Phylogenetic diversity of insecticolous fusaria inferred from multilocus DNA sequence data and their molecular identification via FUSARIUM-ID and Fusarium MLST

Mycologia

Volumn 104, Issue 2, 2012, Pages 427-445

  O'Donnell, Kerry ^a   Humber, Richard A ^b   Geiser, David M ^c   Kang, Seogchan ^c   Park, Bongsoo ^c   Robert, Vincent A R G ^d   Crous, Pedro W ^d   Johnston, Peter R ^e   Aoki, Takayuki ^f   Rooney, Alejandro P ^a   Rehner, Stephen A ^g  

^a NATIONAL CENTER FOR AGRICULTURAL UTILIZATION RESEARCH   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

^d CBS KNAW FUNGAL BIODIVERSITY CENTRE   (Netherlands)

^e LANDCARE RESEARCH   (New Zealand)

^f NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^g AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

Ascomycota; DNA sequence; EF 1 ; GCPSR; RPB1; RPB2; Species limits

Indexed keywords

FUNGAL DNA;

CLADISTICS; DATA SET; DATABASE; ENTOMOPATHOGENIC ORGANISM; FUNGUS; GENE EXPRESSION; GENETIC VARIATION; GENOTYPE; INSECT; MOLECULAR ANALYSIS; PEST SPECIES; PHYLOGENY; RELATEDNESS; SPECIES COMPLEX;

ACARI; ANIMAL; ARTICLE; CHEMISTRY; CLASSIFICATION; FUNGAL GENE; FUSARIUM; GENE LOCUS; GENETIC VARIABILITY; GENETICS; GENOTYPE; INSECT; METHODOLOGY; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; MOLECULAR GENETICS; MULTILOCUS SEQUENCE TYPING; NEMATODE; NUCLEOTIDE SEQUENCE; PHYLOGENY; SEQUENCE ALIGNMENT;

ACARI; ANIMALS; BASE SEQUENCE; DNA, FUNGAL; FUSARIUM; GENES, FUNGAL; GENETIC LOCI; GENETIC VARIATION; GENOTYPE; INSECTS; MOLECULAR SEQUENCE DATA; MULTILOCUS SEQUENCE TYPING; MYCOLOGICAL TYPING TECHNIQUES; NEMATODA; PHYLOGENY; SEQUENCE ALIGNMENT; SOIL MICROBIOLOGY;

ASCOMYCOTA; CENTRAALBUREAU VOOR; FUNGI; FUSARIA; FUSARIUM; HEXAPODA;

EID: 84862313467     PISSN: 00275514     EISSN: 15572536     Source Type: Journal    
DOI: 10.3852/11-179     Document Type: Article

References (64)

1. Bai F-Y, Chen Q-T. 1991. Fusarium species on some insects in China. Acta Mycol Sin 10:120-128.
2. Baker JK, Norris DM. 1968. A complex of fungi mutualistically involved in the nutrition of the ambrosia beetle Xyleborus ferrugineus. J Invert Pathol 11:246-250
3. Balmas V, Migheli Q, Scherm B, Garau P, O'Donnell K, Ceccherelli G, Kang S, Geiser DM. 2010. Multilocus phylogenetics show high levels of endemic fusaria inhabiting Sardinian soils (Tyrrhenian Islands). Mycologia 102:803-812
4. Bills GF, Platas G, Overy DP, Collado J, Fillola A, Jiménez MR, Martin J, del Val AG, Vicente F, Tormo JR, Peláez F, Calati K, Harris G, Parish C, Xu D, Roemer T. 2009. Discovery of the parnafungins, antifungal metabolites that inhibit mRNA polyadenylation, from the Fusarium larvarum complex and other Hypocrealean fungi. Mycologia 101:449-472
5. Bischoff JF, Rehner SA, Humber RA. 2009. A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia 101:512-530
6. Booth C. 1971. The genus Fusarium. Surrey, UK: Commonwealth Mycological Institute. 237 p.
7. Bruns TD, Szaro TM, Gardes M, Cullings KW, Pan JJ, Taylor DL, Horton TR, Kretzer A, Garbelotto M, Li Y. 1998. A sequence database for the identification of ectomycorrhizal basidiomycetes by phylogenetic analysis. Mol Ecol 7:257-272
8. Chang DC, Grant GB, O'Donnell K, Wannemuehler KA, Noble-Wang J, Rao CY, Jacobson LM, Crowell CS, Sneed R, Lewis FMT, Schaffzin JK, Kainer M, Genese CA, Alfonso EC, Jones DB, Srinivasan A, Fridkin SK, Park BJ. 2006. A multistate outbreak of Fusarium keratitis associated with use of a new contact lens solution. JAMA 296:953-963
9. Claydon N, Grove JF. 1984. Fusarium as an insect pathogen. In: Moss MO, Smith JE, eds. The applied mycology of Fusarium. Br Mycol Soc Symp 7. Cambridge: Cambridge Univ. Press. p 117-128.
10. Claydon N, Grove JF., Pople M. 1977. Insecticidal secondary metabolite products from the entomogenous fungus Fusarium solani. J Invertebr Path 30:216-223
11. Dettman JR, Jacobson DJ, Taylor JW. 2003. A multilocus genealogical approach to phylogenetic species recognition in the model eukaryote Neurospora. Evolution 57:2703-2720.
12. Druzhinina LS, Kopchinskiy AG, Komoń M, Bissett J, Szakacs G, Kubicek CP. 2005. An oligonucleotide barcode for species identification in Trichoderma and Hypocrea. Fungal Genet Biol 42:813-828
13. Feldman TS, O'Brien HE, Arnold AE. 2008. Moths that vector a plant pathogen also transport endophytic fungi and mycoparasitic antagonists. Microb Ecol 56: 742-750
14. Felsenstein J, Churchill GA. 1996. A hidden Markov model approach to variation among sites in rate of evolution. Mol Biol Evol 13:93-104.
15. Frøslev TG, Matheny PB, Hibbett DS. 2005. Lower level relationships in the mushroom genus Cortinarius (Basidiomycota, Agaricales): a comparison of RPB1, RPB2 and ITS phylogenies. Mol Phylogenet Evol 37: 602-618
16. Gadd CH, Loos CA. 1947. The ambrosia fungus of Xyleborus fornicatus Eich. Trans Br Mycol Soc 31:13-19
17. Geiser DM, Ivey MLL, Hakiza G, Juba JH, Miller SA. 2005. Gibberella xylarioides (anamorph: Fusarium xylarioides), a causative agent of coffee wilt disease in Africa, is a previously unrecognized member of the G. fujikuroi species complex. Mycologia 97:191-201
18. Geiser DM, Jiménez-Gasco MdD, Kang S, Makalowska I, Veeraraghavan N, Ward TJ, Zhang N, Kuldau GA, O'Donnell K. 2004. FUSARIUM-ID version 1.0: a DNA sequence database for identifying Fusarium. Eur J Plant Pathol 110:473-479
19. Geiser DM, Nirenberg H. 1982. The genus Fusarium-a pictorial atlas. Mitt Biol Bundesanst Land- Forstwirtsch Berlin-Dahlem 209:1-406.
20. Gräfenhan T, Schroers H-J, Nirenberg HI, Seifert KA. 2011. An overview of the taxonomy, phylogeny and typification of nectriaceous fungi in Cosmospora, Acremonium, Fusarium, Stilbella and Volutella. Stud Mycol 68:79-113
21. Gupta S, Krasnoff SB, Underwood NL, Renwick JAA, Roberts DW. 1991. Isolation of beauvericin as an insect toxin from Fusarium semitectum and Fusarium moniliforme var. subglutinans. Mycopathologia 115:185-189
22. Hajek AE, Nelson PE, Humber RA, Perry JL. 1993. Two Fusarium species pathogenic to gypsy moth, Lymantria dispar. Mycologia 85:937-940
23. Hofstetter V, Miadlikowska J, Kauff F, Lutzoni F. 2007. Phylogenetic comparison of protein-coding versus ribosomal RNA-coding sequence data: a case study of the Lecanoromycetes (Ascomycota). Mol Phylogenet Evol 44:412-426
24. James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J, Lumbsch HT, Rauhut A, Reeb V, Arnold AE, Amtoft A, Stajich JE, Hosaka K, Sung G-H, Johnson D, O'Rourke B, Crockett M, Binder M, Curtis JM, Slot JC, Wang Z, Wilson AW, Schüßler A, Longcore JE, O'Donnell K, Mozley-Standridge S, Porter D, Letcher PM, Powell MJ, Taylor JW, White MM, Griffith GW, Davies DR, Humber RA, Morton JB, Sugiyama J, Rossman AY, Rogers JD, Pfister DH, Hewitt D, Hansen K, Hambleton S, Shoemaker RA, Kohlmeyer J, Volkmann-Kohlmeyer B, Spotts RA, Serdani M, Crous PW, Hughes KW, Matsuura K, Langer E, Langer G, Untereiner WA, Lücking R, Büdel B, Geiser DM, Aptroot A, Diederich P, Schmitt I, Schultz M, Yahr R, Hibbett DS, Lutzoni F, McLaughlin DJ, Spatafora JW, Vilgalys R. 2006. Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443:818-822
25. Kok LT, Norris DM, Chu HM. 1970. Sterol metabolism as a basis for a mutualistic symbiosis. Nature 225:661-662
26. Leslie JF, Summerell BA. 2006. The Fusarium laboratory manual. Ames, Iowa: Blackwell Publishing. 388 p.
27. Liu YJ, Hall BD. 2004. Body plan evolution of ascomycetes, as inferred from an RNA polymerase II phylogeny. Proc Natl Acad Sci USA 101:4507-4512
28. Liu YJ, Whelen S, Hall BD. 1999. Phylogenetic relationships among ascomycetes: evidence from an RNA polymerase II subunit. Mol Biol Evol 16:1799-1808.
29. Lutzoni F, Kauff F, Cox CJ, McLaughlin D, Celio G, Dentinger B, Padamsee M, Hibbett D, James TY, Baloch E, Grube M, Reeb V, Hofstetter V, Schoch C, Arnold AE, Miadlikowska J, Spatafora J, Johnson D, Hambleton S, Crockett M, Shoemaker R, Sung G-H, Lücking R, Lumbsch T, O'Donnell K, Binder M, Diederich P, Ertz D, Gueidan C, Hall B, Hansen K, Harris RC, Hosaka K, Lim Y-W, Matheny B, Nishida H, Pfister D, Rogers J, Rossman A, Schmitt I, Sipman H, Stone J, Sugiyama J, Yahr R, Vilgalys R. 2004. Assembling the fungal tree of life, progress, classification and evolution of subcellular traits. Am J Bot 91: 1446-1480
30. Maddison WP, Maddison DR. 2000. MacClade 4.0. Analysis of phylogeny and character evolution. Sunderland, Massachusetts: Sinauer Associates.
31. Marasas WFO, Nelson PE, Toussoun TA, van Wyk PS. 1986. Fusarium polyphialidicum, a new species from South Africa. Mycologia 78:678-682
32. Matheny PB. 2005. Improving phylogenetic inference of mushrooms with RPB1 and RPB2 nucleotide sequences (Inocybe; Agaricales). Mol Phylogenet Evol 35:1-20
33. Migheli Q, Balmas V, Harak H, Sanna S, Scherm B, Aoki T, O'Donnell K. 2010. Molecular phylogenetic diversity of dermatologic and other human pathogenic fusarial isolates from hospitals in northern and central Italy. J Clin Microbiol 48:1076-1084
34. Mueller UG, Rehner SA, Schultz TD. 1998. The evolution of agriculture in ants. Science 281:2034-2038
35. Nelson PE, Toussoun TA, Marasas WFO. 1983. Fusarium species: an illustrated manual for identification. University Park, Pennsylvania: Pennsylvania State University Press. 193 p.
36. Nirenberg HI, O'Donnell K. 1998. New species and combinations within the Gibberella fujikuroi species complex. Mycologia 90:434-458
37. O'Donnell K. 2000. Molecular phylogeny of the Nectria haematococca-Fusarium solani species complex. Mycologia 92:919-938
38. O'Donnell K, Cigelnik E, Nirenberg H. 1998a. Molecular systematics and phylogeography of the Gibberella fujikuroi species complex. Mycologia 90:465-493
39. O'Donnell K, Gueidan C, Sink S, Johnston PR, Crous PW, Glenn A, Riley R, Zitomer NC, Colyer P, Waalwijk C, van der Lee T, Moretti A, Kang S, Kim H-S, Geiser DM, Juba JH, Baayen RP, Cromey MG, Bithell S, Sutton DA, Skovgaard K, Ploetz R, Kistler HC, Elliott M, Davis M, Sarver BAJ. 2009a. A two-locus DNA sequence database for typing plant and human pathogens within the Fusarium oxysporum species complex. Fungal Genet Biol 46:936-948
40. O'Donnell K, Kistler HC, Cigelnik E, Ploetz RC. 1998b. Multiple evolutionary origins of the fungus causing Panama disease of banana: concordant evidence from nuclear and mitochondrial gene genealogies. Proc Natl Acad Sci USA 95:2044-2049
41. O'Donnell K, Kistler HC, Tacke BK, Casper HH. 2000a. Gene genealogies reveal global phylogeographic structure and reproductive isolation among lineages of Fusarium graminearum, the fungus causing wheat scab. Proc Natl Acad Sci USA 97:7905-7910
42. O'Donnell K, Nirenberg HI, Aoki T, Cigelnik E. 2000b. A multigene phylogeny of the Gibberella fujikuroi species complex: Detection of additional phylogenetically distinct species. Mycoscience 41:61-78
43. O'Donnell K, Sarver BAJ, Brandt M, Chang DC, Noble-Wang J, Park BJ, Sutton DA, Benjamin L, Lindsley M, Padhye A, Geiser DM, Ward TJ. 2007. Phylogenetic diversity and microsphere array-based genotyping of human patho-genic Fusaria, including isolates from the multistate contact lens-associated U.S. keratitis outbreaks of 2005 and 2006. J Clin Microbiol 45:2235-2248
44. O'Donnell K, Sutton DA, Fothergill A, McCarthy D, Rinaldi MG, Brandt ME, Zhang N, Geiser DM. 2008. Molecular phylogenetic diversity, multilocus haplotype nomenclature and in vitro antifungal resistance within the Fusarium solani species complex. J Clin Microbiol 46: 2477-2490
45. O'Donnell K, Sutton DA, Rinaldi MG, Gueidan C, Crous PW, Geiser DM. 2009b. Novel multilocus sequence typing scheme reveals high genetic diversity of human pathogenic members of the Fusarium incarnatum-F. equiseti and F. chlamydosporum species complexes within the United States. J Clin Microbiol 47:3851-3861
46. O'Donnell K, Sutton DA, Rinaldi MG, Sarver BAJ, Balajee SA, Schroers HJ, Summerbell RC, Robert VARG, Crous PW, Zhang N, Aoki T, Jung K, Park J, Lee Y-H, Kang S, Park B, Geiser DM. 2010. Internet-accessible DNA sequence database for identifying fusaria from human and animal infections. J Clin Microbiol 48:3708-3718
47. Park B, Park J, Cheong K-C, Choi J, Jung K, Kim D, Lee Y-H, Ward TJ, O'Donnell K, Geiser DM, Kang S. 2011. Cyber infrastructure for Fusarium: three integrated platforms supporting strain identification, phylogenetics, comparative genomics and knowledge sharing. Nucleic Acids Res 39(suppl 1):D640-D646
48. Park J, Park B, Veeraraghavan N, Jung K, Lee Y-H, Blair JE, Geiser DM, Isard S, Mansfield MA, Nikolaeva E, Park SY, Russo J, Kim SH, Greene M, Ivors KL, Balci Y, Peiman M, Erwin DC, Coffey MD, Rossman A, Farr D, Cline E, Grünwald NJ, Luster DG, Schrandt J, Martin F, Ribeiro OK, Makalowska I, Kang S. 2008. Phytophthora database: a forensic database supporting the identification and monitoring of Phytophthora. Plant Dis 92: 966-972
49. Posada D, Crandall K. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14:817-818
50. Reeb V, Lutzoni F, Roux C. 2004. Contribution of RPB2 to multilocus phylogenetic studies of the euascomycetes (Pezizomycotina, Fungi) with special emphasis on the lichen-forming Acarosporaceae and evolution of polyspory. Mol Phylogenet Evol 32:1036-1060
51. Rehner SA, Buckley E. 2005. A Beauveria phylogeny inferred from nuclear ITS and EF1-a sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97:84-98
52. Rehner SA, Minnis AM, Sung G-H, Luangsa-ard JJ, Devotto L, Humber RA. 2011. Phylogenetic systematics of the anamorphic entomopathogen Beauveria. Mycologia. doi:10.3852/10-302.
53. Reinking OA. 1934. Interesting new fusaria. Zentralbl Bakteriol Parasitenkd Infektionskr 89:509-514.
54. Schoch CL, Sung G-H, López-Giráldez F, Townsend JP, Miadlikowska J, Hofstetter V, Robbertse B, Matheny PB, Kauff F, Wang Z, Gueidan C, Andrie RM, Trippe K, Ciufetti LM, Wynns A, Fraker E, Hodkinson BP, Bonito G, Yahr R, Groenewald JZ, Arzanlou M, de Hoog GS, Crous PW, Hewitt D, Pfister DH, Peterson K, Gryzenhout M, Wingfield MJ, Aptroot A, Suh S-O, Blackwell M, Hillis DM, Griffith GW, Castlebury LA, Rossman AY, Lumbsch HT, Lücking R, Büdel B, Rauhut A, Diederich P, Ertz D, Geiser DM, Hosaka K, Inderbitzin P, Kohlmeyer J, Volkmann-Kohlmeyer B, Mostert L, O'Donnell K, Sipman H, Rogers JD, Shoemaker RA, Sugiyama J, Summerbell RC, Untereiner W, Johnston P, Stenroos S, Zuccaro A, Dyer PS, Crittenden PD, Cole MS, Hansen K, Yahr R, Trappe JM, Lutzoni F, Spatafora JW. 2009. The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Syst Biol 58:224-239
55. Schroers H-J, Gräfenhan T, Nirenberg H, Seifert KA. 2011. A revision of Cyanonectria and Geejayessia gen. nov. and related species with fusarium-like anamorphs. Stud Mycol 68:115-138
56. Schroers H-J, O'Donnell K, Lamprecht SC, Kammeyer PL, Johnson S, Sutton DA, Rinaldi MG, Geiser DM, Summerbell RC. 2009. Taxonomy and phylogeny of the Fusarium dimerum species group. Mycologia 101: 44-70
57. StrongmanDB, Strunz GM, Giguère P, Yu C-M, Calhoun L. 1988. Enniatins from Fusarium avenaceum isolated from balsam fir foliage and their toxicity to spruce budworm larvae, Choristoneura fumiferana (Clem.) (Lepidoptera: Tortricidae). J Chem Ecol 14:753-764
58. Swofford DL. 2002. PAUP* 4.0: phylogenetic analysis using parsimony (*and other methods). Sunderland, Massachusetts: Sinauer Associates.
59. Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, Hibbett DS, Fisher MC. 2000. Phylogenetic species recognition and species concepts in fungi. Fungal Genet Biol 31:21-32
60. Taylor JW, Turner E, Townsend JP, Dettman JR, Jacobson D. 2006. Eukaryotic microbes, species recognition and the geographic limits of species: examples from the kingdom Fungi. Philos Trans R Soc Lond B 361: 1947-1963
61. Teetor-Barsch GH, Roberts DW. 1983. Entomogenous Fusarium species. Mycopathologia 84:3-16
62. White TJ, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, eds. PCR protocols: a guide to methods and applications. San Diego: Academic Press. p 315-322.
63. Zhang N, O'Donnell K, Sutton DA, Nalim FA, Summerbell RC, Padhye AA, Geiser DM. 2006. Members of the Fusarium solani species complex that cause infections in both humans and plants are common in the environment. J Clin Microbiol 44:2186-2190
64. Zwickl DJ. 2006. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion [doctoral dissertation]. Austin: Univ. Texas Press. 115 p.