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How Many Fungi Make Sclerotia?

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How Many Fungi Make Sclerotia? fungal ecology xxx (2014) 1e10 available at www.sciencedirect.com ScienceDirect journal homepage: www.elsevier.com/locate/funeco Short Communication How many fungi make sclerotia? Matthew E. SMITHa,*, Terry W. HENKELb, Jeffrey A. ROLLINSa aUniversity of Florida, Department of Plant Pathology, Gainesville, FL 32611-0680, USA bHumboldt State University of Florida, Department of Biological Sciences, Arcata, CA 95521, USA article info abstract Article history: Most fungi produce some type of durable microscopic structure such as a spore that is Received 25 April 2014 important for dispersal and/or survival under adverse conditions, but many species also Revision received 23 July 2014 produce dense aggregations of tissue called sclerotia. These structures help fungi to survive Accepted 28 July 2014 challenging conditions such as freezing, desiccation, microbial attack, or the absence of a Available online - host. During studies of hypogeous fungi we encountered morphologically distinct sclerotia Corresponding editor: in nature that were not linked with a known fungus. These observations suggested that Dr. Jean Lodge many unrelated fungi with diverse trophic modes may form sclerotia, but that these structures have been overlooked. To identify the phylogenetic affiliations and trophic Keywords: modes of sclerotium-forming fungi, we conducted a literature review and sequenced DNA Chemical defense from fresh sclerotium collections. We found that sclerotium-forming fungi are ecologically Ectomycorrhizal diverse and phylogenetically dispersed among 85 genera in 20 orders of Dikarya, suggesting Plant pathogens that the ability to form sclerotia probably evolved 14 different times in fungi. Saprotrophic ª 2014 Elsevier Ltd and The British Mycological Society. All rights reserved. Sclerotium Fungi are among the most diverse lineages of eukaryotes with features such as a hyphal thallus, non-flagellated cells, and an estimated 5.1 million species (Blackwell, 2011). They are the the production of spores (Stajich et al., 2009). However, principle saprotrophs in most terrestrial biomes and play because of their cryptic lifestyles within environments such important ecological and economic roles as plant pathogens as plants and soil, the ecology and evolutionary history of and mutualists. Fungi are found in all terrestrial ecosystems many fungi remains poorly understood. and they use a variety of strategies to colonize appropriate Almost all fungi produce some type of durable, quiescent substrata and survive unfavorable conditions (Blackwell, microscopic structure such as a spore that is important for 2011). They have significant impacts on the biology of plants dispersal and/or survival under adverse conditions (Stajich because they are the most economically significant plant et al., 2009). However, some fungi also produce dense aggre- pathogens, serve as mycorrhizal and endophytic symbionts, gations of fungal tissue called sclerotia (Willetts, 1971). These and act as key players in nutrient cycles (Schumann, 1991; persistent structures help fungi to survive challenging con- Rodriguez et al., 2009; Hobbie and Hogberg, 2012). Two fun- ditions such as freezing temperatures, desiccation, microbial gal phyla, Basidiomycota and Ascomycota, comprise the attack, or the long-term absence of a host (Townsend and subkingdom Dikarya, a diverse group with ca. 100,000 Willetts, 1954; Coley-Smith and Cooke, 1971). Sclerotia are described species (James et al., 2006). Most Dikarya share key highly variable in their morphology (Fig 1). Some have a hard, * Corresponding author. Tel.: þ1 352 273 2837; fax: þ1 352 392 6532. E-mail address: trufflesmith@ufl.edu (M.E. Smith). http://dx.doi.org/10.1016/j.funeco.2014.08.010 1754-5048/ª 2014 Elsevier Ltd and The British Mycological Society. All rights reserved. Please cite this article in press as: Smith, et al., How many fungi make sclerotia?, Fungal Ecology (2014), http://dx.doi.org/ 10.1016/j.funeco.2014.08.010 2 M.E. Smith et al. Fig 1 e Morphologically variable sclerotia found in soil, leaf litter, and decayed wood in natural forest habitats of North and South America: (A) Ceriporia sp. (MES 332; Polyporales) from decayed wood on the forest floor in Pigsah National Forest, North Carolina, USA; (B) Entoloma sp. (MES 347; Agaricales) from soil in a tropical rainforest dominated by leguminous ectomycorrhizal trees, Guyana; (C) Cheilymenia sp. (MES 313; Pezizales) from soil in mixed woods near Cherryfield, Maine, USA; (D) unknown species of Amylocorticiales (MCA 3949) from soil and leaf litter in a tropical rainforest in Guyana; (E) Boletus sp. (MES 260; Boletales) from soil and leaf litter in angiosperm-dominated forest in Lexington, Massachusetts, USA. Identities of illustrated sclerotia were determined based on ribosomal DNA sequence comparisons with GenBank. Scale bars [ approximately 10 mm. melanized rind enclosing compact, undifferentiated hyphae fungi such as Sclerotinia sclerotiorum produce sexual fruiting while others lack a rind (Willetts, 1971). Some species make structures directly on sclerotia (Bolton et al., 2006) whereas round, determinate sclerotia but others have indeterminate others such as Pteromyces flavus (¼Aspergillus flavus) produce forms where the shape and size are influenced by resources fruiting bodies within sclerotia (Horn et al., 2009). Still others, and environmental conditions (Chet and Henis, 1975). Some such as Boletus rubropunctus, produce fruit bodies and sclerotia sclerotia are produced inside of host tissues; Claviceps purpurea at different times or in different places (Smith and Pfister, produces sclerotia in grass florets after it has destroyed the 2009). plant cells (Douhan et al., 2008) and Ophiocordyceps sinensis Although sclerotia have been documented in several fun- colonizes caterpillars and transforms their tissues into a gal lineages, sclerotium formation is primarily recognized as a sclerotium (Xing and Guo, 2008). In contrast, some fungi make key life history trait in several necrotrophic plant pathogens sclerotia that are spatially separated from hosts (e.g. Phyma- (e.g. Sclerotium rolfsii, Rhizoctonia solani, M. phaseolina, P. omni- totrichopsis omnivora forms sclerotia deep in soil e Lyda, 1984). vora, S. sclerotiorum). Collectively, these devastating host gen- Sclerotia also range in size from “microsclerotia” <1mm eralist pathogens are responsible for hundreds of millions of across, as in the plant pathogen Macrophominia phaseolina dollars in global crop losses annually (Aycock, 1966; Parmeter, (Short and Wyllie, 1978), to the massive sclerotia of Polyporus 1971; Purdy, 1979; Mulrean et al., 1984). For example, S. scle- mylittae that reach over 40 cm in diameter (Macfarlane et al., rotiorum and S. rolfsii each attack >400 plant species, including 1978). Sclerotia putatively serve a resource-storage and sur- major crops such as peanuts, potatoes, and soybeans, and can vival role in all sclerotium-forming fungi. However, some cause up to 100 % yield losses (Jenkins and Averre, 1986; Please cite this article in press as: Smith, et al., How many fungi make sclerotia?, Fungal Ecology (2014), http://dx.doi.org/ 10.1016/j.funeco.2014.08.010 How many fungi make sclerotia? 3 Bowen et al., 1992; Cintas and Webster, 2001). For these and schematic phylogeny based on Hibbett et al. (2007) with phy- other sclerotium-forming pathogens, survival is tightly linked logenetic positions of new or revised orders inferred from with sclerotium formation so sclerotia eradication is critical LoBuglio and Pfister (2010), Schoch et al. (2009a, 2009b), Binder for disease control (Coley-Smith and Cooke, 1971). Fur- et al. (2010), Zhang et al. (2011), Toome et al. (2013), Boehm thermore, the ecology of these fungi cannot be fully under- et al. (2009), Campbell et al. (2009), and Padamsee et al. stood without understanding the biology of sclerotium (2012). All but two fungal species, Magnaporthe salvinii and formation. Verticilium dahliae, were easily resolved at the ordinal level Although management of serious plant pathogens is an based on data from published references (Table 2) and Index important rationale for studying sclerotium formation, there Fungorum (www.indexfungorum.org/). are nevertheless several other compelling reasons. First, We documented reports of sclerotium formation in species many sclerotia lie dormant in soil, leaf litter, or wood for from 85 fungal genera in at least 20 orders of Basidiomycota months, so they must survive attacks from a wide variety of and Ascomycota (Table 2, Fig 2). Since only one representative natural enemies, including bacteria, other fungi, and inver- sclerotium-forming species from each genus was recorded, tebrates (Willetts, 1971; Papavizas, 1977; Matsumoto and we cannot accurately estimate the number of sclerotium- Tajimi, 1985). The mechanisms that allow sclerotia to sur- forming species. However, we observed that many genera vive in soil despite ongoing biotic assault are not well known, with one sclerotium-forming species also contain others. but evidence from well-studied species (e.g. S. sclerotiorum, C. Also, despite our limited sampling of sclerotia, we found a purpurea) suggests that most sclerotia contain biologically wide diversity of sclerotium-forming fungi in nature and active secondary metabolites (Morrall et al., 1978; Demain, documented at least three genera for which sclerotium for- 1999; Schardl et al., 2006; Ikewuchi and Ikewuchi, 2008; mation had not previously been reported, Ceriporia (Poly- Frisvad et al., 2014). Since different
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