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Are ericoid and ectomycorrhizal fungi part of a common guild?

2004; Wiley; Volume: 164; Issue: 1 Linguagem: Inglês

10.1111/j.1469-8137.2004.01180.x

1469-8137

Trude Vrålstad,

Plant Pathogens and Fungal Diseases

The ectomycorrhizal (ECM) and ericoid mycorrhizal (ERM) symbioses have commonly been thought to involve different sets of fungi (Smith & Read, 1997). While ECM fungi have been studied and recognized mainly as basidiomycetes, ERM fungi have predominantly been identified as a restricted group of ascomycetes. In the latter group, Hymenoscyphus ericae represents the most extensively studied model taxon for the ecology and function of the ericoid mycorrhizal symbiosis (Smith & Read, 1997; Read & Perez-Moreno, 2003). Molecular studies have blurred the well established distinction between ECM and ERM fungi, partly because H. ericae has been recognized as being part of a larger fungal complex (cf. the H. ericae aggregate; Vrålstad et al., 2000), with a steadily growing range of closely related genotypes detected in ERM and ECM partnerships worldwide (e.g. Vrålstad et al., 2000, 2002b; Allen et al., 2003; Cairney & Meharg, 2003; Rosling et al., 2003; Haug et al., 2004). The hypothesis that ERM and ECM plants may share common mycorrhizal partners (Vrålstad et al., 2000) has been supported by observations of identical fungal genotypes in roots of coexisting ERM and ECM hosts (Bergero et al., 2000; Vrålstad et al., 2002b), but conclusive evidence has, until now, been missing. In pages 183–192 of this issue, Villarreal-Ruiz et al. demonstrate for the first time that a single fungal mycelium can develop ERM and ECM simultaneously. This raises a serious question mark over the ‘accepted wisdom’ that ericoid and ectomycorrhizal fungi represent separate fungal guilds (see also Cairney & Meharg, 2003). Read (1991) recognized that major global gradients and general climatic and edaphic conditions in nature have led to a selection of distinctive types of mycorrhiza that predominate in different biomes. It is, therefore, easy to understand the differences in the ERM and ECM research fields. ERM research has largely focused on heathlands and extreme ecosystems where ericaceous hosts predominate, and ECM research has for the same reasons focused on woodlands. In ERM research, isolates of H. ericae and Oidiodendron spp. have become the most extensively used model fungi, while a limited group of readily cultivable ECM-forming basidiomycetes have served as ECM models (Read & Perez-Moreno, 2003). The ERM models exhibit enzymatic capabilities comparable to brown-rot fungi, and also possess an impressive resistance to heavy metals. They are therefore thought to play a key role in host nutrient acquisition and protection in nutrient poor heathlands and other stressed and toxic habitats dominated by ericaceous plants (Cairney & Meharg, 2003; Read & Perez-Moreno, 2003). In ECM research, some of the model fungi also exhibit saprotrophic capabilities, but commonly not to the extent observed in the ERM model fungi. A large number of studies have uncovered an enormous below-ground diversity of ECM fungi (cf. Horton & Bruns, 2001) and brought new understanding to the functional role of ECM relationships in temperate and boreal forests (Lindahl et al., 2002; Read & Perez-Moreno, 2003). However, there is a major deficiency among mycorrhizal studies in acknowledging that ERM plants and associated fungi predominate in the woodland understorey of several characteristic temperate and boreal forest habitats. Formation of ECM has traditionally been associated with a number of sporocarp-producing basidiomycetes (Molina et al., 1992), and earlier studies of ECM communities were described on the basis of above-ground sporocarp formation. The past eight years of molecular diversity studies have demonstrated a considerable lack of correspondence between the above-ground community of ECM sporocarps and the below-ground community of fungi involved in ECM root tips (cf. Horton & Bruns, 2001). Molecular identification approaches have also added a significant number of fungal taxa to the list of ECM-formers, including representatives of the ascomycete lineage previously thought exclusively to include ERM fungi (cf. the H. ericae aggregate; Vrålstad et al., 2000, 2002b). In ERM research, isolation of fungal cultures from hair roots has served as the method for identification of fungal partners. Numerous molecular studies have detected a much larger genetic diversity of the ERM fungal isolates than previously envisaged (cf. Cairney & Meharg, 2003), still predominantly within the Helotiales (Ascomycota). However, identification based on fungal cultivation only yields cultivable fungi. Consequently, through apparent circular reasoning the common view has been established that ERM fungi merely comprise readily cultivable ascomycetes (Smith & Read, 1997; Read & Perez-Moreno, 2003). Only a fraction of the thousands of known ECM-forming fungi are readily cultivable, and these possess according to Read and Perez-Moreno (2003) probably more ‘decomposer’ capabilities than the numerous non-cultivable ECM mutualists. Could this also apply for the ERM mutualists? Allen et al. (2003) recently demonstrated that the ericoid culture identification concept probably maintains a serious identification bias. They showed that conventional culturing from hair roots of the North American ericoid shrub Gaulteria shallon predominantly detected the ascomycetes H. ericae and Capronia spp., while direct DNA extraction revealed that Sebacina-like genotypes dominated the fungal community of the hair roots. Combined with earlier reports and observations, this strongly suggested that basidiomycetes of the Sebacina complex must be included in the group of ERM-forming fungi. As a parallel story to the H. ericae aggregate of the Ascomycota, the Sebacina-complex of the Basidiomycota apparently includes a broad range of closely related genotypes that are involved in ERM (Allen et al., 2003), ECM (Selosse et al., 2002a; Urban et al., 2003) as well as orchid mycorrhizal partnerships (Selosse et al., 2002b). Phylogenetic analysis based on nuclear ribosomal internal transcribed spacer (ITS) sequences recognize the H. ericae aggregate (Vrålstad et al., 2000) as a monophyletic unit consisting of some well supported clades with numerous closely related genotypes. The clade including Cadophora finlandia (previously Phialophora finlandia) is dominated by ECM-forming isolates. Similarly, ERM isolates are concentrated in the H. ericae clade (Vrålstad et al., 2002a, 2002b). Cadophora finlandia has earlier been reported to form ECM, ectendomycorrhiza (ECEM) and intracellular hyphal coils resembling ERM with respective hosts (see Villarreal-Ruiz et al.). Identical C. finlandia-like genotypes were also isolated from co-occurring ECM and ERM roots (Vrålstad et al., 2002b), and the ERM isolate was later confirmed to form ECM with Pinus sylvestris in vitro (T. Vrålstad, unpublished). All these reports strongly suggest that C. finlandia-like fungi may act as ERM and ECM partners simultaneously. Conclusive evidence for this assumption is presented for the first time by Villarreal-Ruiz et al. They demonstrate that a single isolate from the C. finlandia clade, simultaneously in time and from a continuous mycelium, develops structurally and apparently complete ERM (intracellular coils) with Vaccinium myrtillus and ECM (Hartig net and mantle) with P. sylvestris. The fungal colonization induced a substantial growth response in V. myrtillus roots, and no sign of pathogenic reactions were observed in any of the host plants. The functional aspects of this intriguing triangular relationship are beyond the scope of their study, and important questions about possible mutual benefit to all involved partners (cf. Read, 2000) still remain unanswered. However, demonstrating that a single mycelium is compatible with ERM and ECM roots (i.e. developing the characteristic ERM and ECM organs) is a breakthrough in the ongoing debate and an important encouragement for initiating further research on the ecological, evolutionary and functional relevance of this fungal bridge between ERM and ECM hosts. Judging from the divergent groups of fungi involved in ERM symbioses (cf. Allen et al., 2003), the ERM strategy has probably evolved independently in several fungal lineages. However, the H. ericae aggregate and particularly the C. finlandia clade represent one of the evolutionary links between ECM and ERM strategies. The predominantly ectomycorrhizal C. finlandia clade may be ancestral to the H. ericae clade, which seems more specialized on ERM. This aggregate may provide the key to a better understanding of the evolution of ERM, and potential switches between ECM and ERM. However, the results reported by Villarreal-Ruiz et al. emphasize that from the fungal point of view distinguishing between these strategies may not always be justified. More studies are required before we can predict whether host-specific and/or habitat-specific lineages have evolved within the H. ericae aggregate, or if these fungi are to a major extent compatible with a large range of hosts and habitats worldwide. By referring to how spruce planted into heathland ecosystems commonly show pathogenic reactions, Read (2000) argued that even though sharing of fungal symbionts between ECM trees and ERM shrubs may occur, it is open to considerable doubt as to what extent this is to the benefit of both host plants. There are probably several complex reasons why out-planted spruce seedlings may face severe problems in heathland soils. However, studies on the functional relevance of a shared fungus and the potential mutual benefit to all involved partners should select habitats where ECM and ERM hosts and fungi naturally co-occur. Interestingly, and of significant relevance to the discussion, the C. finlandia-like isolate used by Villarreal-Ruiz and colleagues had been isolated from an ECM root tip of P. sylvestris in a 160-year-old woodland where ECM and ERM plants (including V. myrtillus) naturally co-occur. In this respect, their study is a legitimate reminder of the highly unexplored role of ERM in the boreal woodland understorey. Boreal and temperate woodlands are commonly characterized by an overstorey of coniferous trees with an understorey of ericaceous hosts. In Mediterranean mature Quercus ilex woodland devoid of ericaceous hosts, Bergero et al. (2003) used Erica arborea as a ‘bait’ plant (a native ericaceous hosts dominating in earlier successional stages). They found that the Mediterranean woodland soil contained an effective and diverse inoculum of fungi forming ERM with E. arborea. Interestingly, none of the ERM-forming fungi represented the taxa that we typically perceive as ERM fungi, such as H. ericae and Oidiodenron spp. Instead, the ERM woodland inoculum represented unknown genotypes from different classes of ascomycetes (Leotiomycetes and Dothideomycetes). One possibility is that the ERM fungi persist in soils as saprotrophs, but another alternative is that the ericoid hosts take advantage of the community of ECM fungi that is present (Bergero et al., 2000, 2003). This study suggests that the fungi predominating in ERM relationships may vary significantly between different biomes. Boreal forests cover c. 17% of the global land surface and represent a biome where organic matter accumulates due to low temperatures and recalcitrant conifer and ericaceous litter rich in polyphenolic compounds (cf. Lindahl et al., 2002). Nutrient and carbon cycling in these systems depend heavily on saprotrophic and mycorrhizal fungi (Lindahl et al., 2002; Read & Perez-Moreno, 2003). While the diversity and density of ECM fungi in boreal forests is huge and relatively well studied (Taylor et al., 2000; Horton & Bruns, 2001), we currently know very little about the fungi involved in woodland ERM relationships despite the significant abundance of ericaceous hosts. For example, Norway spruce-dominated bilberry woodland (Fig. 1) characterized by Picea abies (Norway spruce) and a persistent understorey predominated by V. myrtillus (bilberry) is by far the most common forest type in Norway, covering 35% of the productive forest area (Larsson et al., 1994). Bilberry, in terms of plant individuals and biomass (above- and below-ground) evidently possesses a significant role here (cf. Figure 1). It was from a similar boreal habitat that Villarreal-Ruiz et al. captured their ECM- and ERM-forming C. finlandia isolate. In a biome where light might be a limiting factor for understorey vegetation, the possibility that ectomycorrhizal trees and ericoid shrubs may be physically interconnected via common mycorrhizal networks (CMN) is intriguing. A fungal link would provide a theoretical canal for transfer of carbon, which is possible between different ECM species in the field (Simard et al., 1997), as well as between ECM species and specialized mycoheterotrophic plants (Leake, 1994). (a–d): Norway spruce dominated bilberry woodland represents a common natural North boreal forest habitat of intimately coexisting ectomycorrhizal trees and ericoid mycorrhizal shrubs. This woodland is characterized by an overstorey of Picea abies (Norway spruce) and a persistent understorey predominated by Vaccinium myrtillus (bilberry) (a–c). Bilberry is a low-growing deciduous shrub of the family Ericaceae that is native to northern Europe. Ripe bilberry fruits (d) are among the most valuable, tasty and appreciated boreal forest berries. Photos: Trude Vrålstad (a–c) and Leif Ryvarden (d). For the development of a mycorrhizal organ, temporally and spatially controlled activity of genes and proteins participating in morphogenetic processes are required (Martin et al., 2001). For successful mycorrhizal development, the plant and fungal partner have to recognize each other and communicate. Understanding the molecular basis for the development of mycorrhizas requires studies of gene expression and cell-to-cell communication between fungi and roots (Tagu et al., 2002). A fungus possessing the ability to communicate both with ERM and ECM hosts is a highly interesting study system. Eliminating the problem with fungal taxon-related bias, a model fungus of the caliber found by Villarreal-Ruiz and colleagues should allow studies on the gene-regulated differences and similarities that are involved in the development of the structurally different ERM and ECM organs. Clearly, the results presented by Villarreal-Ruiz et al. should encourage creative studies and experiments across several sectors of the mycorrhizal research field.