Abstract
South America is undoubtedly the cradle of orchid diversity. However, few aspects of the biology of this plant group have been explored in the region. Orchids establish an important relationship with fungi that supply them with nutrients in the early stages of development to stimulate the germination of their tiny seeds. These fungi are called orchid mycorrhizal fungi (OMF), and their interaction with orchids forms a particular group of mycorrhizae: the orchid mycorrhiza (OM). In this chapter, we present the advances of the research conducted in South America, which explores some aspects of this interesting interaction. We have noticed that most studies on OM are academic documents deposited in university library repositories or published in local scientific journals. About half of the studies have focused on determining the diversity of OMF associated with a few orchid species of interest. Studies of phylogeny, morphological, and symbiotic seed germination are other of the main topics addressed. Research on ultrastructure and community ecology is hardly representative, while evolutionary implications, mutualistic networks, and metabolic aspects are the least explored topics. We encourage collaborations with the international scientific community to continue investigating complex questions that allow us to understand the role of mycorrhizas in the evolutionary success of tropical orchids. Moreover, we believe that it is important to propose attractive research that generates interest not only in the academic community but also in ordinary people who have traditionally been related to orchids (e.g., growers) in order to develop the enormous potential of the region in this field.
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8.1 Introduction
Orchids have fascinated enthusiasts and naturalists since at least the end of the eighteenth century (Cullen 1992). Certainly, Darwin’s work (1862) inspired by highly specialized floral adaptations for attracting, deceiving, and manipulating insects to promote allogamy (Dressler 1981) was one of the most interesting and stimulating approaches for future generations of researchers. In addition, with about 30, 000 species and a worldwide distribution, Orchidaceae is the second most diverse family among angiosperms (Bánki et al. 2021). Its amazing floral shapes as well as the intricate relationships with both pollinators and mycorrhizal fungi make this plant group one of the most bizarre throughout the plant kingdom.
Among mycorrhizal associations (Peterson et al. 2004; Smith and Read 2010), orchid mycorrhiza (OM) is a special type that only occurs within Orchidaceae. Since orchids form minute seeds (like dust) with a reduced endosperm (Fig. 8.1) in natural conditions, they need a fungal partner that provides the organic source to support the germination and seedling establishment (Bernard 1904; Rasmussen 1995; Brundrett 2017). This symbiosis is recognized for the formation of complex hyphal coils called pelotons within the root cortex tissue (Peterson et al. 2004; Zettler and Corey 2018) (Fig. 8.2).
In early stages of development, the plants are entirely dependent on the supply of nutrients and carbon by the orchid mycorrhizal fungi (OMF). In later stages, most species become green plants (i.e., photosynthetic orchids), and some species can obtain additional carbon supplies from fungi that remain until the adult stage. This mode of nutrition in which the plant gains carbon simultaneously from two sources, its own photosynthesis and the fungal supply, is called partial mycoheterotrophy (Leake 1994; Gebauer 2018) (some authors use also the term mixotrophy; see Selosse et al. (2016)). In a broad sense, all orchid species are mycoheterotrophic in some state of the life cycle. Those species without chlorophyll as adults (i.e., non-photosynthetic orchids), which entirely rely on fungi throughout their lives for mineral and carbon nutrition, are called fully mycoheterotrophic orchids (Gebauer 2018).
Photosynthetic orchids are generally associated with fungi of the Rhizoctonia complex. This group consists of a phylogenetic heterogeneous assemblage that includes saprophytic, parasite, and endophyte species. Orchids also form mycorrhizas with fungi mainly included in the genera Ceratobasidium, Tulasnella, Sebacina, and Serendipita (Suárez et al. 2008; Taylor and McCormick 2008; Kottke and Suárez 2009; Weiß et al. 2016; Fritsche et al. 2021). On the other hand, partially mycoheterotrophic orchids, as well as fully mycoheterotrophic orchids, are associated with ectomycorrhizal fungi (Russula, Thelephora, Tomentella) of other nearby plants or with saprotrophic fungi (Resinicium, Gymnopus, and Mycena) (Martos et al. 2009; Zettler and Corey 2018).
Bernard (1904) reported the first record of mycorrhizal associations in orchids with Rhizoctonia-like fungi and proposed the first techniques for the cultivation of these fungi from sections of infected roots to promote seed germination. Morphologically, members of Rhizoctonia group share some common traits: hyphae without clamp connections branched at right angles, constriction of the hyphal branch, a septum close to the bifurcation site, and production of chains of swollen monilioid cells (Fig. 8.3). Detailed studies such as nuclear condition, septal ultrastructure, enzymatic activity, and the formation of anastomosis groups (Suárez et al. 2006, Suryantini et al. 2015, Thakur et al. 2018, Sathiyadash et al. 2020, Ghirardo et al. 2020, Nandeesha et al. 2021) can provide more taxonomic confidence. In addition, advances in molecular techniques have facilitated the identification of OMF mainly through sequencing of the internal transcribed spacer (ITS) region of ribosomal DNA (Kristiansen et al. 2001; Taylor and McCormick 2008; Kottke and Suárez 2009; Yokoya et al. 2015; Fritsche et al. 2021).
An extensive literature has been published about the structure of orchid mycorrhiza, mechanisms of attraction, infection, nutrient exchange, phylogeny, and isolation techniques (Peterson et al. 2004; Smith and Read 2010; Dearnaley et al. 2012, 2016; Selosse et al. 2016; Swarts and Dixon 2017; Zettler and Corey 2018). Most of the knowledge on this topic comes from studies conducted in temperate ecosystems with terrestrial orchids (Kristiansen et al. 200; Gebauer and Meyer 2003; Bonnardeaux et al. 2007; Roche et al. 2010; Waterman et al. 2011; Jacquemyn et al. 2014, 2015; Těšitelová et al. 2015). In this chapter, a synopsis of the relevant literature on the interactions between OMF and their host plants in subtropical and tropical regions from South America is presented. After that, some perspectives and potential collaborations will be discussed.
8.2 Studies on Orchid Mycorrhizae in South America
A great majority of studies on OM in South America are academic documents named as “gray” literature and deposited in the repositories of university libraries. Others are published in local scientific journals written in native languages (e.g., Spanish, Portuguese). We have compiled the studies conducted in Brazil, Colombia, and Ecuador (Table 8.1), where it was possible to identify the taxon or taxa of the orchids studied, the methods for the identification of mycorrhizal fungi, and their taxonomic determination. The names of the orchid and fungal species were preserved as reported. The contribution of OMF of other countries in the tropical region of South America (Venezuela, Guyana, Surinam, French Guyana, Perú, Bolivia) has been limited or is not available to consult.
Pioneering studies on OM in tropical zones of South America were presented in the early twenty-first century by Díaz et al. (2000) in Colombia, when they were exploring the mycorrhizal associations in several orchid species. This study used morphological traits of mycelium to identify the fungal partner as Rhizoctonia for all species, although the main aim of the research was to identify what type of plant secondary metabolites was producing in the tissues where the endophytes were found. Around the same time, in Brazil, the first studies on orchid mycorrhizae were beginning in the laboratory of Professor Maria Catarina Megumi Kasuya of the Federal University of Viçosa. This time, it included, in addition to morphological characterizations, genetic information (ITS sequencing and RAPDs) (Pereira 2001). The interest in this subject in the country then expands, resulting in several researches throughout the next decade (Table 8.1). Around 2002, in Colombia, mycorrhizal interactions began to be explored in economically important species such as Vanilla planifolia (Ordóñez et al. 2012), and, under the guidance of the second author of this chapter from the National University of Colombia, an important field of research in the country was opened, resulting in multiple studies (Table 8.1). Although Colombia and Brazil were the pioneer countries, Ecuador has established itself as the leading country in research on OMF in the region. Many of the studies carried out in this country are rigorous investigations that have been published in scientific journals (unlike Brazil and Colombia, where many reports are part of gray literature). Professor Juan Pablo Suárez from Universidad Técnica Particular de Loja (Ecuador) as the leader in this field with the academic collaboration of Professor Ingrid Kottke (University Tübingen, Germany) has proposed a more evolutionary and ecological perspective on this type of association, including detailed ultrastructural analyses by transmission electron microscopy and community ecology approaches (Kottke et al. 2008a; Kottke and Suárez 2009; Kottke et al. 2013; Suárez and Kottke 2016).
The initial studies identified the fungi associated with orchids from the isolation of the mycelium that was morphologically characterized (Díaz et al. 2000; Pereira 2001). This approach required a great knowledge of fungi or the consultation to experts and did not provide very precise determinations due to the lack of reliable taxonomic characters to reach the species level, which would only be possible by obtaining the teleomorph or sexual phase of the isolated strain. In the region, unlike the temperate zones, obtaining teleomorphs was not a method addressed among the scientific community. With advances in molecular biology, the first genetic identifications were made with the random amplified polymorphic DNA (RAPD) and restriction fragment length polymorphism (RFLP) methods (Pereira 2001, Pereira et al. 2005a). Later, with the new findings on Sanger sequencing and the primers designed to capture the genetic information of the groups of mycorrhizal fungi frequently found in orchids (Kristiansen et al. 2001, Taylor and McCormick 2008), many researchers bypassed the time-consuming phase of isolation of mycelium in vitro to obtain the genetic information from root tissues infected with orchid mycorrhiza, verifying the presence of pelotons (Suárez et al. 2006; Kottke et al. 2008b; Suárez et al. 2008; Kottke et al. 2010; Oliveira 2012; Valadares et al. 2012; Alomía et al. 2017). The most studied genes are those of the nuclear ribosomal internal transcribed spacer (nrDNA ITS) gene and to a lesser extent those of the mitochondrial large subunit ribosomal (mtLSU) and nuclear large subunit ribosomal (nucLSU) regions. Sanger sequencing is the most widespread approach and is still used today for studies in which the strains are not required to be used in germination experiments or to be conserved in mycelium banks for later purposes. Although recent next-generation sequencing (NGS) techniques with Illumina technology offer more complex and robust information on fungi associated with orchids (Cevallos et al. 2016, 2018), this approach is not the most used due to the costs involved, which are not necessarily within the common financial source availability of researchers from developing countries in the region.
8.3 Research Interests
Some studies explored more than one topic in relation to the fungus-orchid associations. However, most studies (46%) have been focused on determining the diversity of OMF associated with few orchid species of interest. Phylogeny, morphological, and symbiotic seed germination studies are other of the main topics addressed (16%, 12%, and 11%, respectively). Ultrastructure and community ecology researches are hardly representative (6%), while evolutionary implications, mutualistic networks, and metabolic aspects are the least explored topics (1%) (Fig. 8.4). We did not find studies aimed at understanding physiological topics of the OMF-orchid interaction.
These data indicate that basic questions are still being asked in the region as most of the studies describe the diversity of fungi associated with orchids. Few studies ask analytical questions that lead to a better understanding of the interactions between orchids and fungi. This may in part because a low resource availability limits the development of complex issues, such as those related to physiological or biochemical effects on each partner. Since the biodiversity of orchids in tropical South America is so extensive, the knowledge of OMF diversity is far from complete.
8.4 Challenges and Perspectives
Surprisingly, in tropical regions of South America where the Orchidaceae is especially diverse (Meisel et al. 2015; Kirby 2016), studies on orchid mycorrhiza symbiosis are underrepresented. However, in the last 20 years, the interest in endophytic orchid fungi, both mycorrhizal and non-mycorrhizal, has increased in the region (Herrera et al. 2010; Hernández and Alomía 2020).
Future directions for OMF include: (i) The developing of a broader understanding of OMF. Although most studies focus on fungal diversity, they do not understand the evolutionary implications of the orchids and OMF relationship. We encourage collaborations with the international scientific community to continue investigating complex questions that allow us to understand the role of mycorrhizae in the evolutionary success of tropical orchids. (ii) The developing of new fungal culture techniques to be able to use OMF in bioassays since many OMFs are difficult to grow under in vitro conditions. (iii) To publish for a wider audience. We found that most of the studies are in the “grey” literature. For this, it is necessary to generate innovative research that sparks interest in the academic community. (iv) The application of the information produced on OMF for orchid conservation, orchid propagation, and plant protection (Otero et al. 2013). Orchid conservation programs rarely use OMF technologies to propagate endangered orchids. Similarly, orchid growers do not use OMF for propagation. To develop the enormous potential of the region in the cultivation of orchids, we invite companies interested in the production of orchids such as “Ecuagenera” in Ecuador, “Lima Orquídeas” in Perú, and “Colombo Orquídeas,” “Orquídeas del Valle,” “Orquídeas Eva,” and “Libia Orquídeas” in Colombia, to be linked with the academy so that through research projects, added value will be generated in their business. More specifically, the use of mycorrhizae in the cultivation of orchids can contribute to enhancing production and reducing costs in sexual propagation (seeds) represented by asymbiotic media. Furthermore, OMF could also reduce the development time for flower production, generating significant financial gain for orchid sellers.
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Alomía, Y.A., Otero, J.T. (2022). Orchid Mycorrhizas in South America: Tropical and Subtropical Ecosystems. In: Lugo, M.A., Pagano, M.C. (eds) Mycorrhizal Fungi in South America. Fungal Biology. Springer, Cham. https://doi.org/10.1007/978-3-031-12994-0_8
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