserved region, presence of ribozymes, and plastidial replication (Avsunviroidae). Until recently, five grapevine-infecting viroids were known, all belonging to the family Pospiviroidae: Grapevine yellow speckle viroid 1 (GYSVd-1) , Grapevine yellow speckle viroid 2 (GYSVd-2) , Australian grapevine viroid (AGVd) , Hop stunt viroid (HSVd) , and Citrus exocortis viroid (CEVd) (Little and Rezaian 2003). Latest additions to the grapevine viroid list are Grapevine latent viroid (GLVd) (Zhang et al. 2014) and a viroid-like RNA sharing structural features with members of the family Avsunviroidae, whose biological role in grapevines is yet to be ascertained (Wu et al. 2012). Only GYSVd-1 and GYSVd-2 are pathogenic to grapevines inducing a disease called yellow speckle (Taylor and Woodham 1972). Another disease known as “vein banding” (Goheen and Hewitt 1962) was proven to result from a mixed infection by these viroids and GFLV (Krake and Woodham 1983; Hajizaeh et al. 2015).

Detailed accounts on the major grapevine viruses, their relationship to the different diseases, their economic impact on the grape and wine industry, as well as their epidemiology , diagnosis , and control strategies are provided in this book in the individual chapters that follow. It is important to note that the situation with viruses, viroids, and the diseases they cause in grapevine is often complex, due in part to the large number of viruses and their wide range of genetic variants present in mixed infections, as well as to the combination of scion cultivars and rootstock genotypes in a finished vine used in commercial production.