Evolution Of Habitat Preference And Nutrition Mode In A Cosmopolitan Fungal Genus With Evidence Of Interkingdom Host Jumps And Major Shifts In Ecology

Evolution

Volumn 67, Issue 10, 2013, Pages 2823-2837

  Chaverri, Priscila ^a   Samuels, Gary J ^b  

^a UNIVERSITY OF MARYLAND   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

Adaptive radiation; Ascomycota; Horizontal gene transfer; Hypocrea; Phylogenetics; Speciation

Indexed keywords

ADAPTIVE RADIATION; ANCESTRY; BIOLOGICAL CONTROL; EVOLUTIONARY BIOLOGY; FUNGUS; HABITAT SELECTION; HOST-PARASITE INTERACTION; MYCOPARASITE; NUTRITION; PARASITISM; PHYLOGENETICS; SAPROTROPHY; SPECIATION (BIOLOGY);

ASCOMYCOTA; FUNGI; HYPOCREA; TRICHODERMA;

PRIMER DNA;

ADAPTIVE RADIATION; ARTICLE; ASCOMYCETES; BAYES THEOREM; BIOLOGICAL MODEL; CYTOLOGY; DNA SEQUENCE; ECOSYSTEM; EVOLUTION; FRUITING BODY; GENETIC SELECTION; GENETICS; HORIZONTAL GENE TRANSFER; HYPOCREA; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; NUTRITION; PHYLOGENY; PHYSIOLOGY; SPECIES DIFFERENTIATION; STATISTICAL MODEL; SYMBIOSIS; TRICHODERMA;

ADAPTIVE RADIATION; ASCOMYCOTA; HORIZONTAL GENE TRANSFER; HYPOCREA; PHYLOGENETICS; SPECIATION;

BASE SEQUENCE; BAYES THEOREM; BIOLOGICAL EVOLUTION; DNA PRIMERS; ECOSYSTEM; FRUITING BODIES, FUNGAL; GENETIC SPECIATION; LIKELIHOOD FUNCTIONS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; NUTRITIONAL PHYSIOLOGICAL PHENOMENA; PHYLOGENY; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA; SOIL MICROBIOLOGY; SYMBIOSIS; TRICHODERMA;

EID: 84885057683     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12169     Document Type: Article

References (131)

1. Alfaro, M. E., F. Santini, C. Brock, H. Alamillo, A. Dornburg, D. L. Rabosky, G. Carnevale, and L. J. Harmon 2009. Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proc. Natl. Acad. Sci. 106:13410-13414.
2. Argumedo-Delira, R., A. Alarcon, R. Ferbera-Cerrato, and J. J. Pena-Cabriales 2009. The fungal genus Trichoderma and its relationship with organic and inorganic pollutants. Rev. Int. Contam. Ambient. 25:257-269.
3. Arnold, A. E., L. C. Mejia, D. Kyllo, E. I. Rojas, Z. Maynard, N. Robbins, and E. A. Herre 2003. Fungal endophytes limit pathogen damage in a tropical tree. Proc. Natl. Acad. Sci. 100:15649-15654.
4. Arnold, A. E., J. Miadlikowska, K. L. Higgins, S. D. Sarvate, P. Gugger, A. Way, V. Hofstetter, F. Kauff, and F. Lutzoni 2009. A phylogenetic estimation of trophic transition networks for ascomycetous fungi: are lichens cradles of symbiotrophic fungal diversification? Syst. Biol. 58:283-297.
5. Bae, H., R. C. Sicher, M. S. Kim, S. H. Kim, M. D. Strem, R. L. Melnick, and B. A. Bailey 2009. The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. J. Exp. Bot. 60:3279-3295.
6. Bailey, B. A., H. Bae, M. D. Strem, J. Crozier, S. E. Thomas, G. J. Samuels, B. T. Vinyard, and K. A. Holmes 2008. Antibiosis, mycoparasitism, and colonization success for endophytic Trichoderma isolates with biocontrol potential in Theobroma cacao. Biol. Control 46:24-35.
7. Bazinet, A. L., and M. P. Cummings 2008. The Lattice Project: a grid research and production environment combining multiple grid computing models in M. H. W. Weber, ed. Distributed & grid computing-science made transparent for everyone. Rechenkraft.net.
8. Berg, G., C. Zachow, J. Lottmann, M. Gotz, R. Costa, and K. Smalla 2005. Impact of plant species and site on rhizosphere-associated fungi antagonistic to Verticillium dahliae Kleb. Appl. Environ. Microbiol. 71:4203-4213.
9. Blackwell, M. 2011. The Fungi: 1, 2, 3 .. 5.1 million species? Am. J. Bot. 98:426-438.
10. Carbone, I., and L. M. Kohn 1999. A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91:553-556.
11. Carroll, G. C. 1988. Fungal endophytes in stems and leaves: from latent pathogen to mutualistic symbiont. Ecology 69:2-9.
12. Cavender-Bares, J., K. H. Kozak, P. V. A. Fine, and S. W. Kembel 2009. The merging of community ecology and phylogenetic biology. Ecol. Lett. 12:693-715.
13. Chaverri, P., and G. J. Samuels 2003. Hypocrea/Trichoderma (Ascomycota, Hypocreales, Hypocreaceae): species with green ascospores. Stud. Mycol. 48:1-116.
14. Chaverri, P., and B. Vílchez 2006. Hypocrealean (Hypocreales, Ascomycota) fungal diversity in different stages of succession in a tropical forest in Costa Rica. Biotropica 38:531-543.
15. Chaverri, P., L. A. Castlebury, G. J. Samuels, and D. M. Geiser 2003. Multilocus phylogenetic structure of Trichoderma harzianum/Hypocrea lixii complex. Mol. Phylogenet. Evol. 27:302-313.
16. Chaverri, P., R. Gazis, and G. J. Samuels 2011. Trichoderma amazonicum, a new endophytic species on Hevea brasiliensis and H. guianensis from the Amazon basin. Mycologia 103:139-151.
17. Clay, K. 1993. The ecology and evolution of endophytes. Agric. Ecosyst. Environ. 44:39-64.
18. Covert, S. F., J. Bolduc, and D. Cullen 1992. Genomic organization of a cellulase gene family in Phanerochaete chrysosporium. Curr. Genet. 22:407-413.
19. Crozier, J., S. E. Thomas, M. C. Aime, H. C. Evans, and K. A. Holmes 2006. Molecular characterization of fungal endophytic morphospecies isolated from stems and pods of Theobroma cacao. Plant Pathol. 55:783-791.
20. Cummings, M. P., and J. C. Huskamp 2005. Grid computing. Educause Rev. 40:116-117.
21. Darwin, C. 1859. On the origin of species by means of natural selection. John Murray, London.
22. Daszak, P., A. A. Cunningham, and A. D. Hyatt 2000. Emerging infectious diseases of wildlife-threats to biodiversity and human health. Science 287:443-449.
23. Davies, T. J., and A. B. Pedersen 2008. Phylogeny and geography predict pathogen community similarity in wild primates and humans. Proc. R. Soc. B-Biol. Sci. 275:1695-1701.
24. De Queiroz, A. 1993. For consensus (sometimes). Syst. Biol. 42:368-372.
25. De Souza, J. T., B. A. Bailey, A. W. V. Pomella, E. F. Erbe, C. A. Murphy, H. Bae, and P. K. Hebbar 2008. Colonization of cacao seedlings by Trichoderma stromaticum, a mycoparasite of the witches' broom pathogen, and its influence on plant growth and resistance. Biol. Control 46:36-45.
26. Dominguez, J. M., V. A. Kelly, O. S. Kinsman, M. S. Marriott, F. G. De Las Heras, and J. J. Martin 1998. Sordarins: a new class of antifungals with selective inhibition of the protein synthesis elongation cycle in yeasts. Antimicrob. Agents Chemother. 42:2274-2278.
27. Druzhinina, I. S., C. P. Kubicek, M. Komoń-Zelazowska, T. B. Mulaw, and J. Bissett 2010. The Trichoderma harzianum demon: complex speciation history resulting in coexistence of hypothetical biological species, recent agamospecies and numerous relict lineages. BMC Evol. Biol. 10:94-107.
28. Elad, Y. 2000. Biological control of foliar pathogens by means of Trichoderma harzianum and potential modes of action. Crop Prot. 19:709-714.
29. Evans, H. C., K. A. Holmes, and S. E. Thomas 2003. Endophytes and mycoparasites associated with an indigenous forest tree, Theobroma gileri, in Ecuador and a preliminary assessment of their potential as biocontrol agents of cocoa diseases. Mycol. Prog. 2:149-160.
30. Fenton, A., and A. B. Pedersen 2005. Community epidemiology in theory and practice: a conceptual framework for classifying disease threats in human and wild populations. Emerg. Infect. Dis. 11:1815-1821.
31. Fitch, W. M. 1971. Toward defining the course of evolution: minimum change for a specified tree topology. Syst. Zool. 20:406-416.
32. Fitzpatrick, D. A. 2012. Horizontal gene transfer in fungi. FEMS Microbiol. Lett. 329:1-8.
33. Floudas, D., M. Binder, R. Riley, K. Barry, R. A. Blanchette, B. Henrissat, A. T. Martínez, R. Otillar, J. W. Spatafora, J. S. Yadav, et al. 2012 The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336:1715-1719.
34. Fordyce, J. A. 2010. Host shifts and evolutionary radiations of butterflies. Proc. R. Soc. B-Biol. Sci. 277:3735-3743.
35. Galtier, N., M. Gouy, and C. Gautier 1996. SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comp. App. Biosci. 12:543-548.
36. Gao, L., and X. Z. Liu 2010. Nutritional requirements of mycelial growth and sporulation of several biocontrol fungi in submerged and on solid culture. Microbiology 79:612-619.
37. Gazis, R., and P. Chaverri 2010. Diversity of fungal endophytes in leaves and stems of rubber trees (Hevea brasiliensis) in Tambopata, Peru. Fungal Ecol. 4:94-102.
38. Giraud, T., P. Gladieux, and S. Gavrilets 2010. Linking the emergence of fungal plant diseases with ecological speciation. Trends Ecol. Evol. 25:387-395.
39. Gond, S. K., V. C. Verma, A. Kumar, V. Kumar, and R. N. Kharwar 2007. Study of endophytic fungal community from different parts of Aegle marmelos Correae (Rutaceae) from Vanasi (India). World J. Microbiol. Biotechnol. 23:1371-1375.
40. Gracia-Garza, J. A., M. Little, W. Brown, T. J. Blom, K. Schneider, W. Allen, and J. Potter 2003. Efficacy of various biological control agents and biorationals against Pythium root rot in poinsettia. HortTechnology 13:149-153.
41. Hallmann, J., and R. A. Sikora 1996. Toxicity of fungal endophyte secondary metabolites to plant parasitic nematodes and soil-borne plant pathogenic fungi. Eur. J. Plant Pathol. 102:155-162.
42. Hanada, R. E., T. D. Souza, A. W. V. Pomella, K. P. Hebbar, J. O. Pereira, A. Ismaiel, and G. J. Samuels 2008. Trichoderma martiale sp. nov., a new endophyte from sapwood of Theobroma cacao with a potential for biological control. Mycol. Res. 112:1335-1343.
43. Harman, G. E., C. R. Howell, A. Viterbo, I. Chet, and M. Lorito 2004. Trichoderma species-opportunistic, avirulent plant symbionts. Nat. Rev. Microbiol. 2:43-56.
44. Harman, G. E., and C. P. Kubicek, eds. 1998. Trichoderma and Gliocladium. Vol. 2. Enzymes, biological control and commercial applications. Taylor & Francis, London.
45. Harris, A. R., and R. D. Lumsden 1997. Interactions of Gliocladium virens with Rhizoctonia solani and Pythium ultimum in non-sterile potting medium. Biocontrol. Sci. Technol. 7:37-47.
46. Hawksworth, D. L. 1991. The fungal dimension of biodiversity: magnitude, significance, and conservation. Mycol. Res. 95:641-655.
47. Holmes, K. A., H.-J. Schroers, S. E. Thomas, H. C. Evans, and G. J. Samuels 2004. Taxonomy and biocontrol potential of a new species of Trichoderma from the Amazon Basin of South America. Mycol. Prog. 3:199-210.
48. Howell, C. R., and R. D. Stipanovic 1991. Antibiotic production by Gliocladium virens and its relation to biocontrol of seedling diseases (abstract). Phytopathology 81:1152.
49. Huelsenbeck, J. P., F. Ronquist, E. S. Nielsen, and J. P. Bollback 2001. Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294:2310-2314.
50. Hyde, K. D., B. Bussaban, B. Paulus, P. W. Crous, S. Lee, E. H. C. McKenzie, W. Photita, and S. Lumyong 2007. Biodiversity of saprobic fungi. Biodivers. Conserv. 16:17-35.
51. Jaklitsch, W. M. 2009. European species of Hypocrea Part I. The green-spored species. Stud. Mycol. 63:1-91.
52. Jaklitsch, W. M., C. P. Kubicek, and I. S. Druzhinia 2008. Three European species of Hypocrea with reddish brown stromata and green ascospores. Mycologia 100:796-815.
53. John, R. P., R. D. Tyagi, D. Prevost, S. K. Brar, S. Pouleur, and R. Y. Surampalli 2010. Mycoparasitic Trichoderma viride as a biocontrol agent against Fusarium oxysporum f. sp. adzuki and Pythium arrhenomanes and as a growth promoter of soybean. Crop Prot. 29:1452-1459.
54. Kantarcioglu, A. S., T. Celkan, A. Yucel, Y. Mikami, S. Kurugoglu, H. Mitani, and K. Altas 2009. Fatal Trichoderma harzianum infection in a leukemic pediatric patient. Med. Mycol. 47:207-215.
55. Katoh, K., K.-I. Kuma, H. Toh, and T. Miyata 2005. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33:511-518.
56. Kepler, R. M., G.-H. Sung, Y. Harada, K. Tanaka, E. Tanaka, T. Hosoya, J. F. Bischoff, and J. W. Spatafora 2012. Host jumping onto close relatives and across kingdoms by Tyrannicordyceps (Clavicipitaceae) gen. nov. and Ustilaginoidea (Clavicipitaceae). Am. J. Bot. 99:552-561.
57. Kindermann, J., Y. El-Ayouti, G. J. Samuels, and C. P. Kubicek 1998. Phylogeny of the genus Trichoderma based on sequence analysis of the internal transcribed spacer region 1 of the rDNA cluster. Fungal Genet. Biol. 24:298-309.
58. Kosakovsky Pond, S. L., B. Murrell, M. Fourment, S. D. W. Frost, W. Delport, and K. Scheffler 2011. A random effects branch-site model for detecting episodic diversifying selection. Mol. Biol. Evol. 24:1-13.
59. Kowalski, T., and R. D. Kehr 1996. Fungal endophytes in living branch bases in several European tree species. Pp. 67-86 in S. C. Redlin and L. M. Carris, eds. Endophytic fungi in grasses and woody plants: systematics, ecology and evolution. APS Press, St Paul, MN.
60. Kraft, N. J. B., W. K. Cornwell, C. O. Webb, and D. D. Ackerly 2007. Trait evolution, community assembly, and the phylogenetic structure of ecological communities. Am. Nat. 170:271-283.
61. Kubicek, C., U. M. Bölzbauer, W. Kovacs, R. L. Mach, K. Kuhls, E. Leickfeldt, T. Börner, and G. J. Samuels 1996. Cellulase production by species of Trichoderma sect. Longibrachiatum and of Hypocrea species with anamorphs referable to Trichoderma sect. Longibrachiatum. Fungal Genet. Biol. 20:105-114.
62. Kubicek, C. P., M. Komon-Zelazowska, and I. S. Druzhinina 2008. Fungal genus Hypocrea/Trichoderma: from barcodes to biodiversity. J. Zhejiang Univ.-Sci. B 9:753-763.
63. Kubicek, C. P., A. Herrera-Estrella, V. Seidl-Seiboth, D. A. Martinez, I. S. Druzhinina, M. Thon, S. Zeilinger, S. Casas-Flores, B. A. Horwitz, P. K. Mukherjee, et al. 2011. Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol. 12:R40.
64. Kullnig-Gradinger, C. M., G. Szakacs, and C. P. Kubicek 2002. Phylogeny and evolution of the genus Trichoderma: a multigene approach. Mycol. Res. 106:757-767.
65. Leschen, R. A. B., and T. R. Buckley 2007. Multistate characters and diet shifts: evolution of erotylidae (Coleoptera). Syst. Biol. 56:97-112.
66. Lewis, P. O., M. T. Holder, and K. E. Holsinger 2005. Polytomies and Bayesian phylogenetic inference. Syst. Biol. 54:241-253.
67. Liu, K., S. Raghavan, S. Nelesen, C. R. Linder, and T. Warnow 2009. Rapid and accurate large-scale coestimation of sequence alignments and phylogenetic trees. Science 324:1561-1564.
68. Liu, Y. J., S. Whelen, and B. D. Hall 1999. Phylogenetic relationships among ascomycetes: evidence from an RNA polymerase II subunit. Mol. Biol. Evol. 16:1799-1808.
69. Lord, J., M. Westoby, and M. Leishman 1995. Seed size and phylogeny in six temperate floras: constraints, niche conservatism, and adaptation. Am. Nat. 146:349-364.
70. Lübeck, M., S. K. Poulsen, P. S. Lübeck, D. F. Jensen, and U. Thrane 2000. Identification of Trichoderma strains from building materials by ITS1 ribotyping, UP-PCR fingerprinting and UP-PCR cross hybridization. FEMS Microbiol. Lett. 185:129-134.
71. Lumsden, R. D., and J. C. Locke 1989. Biological control of damping-off caused by Pythium ultimum and Rhizoctonia solani in soilless mix. Phytopathology 79:361-366.
72. Lutz, M., R. Bauer, D. Begerow, and F. Oberwinkler 2004. Tuberculina-Thanatophytum /Rhizoctonia crocorum-Helicobasidium: a unique mycoparasitic-phytoparasitic life strategy. Mycol. Res. 108:227-238.
73. Maddison, W. P., and D. R. Maddison 2011. Mesquite: a modular system for evolutionary analysis. Version 2.75. Available at http://mesquiteproject.org.
74. Maddison, W. P., P. E. Midford, and S. P. Otto 2007. Estimating a binary character's effect on speciation and extinction. Syst. Biol. 56:701-710.
75. Mahesh, B., M. V. Tejesvi, M. S. Nalini, H. S. Prakash, K. R. Kini, V. Subbiah, and H. S. Shetty 2005. Endophytic mycoflora of inner bark of Azadirachta indica A. Juss. Curr. Sci. 88:218-219.
76. Mäntylä, A., M. Paloheimo, and P. Suominen 1998. Industrial mutants and recombinant strains of Trichoderma reesei. Pp. 291-309 in G. E. Harman and C. P. Kubicek, eds. Trichoderma and Gliocladium. Vol. 23. Enzymes, biological control and commercial applications. Taylor and Francis, London.
77. Mason-Gamer, R. J., and E. A. Kellogg 1996. Testing for phylogenetic conflict among molecular data sets in the tribe Triticeae (Gramineae). Syst. Biol. 45:524-545.
78. Mejia, L. C., E. I. Rojas, Z. Maynard, S. Van Bael, A. E. Arnold, P. K. Hebbar, G. J. Samuels, N. Robbins, and E. A. Herre 2008. Endophytic fungi as biocontrol agents of Theobroma cacao pathogens. Biol. Control 46:4-14.
79. Messier, W., and C. B. Stewart 1997. Episodic adaptive evolution of primate lysozymes. Nature 385:151-154.
80. Mishra, R. C., R. Singh, H. B. Singh, and A. Dikshit 2000. In situ efficacy of Trichoderma harzianum as mycoparasite on Sclerotium rolfsii and Rhizoctonia solani. Trop. Agric. 77:205-206.
81. Müller, M. M., R. Valjakka, A. Suokko, and J. Hantula 2001. Diversity of endophytic fungi of single Norway spruce needles and their role as pioneer decomposers. Mol. Ecol. 10:1801-1810.
82. Myers, D. S., A. L. Bazinet, and M. P. Cummings 2008. Expanding the reach of grid computing: combining globus- and BOINC-based systems. Pp. 71-85 in E.-G. Talbi, and A. Zomaya, eds. Grids for bioinformatics and computational biology. John Wiley & Sons, New York.
83. Nikoh, N., and T. Fukatsu 2000. Interkingdom host jumping underground: phylogenetic analysis of entomoparasitic fungi of the genus Cordyceps. Mol. Biol. Evol. 17:629-638.
84. Overton, B. E., E. L. Stewart, and D. M. Geiser 2006. Taxonomy and phylogenetic relationships of nine species of Hypocrea with anamorphs assignable to Trichoderma section Hypocreanum. Stud. Mycol. 56:39-65.
85. Pagel, M. 1999. The maximum likelihood approach to recosntructing ancestral character states of discrete characters on phylogenies. Syst. Biol. 48:612-622.
86. Parfitt, D., J. Hunt, D. Dockrell, H. J. Rogers, and L. Boddy 2010. Do all trees carry the seeds of their own destruction? PCR reveals numerous wood decay fungi latently present in sapwood of a wide range of angiosperm trees. Fungal Ecol. 3:338-346.
87. Parrent, J. L., K. Peay, A. E. Arnold, L. H. Comas, P. Avis, and A. Tuininga 2010. Moving from pattern to process in fungal symbioses: linking functional traits, community ecology and phylogenetics. New Phytol. 185:882-886.
88. Petrini, O. 1986. Taxonomy of endophytic fungi of aerial plant tissues. Pp. 175-187 in N. J. Fokkema, and J. van den Heuvel, eds. Microbiology of the phyllosphere. Cambridge Univ. Press, Cambridge, MA.
89. Polizzi, V., A. Adams, A. M. Picco, E. Adriaens, J. Lenoir, C. Van Peteghem, S. De Saeger, and N. De Kimpe 2011. Influence of environmental conditions on production of volatiles by Trichoderma atroviride in relation with the sick building syndrome. Build. Environ. 46:945-954.
90. Pond, S. L. K., S. D. W. Frost, and S. V. Muse 2005. HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676-679.
91. Posada, D. 2008. jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25:1253-1256.
92. Powell, J. R., J. L. Parrent, M. M. Hart, J. N. Klironomos, M. C. Rillig, and H. Maherali 2009. Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi. Proc. R. Soc. Lond. B Biol. Sci. 276:4237-4245.
93. Prasad, R. D., R. Rangeshwaran, S. V. Hegde, and C. P. Anuroop 2002. Effect of soil and seed application of Trichoderma harzianum on pigeonpea wilt caused by Fusarium udum under field conditions. Crop Prot. 21:293-297.
94. Promputtha, I., P. Lumyong, V. Dhanasekaran, E. H. C. McKenzie, K. D. Hyde, and R. Jeewon 2007. A phylogenetic evaluation of whether endophytes become saprotrophs at host senescence. Microb. Ecol. 53:579-590.
95. Promputtha, I., K. D. Hyde, E. H. C. McKenzie, J. F. Peberdy, and S. Lumyong 2010. Can leaf degrading enzymes provide evidence that endophytic fungi becoming saprobes? Fungal Divers. 41:89-99.
96. Rabosky, D. L. 2010. Extinction rates should not be estimated from molecular phylogenies. Evolution 64:1816-1824.
97. Rambaut, A., and A. J. Drummond 2009. Tracer v1.5. Available from beast.bio.ed.ac.uk/Tracer
98. Reeb, V., F. Lutzoni, and C. Roux 2004. Contribution of RPB2 to multilocus phylogenetic studies of the euascomycetes (Pezizomycotina, Fungi) with special emphasis on lichen-forming acarosporaceae and evolution of polyspory. Mol. Phylogenet. Evol. 32:1036-1060.
99. Rehner, S. A. 2001. Primers for elongation factor 1-alpha (EF1-alpha). Available from www.aftol.org/pdfs/EF1primer.pdf
100. Ricklefs, R. E. 2007. Estimating diversification rates from phylogenetic information. Trends Ecol. Evol. 22:601-610.
101. Rogerson, C. T. 1970. The Hypocrealean fungi (Ascomycetes, Hypocreales). Mycologia 62:865-910.
102. Rojas, E. I., S. A. Rehner, G. J. Samuels, S. A. Van Bael, E. A. Herre, P. Cannon, R. Chen, J. F. Pang, R. W. Wang, Y. P. Zhang, et al. 2010. Colletotrichum gloeosporioides s.l. associated with Theobroma cacao and other plants in Panama: multilocus phylogenies distinguish host-associated pathogens from asymptomatic endophytes. Mycologia 102:1318-1338.
103. Ronquist, F. 2004. Bayesian inference of character evolution. Trends Ecol. Evol. 19:475-481.
104. Rossman, A. Y., G. J. Samuels, C. T. Rogerson, and R. Lowen 1999. Genera of the Bionectriaceae, Hypocreaceae and Nectriaceae (Hypocreales, Ascomycetes). Stud. Mycol. 42:1-248.
105. Saikkonen, K., S. H. Faeth, M. Helander, and T. J. Sullivan 1998. Fungal endophytes: a continuum of interactions with host plants. Annu. Rev. Ecol. Syst. 29:319-343.
106. Samuels, G. J. 2006. Trichoderma: systematics, the sexual state, and ecology. Phytopathology 96:195-206.
107. Samuels, G. J., and A. Ismaiel 2009. Trichoderma evansii and T. lieckfeldtiae: two new T. hamatum-like species. Mycologia 101:142-156.
108. Samuels, G. J., O. Petrini, K. Kuhls, E. Lieckfeldt, and C. P. Kubicek 1998. The Hypocrea schweinitzii complex and Trichoderma sect. Longibrachiatum. Stud. Mycol. 41:1-54.
109. Samuels, G. J., R. Pardo-Schultheiss, K. P. Hebbar, R. D. Lumsden, C. N. Bastos, J. C. Costa, and J. L. Bezerra 2000. Trichoderma stromaticum sp. nov., a parasite of the cacao witches' broom. Mycol. Res. 104:760-764.
110. Samuels, G. J., S. L. Dodd, W. Gams, L. A. Castlebury, and O. Petrini 2002. Trichoderma species associated with the green mold epidemic of commercially grown Agaricus bisporus. Mycologia 94:146-168.
111. Samuels, G. J., C. Suarez, K. Solis, K. A. Holmes, S. E. Thomas, A. Ismaiel, and H. C. Evans 2006. Trichoderma theobromicola and T. paucisporum: two new species isolated from cacao in South America. Mycol. Res. 110:381-392.
112. Saunders, M., A. E. Glenn, and L. M. Kohn 2010. Exploring the evolutionary ecology of fungal endophytes in agricultural systems: using functional traits to reveal mechanisms in community processes. Evol. Appl. 3:525-537.
113. Schluter, D. 2000. The ecology of adaptive radiation. Oxford Univ. Press, New York, NY.
114. Schluter, D., T. Price, A. O. Mooers, and D. Ludwig 1997. Likelihood of ancestor states in adaptive radiation. Evolution 51:1699-1711.
115. Schulz, B., and C. Boyle 2005. The endophytic continuum. Mycol. Res. 109:661-686.
116. Schuster, A., and M. Schmoll 2010. Biology and biotechnology of Trichoderma. Appl. Microbiol. Biotechnol. 87:787-799.
117. Seidl, V., L. Song, E. Lindquist, S. Gruber, A. Koptchinskiy, S. Zeilinger, M. Schmoll, P. Martínez, J. Sun, I. Grigoriev, et al. 2009. Transcriptomic response of the mycoparasitic fungus Trichoderma atroviride to the presence of a fungal prey. BMC Genom. 10:567.
118. Sharon, E., M. Bar-Eyal, I. Chet, A. Herrera-Estrella, O. Kleifeld, and Y. Spiegel 2001. Biological control of the root-knot nematode Meloidogyne javanica by Trichoderma harzianum. Phytopathology 91:687-693.
119. Sharpton, T. J., J. E. Stajich, S. D. Rounsley, M. J. Gardner, J. R. Wortman, V. S. Jordar, R. Maiti, C. D. Kodira, D. E. Neafsey, Q. D. Zeng, et al. 2009. Comparative genomic analyses of the human fungal pathogens Coccidioides and their relatives. Genome Res. 19:1722-1731.
120. Silva, D. N., P. Talhinhas, L. Cai, L. Manuel, E. K. Gichuru, A. Loureiro, V. Varzea, O. S. Paulo, and D. Batista 2012. Host-jump drives rapid and recent ecological speciation of the emergent fungal pathogen Colletotrichum kahawae. Mol. Ecol. 21:2655-2670.
121. Simon, A., and K. Sivasithamparam 1989. Pathogen suppression: a case study of Gaeumannomyces gramminis var. tritici in soil. Soil Biol. Biochem. 21:331-337.
122. Slot, J. C., and D. S. Hibbett 2007. Horizontal transfer of a nitrate assimilation gene cluster and ecological transitions in fungi: a phylogenetic study. PLoS One 2:e1097.
123. Spatafora, J. W., G. H. Sung, J. M. Sung, N. L. Hywel-Jones, and J. F. White 2007. Phylogenetic evidence for an animal pathogen origin of ergot and the grass endophytes. Mol. Ecol. 16:1701-1711.
124. Stamatakis, A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690.
125. Sung, G.-H., N. L. Hywel-Jones, J.-M. Sung, J. J. Luangsa-ard, B. Shrestha, and J. W. Spatafora 2007. Phylogenetic classification of Cordyceps and the clavicipitaceous fungi. Stud. Mycol. 57:5-59.
126. Taylor, J. W., D. J. Jacobson, S. Kroken, T. Kasuga, D. M. Geiser, D. S. Hibbett, and M. C. Fisher 2000. Phylogenetic species recognition and species concepts in fungi. Fungal Genet. Biol. 31:21-32.
127. Verma, V. C., S. K. Gond, A. Kumar, R. N. Kharwar, and G. A. Strobel 2007. The endophytic mycoflora of bark, leaf, and stem tissues of Azadirachta indica A. Juss (Neem) from Vanasi (India). Microb. Ecol. 54:119-125.
128. Walsh, T. J., A. Groll, J. Hiemenz, R. Fleming, E. Roilides, and E. Anaissie 2004. Infections due to emerging and uncommon medically important fungal pathogens. Clin. Microbiol. Infect.10:48-66.
129. White, T. J., T. Bruns, S. Lee, and J. W. Taylor 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. Pp. 315-322 in M. A. Innis, D. H. Gelfand, J. J. Sninsky, and T. J. White ., eds. PCR protocols: a guide to methods and applications. Academic Press, Inc., New York.
130. Wiegmann, B. M., M. D. Trautwein, I. S. Winkler, N. B. Barr, J. W. Kim, C. Lambkin, M. A. Bertone, B. K. Cassel, K. M. Bayless, A. M. Heimberg, et al. 2011. Episodic radiations in the fly tree of life. Proc. Natl. Acad. Sci. 108:5690-5695.
131. Zwickl, D. J. 2006. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph.D. diss., The University of Texas at Austin, Austin. TX.