Structure and evolution of the Fusarium mating type locus: New insights from the Gibberella fujikuroi complex

Fungal Genetics and Biology

Volumn 48, Issue 7, 2011, Pages 731-740

  Martin, Simon H ^a   Wingfield, Brenda D ^a   Wingfield, Michael J ^a   Steenkamp, Emma T ^a  

^a UNIVERSITY OF PRETORIA   (South Africa)

Author keywords

Fusarium; Heterothallic; Homothallic; Idiomorph; MAT1 2 3

Indexed keywords

ARTICLE; CONTROLLED STUDY; FUNGAL GENE; FUSARIUM; FUSARIUM SACCHARI; GENE EXPRESSION; GENE FLOW; GENE LOCUS; GENE SEQUENCE; GENE STRUCTURE; GENETIC REGULATION; GIBBERELLA FUJIKUROI; HYPOCREALES; MAT GENE; MAT1 1 GENE; MAT1 2 1 GENE; MAT1 2 3 GENE; MAT1 2 GENE; MATING TYPE; MOLECULAR EVOLUTION; NEUROSPORA; NONHUMAN; PRIORITY JOURNAL;

DNA, FUNGAL; EVOLUTION, MOLECULAR; GENE ORDER; GENES, MATING TYPE, FUNGAL; GIBBERELLA; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA;

FUSARIUM; FUSARIUM SACCHARI; GIBBERELLA; GIBBERELLA FUJIKUROI; GIBBERELLA FUJIKUROI COMPLEX; GIBBERELLA ZEAE; HYPOCREALES; NEUROSPORA;

EID: 79956087342     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2011.03.005     Document Type: Article

References (77)

1. Arie T., Christiansen S.K., Yoder O.C., Turgeon B.G. Efficient cloning of ascomycete mating type genes by PCR amplification of the conserved MAT HMG Box. Fungal Genet. Biol. 1997, 21:118-130.
2. Arie T., Yoshida T., Shimizu T., Kawabe M., Yoneyama K., Yamaguchi I. Assessment of Gibberella fujikuroi mating type by PCR. Mycoscience 1999, 40:311-314.
3. Birky C.W., Walsh J.B. Effects of linkage on rates of molecular evolution. Proc. Nat. Acad. Sci. USA 1988, 85:6414-6418.
4. Britz H., Coutinho T.A., Wingfield M.J., Marasas W.F.Â.O., Gordon T.R., Leslie J.F. Fusarium subglutinans f. Sp. pini represents a distinct mating population in the Gibberella fujikuroi species complex. Appl. Environ. Microbiol. 1999, 65:1198-1201.
5. Britz H., Steenkamp E.T., Coutinho T.A., Wingfield B.D., Marasas W.F.O., Wingfield M.J. Two new species of Fusarium section Liseola associated with mango malformation. Mycologia 2002, 94:722-730.
6. Charlesworth B. Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation. Nat. Rev. Genet. 2009, 10:195-205.
7. Chaturvedi V., Fan J., Stein B., Behr M.J., Samsonoff W.A., Wickes B.L., Chaturvedi S. Molecular genetic analyses of mating pheromones reveal intervariety mating or hybridization in Cryptococcus neoformans. Infect. Immun. 2002, 70:5225-5235.
8. Cisar C.R., TeBeest D.O., Spiegel F.W. Sequence similarity of mating type idiomorphs: a method which detects similarity among the Sordariaceae fails to detect similar sequences in other filamentous ascomycetes. Mycologia 1994, 86:540-546.
9. Civetta A., Singh R.S. Sex-related genes, directional sexual selection, and speciation. Mol. Biol. Evol. 1998, 15:901-909.
10. Clark N.L., Aagaard J.E., Swanson W.J. Evolution of reproductive proteins from animals and plants. Reproduction 2006, 131:11-22.
11. Coppin E., Debuchy R., Arnaise S., Picard M. Mating types and sexual development in filamentous ascomycetes. Microbiol. Mol. Biol. Rev. 1997, 61:411-428.
12. Devier B., Aguileta G., Hood M.E., Giraud T. Using phylogenies of pheromone receptor genes in the Microbotryum violaceum species complex to investigate possible speciation by hybridization. Mycologia 2010, 102:689-696.
13. Doohan F.M., Brennan J., Cooke B.M. Influence of climatic factors on Fusarium species pathogenic to cereals. Eur. J. Plant Path. 2003, 109:755-768.
14. Gasser T., Muller H.G., Mammitzsch V. Kernels for nonparametric curve estimation. J. Roy Stat Soc. Ser. B (Meth.) 1985, 47:238-252.
15. Glass N.L., Grotelueschen J., Metzenberg R.L. Neurospora crassa a mating-type region. Proc. Nat. Acad. Sci. USA 1990, 87:4912-4916.
16. Glass N.L., Smith M.L. Structure and function of a mating-type gene from the homothallic species Neurospora africana. Mol. Gen. Genet. 1994, 244:401-409.
17. Glass N.L., Vollmer S.J., Staben C., Grotelueschen J., Metzenberg R.L., Yanofsky C. DNAs of the two mating-type alleles of Neurospora crassa are highly dissimilar. Science 1988, 241:570-573.
18. Goode M.G., Rodrigo A.G. SQUINT: a multiple alignment program and editor. Bioinformatics 2007, 23:1553-1555.
19. Güldener U., Mannhaupt G., Münsterkötter M., Haase D., Oesterheld M., Stümpflen V., Mewes H.-W., Adam G. FGDB: A comprehensive fungal genome resource on the plant pathogen Fusarium graminearum. Nucleic Acids Res. 2006, 34:456-458.
20. Güldener U., Seong K., Boddu J., Cho S., Trail F., Xu J., Adam G., Mewes H., Muehlbauer G., Kistler H. Development of a Fusarium graminearum affymetrix GeneChip for profiling fungal gene expression in vitro and in planta. Fungal Genet. Biol. 2006, 43:316-325.
21. Guindon S., Delsuc F., Dufayard J.F., Gascuel O. Estimating maximum likelihood phylogenies with PhyML. Met. Mol. Cell. Biol. 2009, 537:113-137.
22. Hudson R.R. How can the low levels of DNA sequence variation in regions of the Drosophila genome with low recombination rates be explained?. Proc. Nat. Acad. Sci. USA 1994, 91:6815-6818.
23. Johnson A.D. Molecular mechanisms of cell-type determination in budding yeast. Curr. Opin. Genet. Dev. 1995, 5:552-558.
24. Kanamori M., Kato H., Yasuda N., Koizumi S., Peever T.L., Kamakura T., Teraoka T., Arie T. Novel mating type-dependent transcripts at the mating type locus in Magnaporthe oryzae. Gene 2007, 403:6-17.
25. Kimura M. Estimation of evolutionary distances between homologous nucleotide sequences. Proc. Nat. Acad. Sci. USA 1981, 78:454-458.
26. Kjaerulff S., Dooijes D., Clevers H., Nielsen O. Cell differentiation by interaction of two HMG-box proteins: Mat1-Mc activates M cell-specific genes in S.pombe by recruiting the ubiquitous transcription factor Ste11 to weak binding sites. EMBO J. 1997, 16:4021-4033.
27. Klaasen J.A., Nelson P.E. Identification of a mating population, Gibberella nygamai sp. Nov., within the Fusarium nygamai anamorph. Mycologia 1996, 88:965-969.
28. Klittich C.J.R., Leslie J.F. Identification of a second mating population within the Fusarium moniliforme anamorph of Gibberella fujikuroi. Mycologia 1992, 84:541-547.
29. Klittich C.J.R., Leslie J.F., Nelson P.E., Marasas W.F.O. Fusarium thapsinum (Gibberella thapsina): a new species in section Liseola from sorghum. Mycologia 1997, 89:643-652.
30. Kronstad J.W., Staben C. Mating type in filamentous fungi. Ann. Rev. Genet. 1997, 31:245-276.
31. Kuhlman E.G. Varieties of Gibberella fujikuroi with Anamorphs in Fusarium Section. Mycologia 1982, 74:759-768.
32. Kvas M., Marasas W.F.O., Wingfield B.D., Wingfield M.J., Steenkamp E.T. Diversity and evolution of Fusarium species in the Gibberella fujikuroi complex. Fungal Div. 2009, 34:1-21.
33. Lee J., Lee T., Lee Y.W., Yun S.H., Turgeon B.G. Shifting fungal reproductive mode by manipulation of mating type genes: obligatory heterothallism of Gibberella zeae. Mol. Microbiol. 2003, 50:145-152.
34. Lee S.C., Ni M., Li W., Shertz C., Heitman J. The evolution of sex: a perspective from the fungal kingdom. Microbiol. Mol. Biol. Rev. 2010, 74:298-340.
35. Leslie J., Zeller K., Wohler M., Summerell B. Interfertility of two mating populations in the gibberella fujikuroi species complex. Eur. J. Plant Path. 2004, 110:611-618.
36. Leslie J.F. Mating populations in Gibberella fujikuroi (Fusarium section Liseola). Phytopathology 1991, 81:1058-1060.
37. Leslie J.F. Gibberella fujikuroi: available populations and variable traits. Can. J. Bot. 1995, 73:282-291.
38. Leslie J.F., Summerell B.A., Bullock S., Doe F.J. Description of Gibberella sacchari and Neotypification of its Anamorph Fusarium sacchari. Mycologia 2005, 97:718-724.
39. Librado P., Rozas J. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.
40. Loubradou G., Begueret J., Turcq B. A mutation in an HSP90 gene affects the sexual cycle and suppresses vegetative incompatibility in the fungus Podospora anserina. Genetics 1997, 147:581-588.
41. Markell S.G., Francl L.J. Fusarium head blight inoculum: species prevalence and Gibberella zeae spore type. Plant Dis 2003, 87:814-820.
42. Nix D., Eisen M. GATA: a graphic alignment tool for comparative sequence analysis. BMC Bioinf. 2005, 6:9.
43. O'Donnell K., Cigelnik E., Nirenberg H.I. Molecular systematic and phylogeography of the Gibberella fujikuroi species complex. Mycologia 1998, 90:465-493.
44. O'Donnell K., Nirenberg H.I., Aoki T., Cigelnik E. A multigene phylogeny of the Gibberella fujikuroi species complex: Detection of additional phylogenetically distinct species. Mycoscience 2000, 41:61-78.
45. O'Donnell K., Ward T.J., Geiser D.M., Corby Kistler H., Aoki T. Genealogical concordance between the mating type locus and seven other nuclear genes supports formal recognition of nine phylogenetically distinct species within the Fusarium graminearum clade. Fungal Genet. Biol. 2004, 41:600-623.
46. O'Donnell K., Ward T.J., Aberra D., Kistler H.C., Aoki T., Orwig N., Kimura M., Bjørnstad A., Klemsdal S.S. Multilocus genotyping and molecular phylogenetics resolve a novel head blight pathogen within the Fusarium graminearum species complex from Ethiopia. Fungal Genet. Biol. 2008, 45:1514-1522.
47. Paoletti M., Buck K.W., Brasier C.M. Selective acquisition of novel mating type and vegetative incompatibility genes via interspecies gene transfer in the globally invading eukaryote Ophiostoma novo-ulmi. Mol. Ecol. 2006, 15:249-262.
48. Pöggeler, S., Nowrousian, M., Kück, U., 2006. Fruiting-body development in ascomycetes. In: Kües, U., Fischer, R. (Eds.), Growth, Differentiation and Sexuality. Vol. 1 of The Mycota. Springer Berlin Heidelberg, Berlin/Heidelberg, (Chapter 16). pp. 325-355.
49. Posada D. JModelTest: Phylogenetic model averaging. Mol. Biol. Evol. 2008, 25:1253-1256.
50. Salamov A.A., Solovyev V.V. Ab initio gene finding in Drosophila genomic DNA. Genom. Res. 2000, 10:516-522.
51. Sambrook J., Russell D. Molecular Cloning: A Laboratory Manual 2001, Cold Spring Harbor Laboratory Press, Plainview, NY. third ed.
52. Schmidt H.A., Strimmer K., Vingron M., von Haeseler A. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 2002, 18:502-504.
53. Shimodaira H. An approximately unbiased test of phylogenetic tree selection. Syst. Biol. 2002, 51:492-508.
54. Shimodaira H., Hasegawa M. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 1999, 16:1114.
55. Shimodaira H., Hasegawa M. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 2001, 17:1246-1247.
56. Shiu P.K.T., Glass N.L. Cell and nuclear recognition mechanisms mediated by mating type in filamentous ascomycetes. Curr. Opin. Microbiol. 2000, 3:183-188.
57. Staben C., Yanofsky C. Neurospora crassa a mating-type region. Proc. Nat. Acad. Sci. USA 1990, 87:4917-4921.
58. Stanke M., Steinkamp R., Waack S., Morgenstern B. AUGUSTUS: A web server for gene finding in eukaryotes. Nucleic Acids Res. 2004, 32:W309-W312.
59. Steenkamp E.T., Wingfield B.D., Coutinho T.A., Wingfield M.J., Marasas W.F.O. Differentiation of Fusarium subglutinans f. Sp. pini by histone gene sequence data. Appl. Environ. Microbiol. 1999, 65:3401-3406.
60. Steenkamp E.T., Wingfield B.D., Coutinho T.A., Zeller K.A., Wingfield M.J., Marasas W.F.O., Leslie J.F. PCR-based identification of MAT-1 and MAT-2 in the Gibberella fujikuroi species complex. Appl. Environ. Microbiol. 2000, 66:4378-4382.
61. Steenkamp E.T., Wingfield B.D., Desjardins A.E., Marasas W.F.O., Wingfield M.J. Cryptic speciation in Fusarium subglutinans. Mycologia 2002, 94:1032-1043.
62. Strandberg, R., Nygren, K., Menkis, A., James, T.Y., Wik, L., Stajich, J.E., Johannesson, H. Conflict between reproductive gene trees and species phylogeny among heterothallic and pseudohomothallic members of the filamentous ascomycete genus Neurospora. Fungal Genet. Biol. 47: 869-878.
63. Swanson W.J., Vacquier V.D. The rapid evolution of reproductive proteins. Nat. Rev. Genet. 2002, 3:137-144.
64. Tatusova T.A., Madden T.L. BLAST 2 Sequences, a new tool for comparing protein and nucleotide sequences. FEMS Microbiol. Lett. 1999, 174:247-250.
65. Tavaré, S., 1986. Some Probabilistic and Statistical Problems in the Analysis of DNA Sequences. Amer Mathematical Society, vol. 17, 57-86.
66. Thompson J.D., Higgins D.G., Gibson T.J. CLUSTAL w: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994, 22:4673-4680.
67. Turgeon B.G. Application of mating type gene technology to problems in fungal biology. Ann. Rev. Phytopath. 1998, 36:115-137.
68. Turgeon B.G., Yoder O.C. Proposed nomenclature for mating type genes of filamentous ascomycetes. Fungal Genet. Biol. 2000, 31:1-5.
69. Vicoso B., Charlesworth B. Recombination rates may affect the ratio of X to autosomal non-coding polymorphism in African populations of Drosophila melanogaster. Genetics 2009, 181:1699-1701.
70. Wik L., Karlsson M., Johannesson H. The evolutionary trajectory of the mating-type (mat) genes in Neurospora relates to reproductive behavior of taxa. Bmc Evol. Biol. 2008, 8:109.
71. Wingender E., Dietze P., Karas H., Knüppel R. TRANSFAC: A database on transcription factors and their DNA binding sites. Nucleic Acids Res. 1996, 24:238-241.
72. Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 2007, 24:1586-1591.
73. Yang Z.H., Nielsen R., Goldman N., Pedersen A.M.K. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 2000, 155:431-449.
74. Yli-Mattila T., Gagkaeva T., Ward T.J., Aoki T., Kistler H.C., O'Donnell K. A novel Asian clade within the Fusarium graminearum species complex includes a newly discovered cereal head blight pathogen from the Russian Far East. Mycologia 2009, 101:841-852.
75. Yun S.H., Berbee M.L., Yoder O.C., Turgeon B.G. Evolution of the fungal self-fertile reproductive life style from self-sterile ancestors. Proc. Nat. Acad. Sci. USA 1999, 96:5592-5597.
76. Yun S.-H., Arie T., Kaneko I., Yoder O.C., Turgeon B.G. Molecular organization of mating type loci in heterothallic, homothallic, and asexual Gibberella/Fusarium species. Fungal Genet. Biol. 2000, 31:7-20.
77. Zeller K.A., Summerell B.A., Bullock S., Leslie J.F. Gibberella konza (Fusarium konzum) sp. Nov. from prairie grasses, a new species in the Gibberella fujikuroi species complex. Mycologia 2003, 95:943-954.