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Ectomycorrhizal Fungal Diversity: Separating the Wheat from the Chaff

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Ectomycorrhizal Fungal Diversity: Separating the Wheat from the Chaff Fungal Diversity Reviews, Critiques and New Ideas Ectomycorrhizal fungal diversity: separating the wheat from the chaff Rinaldi, A.C. 1, Comandini, O. 1* , and Kuyper, T.W.2 1Department of Biomedical Sciences and Technologies, University of Cagliari, I -09042 Monserrato (CA), Italy 2Department of Soil Quality, Wageningen University, Box 47, 6700 AA Wageningen, The Netherlands Rinaldi, A.C., Comandini, O. and Kuyper, T.W. (2008) . Ectomycorrhizal fungal diversity: separating the wheat from the chaff. Fungal Diversity 33: 1 -45. Thousands of ectomycorrhiz al (ECM) fungal species exist, but estimates of global species richness of ECM fungi differ widely. Many genera have been proposed as being ECM, but in a number of studies evidence for the hypothesized ECM habit is lacking. Progress in estimating ECM speci es richness is therefore slow. In this paper we have retrieved studies providing evidence for the ECM habit of fungal species and for the identification of the mycobiont(s) in specific ECM associations, using published and web -based mycorrhiza literature. The identification methods considered are morpho - anatomical characterization of naturally occurring ECMs, pure culture synthesis, molecular identification, and isotopic evidence. In addition, phylogenetic information is also considered as a relevant criter ion to assess ECM habit. Of 343 fungal genera for which an ECM status has been alleged, about two thirds have supportive published evidence or ECM status can be at least hypothesized. For the remaining taxa, currently no indication exists as for their ECM nutritional habit, besides field observations of associations with putative hosts. Our survey clearly indicates that current knowledge of ECM fungal diversity, as supported by experimental evidence, is only partly complete, and that inclusion of many fungal genera in this trophic and ecological category is not verified at this stage. Care must thus be used when compiling lists of ECM and saprotrophic fungi in community -level studies on the basis of published information only. On the basis of our literature search we conservatively estimate ECM species richness around 7750 species. However, on the basis of estimates of knowns and unknowns in macromycete diversity, a final estimate of ECM species richness would likely be between 20000 and 25000. Key words: ec ological role, ectomycorrhizal (ECM) fungi, diversity, host specificity, trophic status Article Information Received 4 June 2007 Accepted 30 September 2007 Published online 30 November 2008 *Corresponding author: Ornella Comandini; e-mail: ornella_comand [email protected] Introduction symbiosis research pursues the understanding of the causes and consequences of ECM fungal The ectomycorrhizal (ECM) symbiosis species diversity (richness, species composi - represents one of the most prominent and tion) and of ECM fungal assemblages or ecologically crucial mutualistic associations in communities. There is increasing support for terrestrial habitats. This involves several the hypothesis that ECM fungal species thousands of species of fungi grouped within composition affects the structure of plant the phyla Ba sidiomycota, Ascomycota, and communities. ECM fungal diversity is shaped Zygomycota, and hundreds of mostly woody by a complex mix of abiotic a nd biotic factors. plant species worldwide; ectomycorrhizas One important biotic factor in this regard is that (ECMs) occur in most of the temperate and of host plant specificity or selectivity (Zhou boreal ecosystems and in large forested areas of and Hyde, 2001). The latter phenomenon can tropical and subtropical regions (Smith and be considered from either a “phytocentric” or Read, 1997; Cairney and Chambers, 1999; “mycocentric” point of view, i.e., emphasizing Verbeken and Buyck, 2001; Comandini et al., the fungal partners forming symbioses with a 2006; Wang and Qiu, 2006). particular plant taxon (the fungus as a suitable One of the most active lines of ECM and compatible partner for plants), or the 1 diversity of plant species with which a fungal Compilation of data on ECM associations species can form mycorrhiza (the plant as a Our data set on the ECM fungi contains compatible host) (Molina et al., 1992; van der information collated from a variety of Heijden and Sanders, 2002). Given the published and web -based sources. The primary ecological importance of host selectivity for list (Table 1) reports all fungal genera for plant communities and the associated fungal which the ECM symbiosis has been alleged, assemblages, studies describing such specific - regardless of putative or demonstrated plant ity or selectivity patterns in ecosystems are of host(s), which is not listed. Such information particular signif icance, as they can contribute was retrieved either from reviews of the to a better understanding of the environmental mycorrhizal status of fungal genera or from factors that affect species diversity over publications dealing with a limited number of ecological and evolutionary time scales. taxa. Studies addressing ECM diversity and Our analysis focuses on those works that host selectivity in a detailed and reliable provide some kind of evidential information. In manner can only stem from basic information the list presented in Table 1, the fungal genera on the trophic status of fungi in a given for which we conclude, on the basis of the ecosystem. Such knowledge is also needed for information presented, that they have an ECM investigating wider aspects of community habit are report ed in boldface. In these cases, ecology in habitats where fungi play a major the number of currently recognized species is role, and for interpreting the evolutionary reported, as retrieved from the Dictionary of history of fungi and their associated hosts. In Fungi (Kirk et al., 2001). Information for this other words, it is important to know which section was collated by browsing (up to June fungi are ECM and which are saprotrophic or 2008) web resources [Determination of possess a mixotrophic life style (Taylor and Ectomycorrhizae (DEEMY), http://www. Alexander, 2005; Koide et al. , 2008). It might deemy.de; Database of Descriptions of sound as a trivial matter, but it is not. Indeed, Ectomycorrhizae (DDE), http://dde.forrex.org despite over 100 years of investigation on the /biodiversity/ecto/index_e-html; UNITE, http:// subject, our knowledge of ECM -forming fungi hermes.zbi.ee; Mycorrhiza Literature Ex - is still rudimentary, and establishing the trophic change, http://mycorrhiza.ag.utk.edu], recent status of fungal species in the field often rev iews ( de Román et al., 2005; Agerer, 2006), remains a challenging task. specialized publications (e.g., Descriptions of We present here a critical re view of the Ectomycorrhizae), and the main mycological evidence available about the ECM status of and botanical journals. For those fungal genera fungal genera. Five different types of evidence (e.g., Lactarius, Rhizopogon, Russula , Suillus) are considered: i) morpho-anatomical for which a plethora of d ata supporting ECM characterization of naturally occurring ECMs; symbiosis are available, only representative ii) pure culture synthesis (including in articles are quoted. microcosms); iii) molecular i dentification; iv) Browsing the literature, one may isotopic evidence; v) phylogenetic evidence. encounter a number of other fungal genera for Owing to limitations of each method, we which the mycorrhizal status is strongly unlike highlight those genera for which several quoted as ECM. methods produce mutually reinforcing evidence of ECM status. The types of evidence, Results and Discussion and their accuracy and reli ability are also discussed. We also reflect on the issues ECM fungal richness and diversity whether the generic level is the appropriate Table 1 lists 343 genera in the level for analysis and on the problem of Ascomycota (84 genera), Basidiomycota (252), mixotrophy (a combination of the ECM and Zygomycota (five) and Incertae Sedis (two) for saprotrophic life style). We conclude our paper which the ECM status has been alleged. The with a revised estimate of the number of ECM number of enlisted genera exceed that reported fungal species. by other au thors who have earlier summarized the diversity of ECM fungi (Molina et al., Methods 2 Fungal Diversity 1992; Bougher, 1995; Brundrett et al., 1996; fungi has been overwhelmingly based on field Agerer, 2006). For 122 genera reported in observation of sporocarp associations with Table 1 (in boldface), hosting a total of ~7200 potential h osts, a practice inherently exposed to species, evidence of ECM status by two or a substantial degree of error (Trappe, 1962; mo re approaches is available. For 114 genera, 1969). More recently, the detailed study of the hosting ~550 species, relevant information on morpho-anatomical features of hundreds of ECM -forming ability stems from application of ECMs has been conducted , in large part a single criterion or ECM status can be at least following the standardized guidelines by hypothesized. Finally, for about one third of Re inhard Agerer (1986; 1987-2006; 1991a). listed genera (107, hosti ng ~4200 species) no Tracing mycelial connections between fruit - evidence was observed, although in many cases bodies and ectomycorrhizas is still the most these genera have been repeatedly reported to reliable way of assessing in the field the trophic have an ECM ecology (mostly on the ground of status of fungi. A recent survey by de Román consistent association of fruitbodies with a and colleagues (2005)
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