Fungal Diversity

, Volume 58, Issue 1, pp 1–12 | Cite as

Mate-recognition and species boundaries in the ascomycetes

  • Simon H. Martin
  • Emma T. Steenkamp
  • Michael J. Wingfield
  • Brenda D. WingfieldEmail author


Reproductive gene evolution is commonly invoked as a source of reproductive isolation during speciation. This possibility has not been adequately explored in the Ascomycota, the most species-rich fungal phylum. The mechanisms of mate-recognition in this group are relatively simple: a “mating type” locus determines reproductive mode and sexual compatibility, and two pheromone/receptor pairs control sexual attraction. However, ascomycete reproductive genes can experience unique and interesting evolutionary forces, which could lead to rapid divergence. In this review, we examine the mechanisms of sexual interaction in ascomycetes and explore current evidence as to whether these mechanisms allow for species-specificity in mate-recognition. We discuss the evolutionary forces that can drive reproductive gene divergence, how these may apply in the world of ascomycetes, and their possible consequences for speciation.


Ascomycota Speciation Mating type Pheromone Receptor 



This work was supported by The National Research Foundation (NRF), the DST/NRF Centre of Excellence in Tree Health Biotechnology (CTHB), the University of Pretoria and the Tree Protection Cooperative Programme (TPCP).


  1. Alby K, Schaefer D, Bennett RJ (2010) Sexual reproduction in the Candida clade: cryptic cycles, diverse mechanisms, and alternative functions. NIH Public Access 460(7257):890–893Google Scholar
  2. Amselem J, Cuomo C, van Kan JL, Viaud M, Benito EP, Coutinho PM et al (2011) Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS genetics 7(8):e1002230PubMedCrossRefGoogle Scholar
  3. Arnaise S, Zickler D, Glass NL (1993) Heterologous expression of mating-type genes in filamentous fungi. Proc Natl Acad Sci U S A 90(14):6616–6620PubMedCrossRefGoogle Scholar
  4. Beatty NP, Smith ML, Louise Glass N (1994) Molecular characterization of mating-type loci in selected homothallic species of Neurospora, Gelasinospora and Anixiella. Mycol Res 98(11):1309–1316CrossRefGoogle Scholar
  5. Bender A, Sprague F (1989) Pheromones and Pheromone Receptors Are the Primary Determinants of Mating Specificity in the Yeast Saccharomyces cerevisiae. Genetics 121:463–476PubMedGoogle Scholar
  6. Bennett RJ, Johnson AD (2003) Completion of a parasexual cycle in Candida albicans by induced chromosome loss in tetraploid strains. The European Molecular Biology Organization Journal 22(10):2505–2515Google Scholar
  7. Berbee M, Taylor J (1992) 18S Ribosomal RNA gene sequence characters place the human pathogen Sporothrix schenckii in the genus Ophiostoma. Exp Mycol 91:87–91CrossRefGoogle Scholar
  8. Bistis GN (1981) Chemotropic Interactions between Trichogynes and Conidia of Opposite Mating-Type in Neurospora crassa. Mycologia 73(5):959–975CrossRefGoogle Scholar
  9. Bistis GN (1983) Evidence for diffusible, mating-type-specific trichogyne attractants in Neurospora crassa. Exp Mycol 7:292–295CrossRefGoogle Scholar
  10. Bobrowicz P, Pawlak R, Correa A, Bell-Pedersen D, Ebbole DJ (2002) The Neurospora crassa pheromone precursor genes are regulated by the mating type locus and the circadian clock. Mol Microbiol 45:795–804PubMedCrossRefGoogle Scholar
  11. Brake AJ, Brenner C, Najarian R, Laybourn P, Merrywheather J (1985) Structure of genes encoding precursors of the yeast peptide mating pheromone a-factor. In: Gething MJ (ed) Protein transport and secretion. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New YorkGoogle Scholar
  12. Brown JKM, Hovmøller MS (2002) Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297(5581):537–541PubMedCrossRefGoogle Scholar
  13. Burke D, Mendonça-Previato L, Ballou CE (1980) Cell-cell recognition in yeast: purification of Hansenula wingei 21-cell sexual agglutination factor and comparison of the factors from three genera. Proc Natl Acad Sci U S A 77:318–322PubMedCrossRefGoogle Scholar
  14. Caldwell GA, Naider F, Becker JM (1995) Fungal lipopeptide mating pheromones: A model system for the study of protein prenylation. Microbiol Rev 59:406–422PubMedGoogle Scholar
  15. Caplan S, Green R, Rocco J, Kurjan J (1991) Glycosylation and structure of the yeast MF alpha 1 alpha-factor precursor is important for efficient transport through the secretory pathway. Journal Of Bacteriology 173(2):627–635PubMedGoogle Scholar
  16. Chen P, Sapperstein SK, Choi JD, Michaelis S (1997) Biogenesis of the Saccharomyces cerevisiae mating pheromone a-factor. The Journal of Cell Biology 136:251–269PubMedCrossRefGoogle Scholar
  17. Cisar CR, TeBeest DO, Spiegel FW (1994) Sequence similarity of mating type idiomorphs: a method which detects similarity among the Sordariaceae fails to detect similar sequences in other filamentous Ascomycetes. Mycologia 86:540–546CrossRefGoogle Scholar
  18. Clark NL, Aagaard JE, Swanson WJ (2006) Evolution of reproductive proteins from animals and plants. Reproduction 131:11–22PubMedCrossRefGoogle Scholar
  19. Coppin E, de Renty C, Debuchy R (2005) The function of the coding sequences for the putative pheromone precursors in Podospora anserina is restricted to fertilization. Eukaryotic Cell 4:407–420PubMedCrossRefGoogle Scholar
  20. Coppin E, Debuchy R, Arnaise S, Picard M (1997) Mating types and sexual development in filamentous Ascomycetes. Microbiol Mol Biol Rev 61:411–428PubMedGoogle Scholar
  21. Coyne JA, Orr HA (2004) Speciation. Sinauer, Sunderland, MassachusettsGoogle Scholar
  22. Daniels KJ, Srikantha T, Lockhart SR, Pujol C, Soll DR (2006) Opaque cells signal white cells to form biofilms in Candida albicans. EMBO J 25(10):2240–2252PubMedCrossRefGoogle Scholar
  23. Dettman JR, Jacobson DJ, Turner E, Pringle A, Taylor JW (2003) Reproductive isolation and phylogenetic divergence in Neurospora: Comparing methods of species recognition in a model eukaryote. Evolution 57:2721–2741PubMedGoogle Scholar
  24. Duntze W, Betz R, Nientiedt M (1991) Pheromones in yeasts. In: Wessels JMF (ed) The Mycota I: Growth, differentiation and sexuality. Springer Verlag, Heidelberg, pp 381–399Google Scholar
  25. Dyer PS, Paoletti M, Archer DB (2003) Genomics reveals sexual secrets of Aspergillus. Microbiology (Reading, England), 149(Pt 9), 2301–2303Google Scholar
  26. Dyer PS, O’Gorman CM (2011) A fungal sexual revolution: Aspergillus and Penicillium show the way. Curr Opin Microbiol 14(6):649–654PubMedCrossRefGoogle Scholar
  27. Galagan JE, Calvo SE, Cuomo C, Ma L-J, Wortman JR, Batzoglou S, Lee S-I et al (2005) Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438(7071):1105–1115PubMedCrossRefGoogle Scholar
  28. Galindo BE, Vacquier VD, Swanson WJ (2003) Positive selection in the egg receptor for abalone sperm lysin. Proc Natl Acad Sci U S A 100:4639–4643PubMedCrossRefGoogle Scholar
  29. Gavrilets S (2000) Rapid evolution of reproductive barriers driven by sexual conflict. Nature 403:886–889PubMedCrossRefGoogle Scholar
  30. Gavrilets S, Arnqvist G, Friberg U (2001) The evolution of female mate choice by sexual conflict. Proc R Soc London, Ser B 268:531–539CrossRefGoogle Scholar
  31. Gibson AK, Hood ME, Giraud T (2011) Sibling Competition Arena: Selfing and a Competition Arena Can Combine To Constitute a Barrier To Gene Flow in Sympatry. Evolution, 1–14.Google Scholar
  32. Giraud T, Gourbière S (2012) The tempo and modes of evolution of reproductive isolation in fungi. Heredity 109(4):204–214PubMedCrossRefGoogle Scholar
  33. Giraud T, Refrégier G, Le Gac M, de Vienne DM, Hood ME (2008) Speciation in fungi. Fungal Genetics and Biology 45:791–802PubMedCrossRefGoogle Scholar
  34. Glass NL, Metzenberg RL, Raju NB (1990) Homothallic Sordariaceae from nature: The absence of strains containing only thea mating type sequence. Exp Mycol 14(3):274–289CrossRefGoogle Scholar
  35. Glass NL, Smith ML (1994) Structure and function of a mating-type gene from the homothallic species Neurospora africana. Mol Gen Genet 244:401–409PubMedCrossRefGoogle Scholar
  36. Gonçalves-Sá J, Murray A (2011) Asymmetry in sexual pheromones is not required for ascomycete mating. Current biology: CB 21(16):1337–1346PubMedCrossRefGoogle Scholar
  37. Haynes KF, Yeargan KV (1999) Exploitation of intraspecific communication systems: Illicit signalers and receivers. Annals of the Entomological Society of America 92:960–970Google Scholar
  38. Heitman J (2010) Evolution of eukaryotic microbial pathogens via covert sexual reproduction. Cell host microbe 8(1):86–99PubMedCrossRefGoogle Scholar
  39. Herskowitz I (1989) A regulatory hierarchy for cell specialization in yeast. Nature 342:749–757PubMedCrossRefGoogle Scholar
  40. Hisatomi T, Yanagishima N, Sakurai A, Kobayashi H (1988) Interspecific actions of α mating pheromones on the a mating-type cells of three Saccharomyces yeasts. Curr Genet 13:25–27PubMedCrossRefGoogle Scholar
  41. Howard DJ (1993) Reinforcement: Origin, dynamics and fate of an evolutionary hypothesis. In: Harrison RG (ed) Hybrid zones and the evolutionary process. Oxford University Press, EnglandGoogle Scholar
  42. Idnurm A (2011) Sex and speciation: The paradox that non-recombining DNA promotes recombination. Fungal Biology Reviews 25(3):121–127PubMedCrossRefGoogle Scholar
  43. Jones SK, Bennett RJ (2011) Fungal mating pheromones: Choreographing the dating game. Fungal genetics and biology FG B 48(7):668–676PubMedCrossRefGoogle Scholar
  44. Karlsson M, Nygren K, Johannesson H (2008) The evolution of the pheromonal signal system and its potential role for reproductive isolation in heterothallic Neurospora. Mol Biol Evol 25:168–178PubMedCrossRefGoogle Scholar
  45. Kim H-K, Lee T, Yun S-H (2008) A putative pheromone signaling pathway is dispensable for self-fertility in the homothallic ascomycete Gibberella zeae. Fungal Genetics and Biology 45:1188–1196PubMedCrossRefGoogle Scholar
  46. Kim H, Borkovich KA (2004) A pheromone receptor gene, pre-1, is essential for mating type-specific directional growth and fusion of trichogynes and female fertility in Neurospora crassa. Mol Microbiol 52:1781–1798PubMedCrossRefGoogle Scholar
  47. Kim H, Borkovich KA (2006) Pheromones are essential for male fertility and sufficient to direct chemotropic polarized growth of trichogynes during mating in Neurospora crassa. Eukaryotic Cell 5:544–554PubMedCrossRefGoogle Scholar
  48. Kim H, Metzenberg RL, Nelson MA (2002) Multiple functions of mfa-1, a putative pheromone precursor gene of Neurospora crassa. Eukaryotic Cell 1:987–999PubMedCrossRefGoogle Scholar
  49. Kim H, Wright SJ, Park G, Ouyang S, Krystofova S, Borkovich K (2012) Roles for receptors, pheromones, G proteins, and mating type genes during sexual reproduction in Neurospora crassa. Genetics 190(4):1389–1404PubMedCrossRefGoogle Scholar
  50. Kohn LM (2005) Mechanisms of fungal speciation. Annu Rev Phytopathol 43(11):279–308PubMedCrossRefGoogle Scholar
  51. Kronstad JW, Staben C (1997) Mating type in filamentous fungi. Annu Rev Genet 31:245–276PubMedCrossRefGoogle Scholar
  52. Kuhlman EG (1982) Varieties of Gibberella fujikuroi with Anamorphs in Fusarium Section Mycologia 74: 759–768Google Scholar
  53. Kurjan J (1993) The pheromone response pathway in Saccharomyces cerevisiae. Annu Rev Genet 27:147–179PubMedCrossRefGoogle Scholar
  54. Kvas M, Marasas W, Wingfield B (2009) Diversity and evolution of Fusarium species in the Gibberella fujikuroi complex, 1–21.Google Scholar
  55. Le Gac M, Giraud T (2008) Existence of a pattern of reproductive character displacement in Homobasidiomycota but not in Ascomycota. J Evol Biol 21:761–772PubMedCrossRefGoogle Scholar
  56. Lee J, Lee T, Lee YW, Yun SH, Turgeon BG (2003) Shifting fungal reproductive mode by manipulation of mating type genes: obligatory heterothallism of Gibberella zeae. Mol Microbiol 50:145–152PubMedCrossRefGoogle Scholar
  57. Lee J, Leslie JF, Bowden RL (2008) Expression and function of sex pheromones and receptors in the homothallic ascomycete Gibberella zeae. Eukaryotic Cell 7:1211–1221PubMedCrossRefGoogle Scholar
  58. Lee SC, Ni M, Li W, Shertz C, Heitman J (2010) The evolution of sex: A perspective from the fungal kingdom. Microbiol Mol Biol Rev 74:298–340PubMedCrossRefGoogle Scholar
  59. Leslie JF, Klein KK (1996) Female fertility and mating type effects on effective population size and evolution in filamentous fungi. Genetics 144:557–567PubMedGoogle Scholar
  60. Lobuglio KF, Pitt JI, Taylor JW (1993) Phylogenetic analysis of two ribosomal DNA regions indicates multiple independent losses of a sexual talaromyces state among asexual penicillium species in subgenus biverticillium. Mycologia 85(4):592–604CrossRefGoogle Scholar
  61. Louis EJ (2011) Population genomics and speciation in yeasts. Fungal Biology Reviews 25(3):136–142CrossRefGoogle Scholar
  62. Lu S-W, Yun S-H, Lee T, Turgeon BG (2011) Altering sexual reproductive mode by interspecific exchange of MAT loci. Fungal genetics and biology FG B 48(7):714–724PubMedCrossRefGoogle Scholar
  63. Martin SH, Wingfield BD, Wingfield MJ, Steenkamp ET (2011a) Causes and consequences of variability in peptide mating pheromones of ascomycete fungi. Mol Biol Evol 28(7):1987–2003PubMedCrossRefGoogle Scholar
  64. Martin SH, Wingfield BD, Wingfield MJ, Steenkamp ET (2011b) Structure and evolution of the Fusarium mating type locus: new insights from the Gibberella fujikuroi complex. Fungal genetics and biology: FG & B 48(7):731–740CrossRefGoogle Scholar
  65. Mayrhofer S, Weber JM, Pöggeler S (2006) Pheromones and pheromone receptors are required for proper sexual development in the homothallic ascomycete Sordaria macrospora. Genetics 172:1521–1533PubMedCrossRefGoogle Scholar
  66. McCullough J, Herskowitz I (1979) Mating pheromones of Saccharomyces kluyveri: pheromone interactions between Saccharomyces kluyveri and Saccharomyces cerevisiae. J Bacteriol 138:146–154PubMedGoogle Scholar
  67. Menkis A, Whittle CA, Johannesson H (2010) Gene genealogies indicates abundant gene conversions and independent evolutionary histories of the mating-type chromosomes in the evolutionary history of Neurospora tetrasperma. BMC Evol Biol 10:234PubMedCrossRefGoogle Scholar
  68. Metzenberg RL, Glass NL (1990) Mating type and mating strategies in Neurospora. BioEssays news and reviews in molecular cellular and developmental biology 12(2):53–59CrossRefGoogle Scholar
  69. Murphy HA, Kuehne HA, Francis CA, Sniegowski PD (2006) Mate choice assays and mating propensity differences in natural yeast populations. Biol Lett 2:553–556PubMedCrossRefGoogle Scholar
  70. Naider F, Becker JM (2004) The α-factor mating pheromone of Saccharomyces cerevisiae: a model for studying the interaction of peptide hormones and G protein-coupled receptors. Peptides 25:1441–1463PubMedCrossRefGoogle Scholar
  71. Nakayama N, Miyajima A, Arai K (1985) Nucleotide sequences of STE2 and STE3, cell type-specific sterile genes from Saccharomyces cerevisiae. EMBO J 4:2643PubMedGoogle Scholar
  72. Nei M, Rooney AP (2005) Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39(1):121–152PubMedCrossRefGoogle Scholar
  73. Nelson MA, Kang S, Braun EL, Crawford ME, Dolan PL, Leonard PM, Mitchell J, Armijo AM, Bean L, Blueyes E, Cushing T, Errett A, Fleharty M, Gorman M, Judson K, Miller R, Ortega J, Pavlova I, Perea J, Todisco S, Trujillo R, Valentine J, Wells A, Werner-Washburne M, Yazzie S, Natvig DO (1997) Expressed sequences from conidial, mycelial, and sexual stages of Neurospora crassa. Fungal Genetics and Biology 21:348–363PubMedCrossRefGoogle Scholar
  74. Nosil P, Crespi B, Gries R, Gries G (2007) Natural selection and divergence in mate preference during speciation. Genetica 129:309–327PubMedCrossRefGoogle Scholar
  75. Nygren K, Strandberg R, Wallberg A, Nabholz B, Gustafsson T, García D, Cano J et al (2011) A comprehensive phylogeny of Neurospora reveals a link between reproductive mode and molecular evolution in fungi. Molecular Phylogenetics and Evolution 59(3):649–663PubMedCrossRefGoogle Scholar
  76. O’Donnell K, Ward TJ, Geiser DM, Corby Kistler H, Aoki T (2004) 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 genetics and biology 41(6):600–623PubMedCrossRefGoogle Scholar
  77. O’Donnell K, Cigelnik E, Nirenberg HI (1998) Molecular systematics and phylogeography of the Gibberella fujikuroi species complex. Mycologia 90(3):465–493CrossRefGoogle Scholar
  78. Palumbi SR (2008) Speciation and the evolution of gamete recognition genes: pattern and process. Heredity 102:66–76PubMedCrossRefGoogle Scholar
  79. Paoletti M, Buck KW, Brasier CM (2006) Selective acquisition of novel mating type and vegetative incompatibility genes via interspecies gene transfer in the globally invading eukaryote Ophiostoma novo-ulmi. Mol Ecol 15:249–262PubMedCrossRefGoogle Scholar
  80. Paoletti M, Seymour F, Alcocer MJC, Kaur N, Calvo AM, Archer DB, Dyer PS (2007) Mating type and the genetic basis of self-fertility in the model fungus Aspergillus nidulans. Current biology: CB 17(16):1384–1389PubMedCrossRefGoogle Scholar
  81. Paterson HEH (1985) The recognition concept of species. In: Vrba E (ed) Species and speciation. Transvaal Museum, Pretoria, South Africa, pp 21–29Google Scholar
  82. Pöggeler S (2000) Two pheromone precursor genes are transcriptionally expressed in the homothallic ascomycete Sordaria macrospora. Curr Genet 37:403–411PubMedCrossRefGoogle Scholar
  83. Pöggeler S, Kück U (2001) Identification of transcriptionally expressed pheromone receptor genes in filamentous ascomycetes. Gene 280(1–2):9–17PubMedCrossRefGoogle Scholar
  84. Pöggeler S, Nowrousian M, Kück U (2006) Fruiting-body development in Ascomycetes. In: Kües U, Fischer R (eds) Growth, differentiation and sexuality. Springer, Berlin, Heidelberg, pp 325–355CrossRefGoogle Scholar
  85. Pöggeler S, Risch S, Kuck U, Osiewacz HD (1997) Mating-type genes from the homothallic fungus Sordaria macrospora are functionally expressed in a heterothallic ascomycete. Genetics 147:567–580PubMedGoogle Scholar
  86. Pöggeler S, Hoff B, Kück U (2008) Asexual cephalosporin C producer Acremonium chrysogenum carries a functional mating type locus. Appl Environ Microbiol 74(19):6006–6016PubMedCrossRefGoogle Scholar
  87. Sahni N, Yi S, Daniels KJ, Huang G, Srikantha T, Soll DR (2010) Tec1 mediates the pheromone response of the white phenotype of Candida albicans: insights into the evolution of new signal transduction pathways. PLoS biology 8(5)Google Scholar
  88. Saleh D, Milazzo J, Adreit H, Tharreau D, Fournier E (2012) Asexual reproduction induces a rapid and permanent loss of sexual reproduction capacity in the rice fungal pathogen, Magnaporthe oryzae: results of in vitro experimental evolution assays. BMC Evol Biol 12(42)Google Scholar
  89. Schmoll M, Seibel C, Tisch D, Dorrer M, Kubicek CP (2010) A novel class of peptide pheromone precursors in ascomycetous fungi. Mol Microbiol 77(6):1483–1501PubMedCrossRefGoogle Scholar
  90. Schoustra SE, Debets AJM, Slakhorst M, Hoekstra RF (2007) Mitotic Recombination Accelerates Adaptation in the Fungus Aspergillus nidulans. PLoS Genetics 3(4):6CrossRefGoogle Scholar
  91. Seibel C, Tisch D, Kubicek CP, Schmoll M (2012) The role of pheromone receptors for communication and mating in Hypocrea jecorina (Trichoderma reesei). Fungal genetics and biology: FG & B 49(10):814–824CrossRefGoogle Scholar
  92. Seike T, Yamagishi Y, Iio H, Nakamura T, Shimoda C (2012) Remarkably simple sequence requirement of the M-factor pheromone of Schizosaccharomyces pombe. Genetics 191(3):815–825PubMedCrossRefGoogle Scholar
  93. Singh A, Chen EY, Lugovoy JM, Chang CN, Hitzeman RA, Seeburg PH (1983) Saccharomyces cerevisiae contains two discrete genes coding for the α-factor pheromone. Nucleic Acids Res 11:4049–4063PubMedCrossRefGoogle Scholar
  94. Smadja C, Butlin RK (2009) On the scent of speciation: the chemosensory system and its role in premating isolation. Heredity 102(1):77–97PubMedCrossRefGoogle Scholar
  95. Strandberg R, Nygren K, Menkis A, James TY, Wik L, Stajich JE, Johannesson H (2010) Conflict between reproductive gene trees and species phylogeny among heterothallic and pseudohomothallic members of the filamentous ascomycete genus Neurospora. Fungal genetics and biology: FG & B 47(10):869–878CrossRefGoogle Scholar
  96. Swanson WJ, Vacquier VD (2002) The rapid evolution of reproductive proteins. Nat Rev Genet 3:137–144PubMedCrossRefGoogle Scholar
  97. Symonds MRE, Elgar MA (2008) The evolution of pheromone diversity. Trends in Ecology & Evolution 23:220–228CrossRefGoogle Scholar
  98. Taylor J, Jacobson D (1999) The evolution of asexual fungi: Reproduction, speciation and classification. Annual Review of, 197–246.Google Scholar
  99. Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, Hibbett DS, Fisher MC (2000) Phylogenetic species recognition and species concepts in fungi. Fungal Genetics and Biology 31:21–32PubMedCrossRefGoogle Scholar
  100. Templeton AR (1989) The meaning of species and speciation: A genetic perspective. In: Otte D, Endler JA (eds) Speciation and its consequences. Sinauer Associates, Sunderland, Massachusetts, pp 3–27Google Scholar
  101. Turgeon BG, Sharon A, Wirsel S, Yamaguchi K, Christiansen SK, Yoder OC (1995) Structure and function of mating-type genes in Cochliobolus Spp and asexual fungi. Canadian Journal of BotanyRevue Canadienne De Botanique 73:S778–S783CrossRefGoogle Scholar
  102. Turgeon BG (1998) Application of mating type gene technology to problems in fungal biology. Annu Rev Phytopathol 36:115–137PubMedCrossRefGoogle Scholar
  103. Turina M, Prodi A, Alfen NKV (2003) Role of the Mf1-1 pheromone precursor gene of the filamentous ascomycete Cryphonectria parasitica. Fungal Genetics and Biology 40(3):242–251PubMedCrossRefGoogle Scholar
  104. Turner BC, Perkins DD, Fairfield A (2001) Neurospora from natural populations: A global study. Fungal Genetics and Biology 32:67–92PubMedCrossRefGoogle Scholar
  105. Turner E, Jacobson DJ, Taylor JW (2010) Reinforced postmating reproductive isolation barriers in Neurospora, an Ascomycete microfungus. J Evol Biol 23:1642–1656PubMedCrossRefGoogle Scholar
  106. Turner E, Jacobson DJ, Taylor JW (2011) Genetic architecture of a reinforced, postmating, reproductive isolation barrier between neurospora species indicates evolution via natural selection. (J. C. Fay, Ed.). PLoS Genetics 7(8):e1002204PubMedCrossRefGoogle Scholar
  107. Vacquier V, Swanson W, Lee Y-H (1997) Positive darwinian selection on two homologous fertilization proteins: what is the selective pressure driving their divergence? J Mol Evol 44:S15–S22PubMedCrossRefGoogle Scholar
  108. Wik L, Karlsson M, Johannesson H (2008) The evolutionary trajectory of the mating-type (mat) genes in Neurospora relates to reproductive behavior of taxa. BMC Evol Biol 8:109PubMedCrossRefGoogle Scholar
  109. Whittle C, Nygren K, Johannesson H (2011) Consequences of reproductive mode on genome evolution in fungi. Fungal Genetics and Biology: FG & B 48(7):661–667CrossRefGoogle Scholar
  110. Yun SH, Berbee ML, Yoder OC, Turgeon BG (1999) Evolution of the fungal self-fertile reproductive life style from self-sterile ancestors. Proc Natl Acad Sci U S A 96(10):5592–5597PubMedCrossRefGoogle Scholar
  111. Yun SH, Arie T, Kaneko I, Yoder OC, Turgeon BG (2000) Molecular organization of mating type loci in heterothallic, homothallic, and asexual Gibberella/Fusarium species. I: FG & B 31(1):7–20Google Scholar

Copyright information

© Mushroom Research Foundation 2012

Authors and Affiliations

  • Simon H. Martin
    • 1
  • Emma T. Steenkamp
    • 2
  • Michael J. Wingfield
    • 1
  • Brenda D. Wingfield
    • 1
    Email author
  1. 1.Department of GeneticsForestry and Agricultural Biotechnology Institute, University of PretoriaPretoriaSouth Africa
  2. 2.Department of Microbiology and Plant PathologyForestry and Agricultural Biotechnology Institute, University of PretoriaPretoriaSouth Africa

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