1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

Fungal Sex: The Basidiomycota

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • PDF
    24.59 MB
  • HTML
    216.57 Kb
  • XML
    208.25 Kb
  • Authors: Marco A. Coelho1, Guus Bakkeren2, Sheng Sun3, Michael E. Hood4, Tatiana Giraud5
  • Editors: Joseph Heitman6, Neil A. R. Gow7
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: UCIBIO-REQUIMTE, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade NOVA de Lisboa, 2829-516 Caparica, Portugal; 2: Agriculture and Agri-Food Canada, Summerland Research and Development Centre, Summerland, BC, V0H 1Z0, Canada; 3: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; 4: Department of Biology, Amherst College, Amherst, MA 01002; 5: Ecologie Systématique Evolution, Univ. Paris-Sud, CNRS, AgroParisTech, Université Paris-Saclay, 91400, Orsay, France; 6: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; 7: School of Medical Sciences, University of Aberdeen, Fosterhill, Aberdeen, AB25 2ZD, United Kingdom
    • Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0046-2016
  • Received 14 February 2016 Accepted 02 March 2017 Published 09 June 2017
  • Marco A. Coelho [email protected]
image of Fungal Sex: The Basidiomycota
    Preview this microbiology spectrum article:
    Preview Magnify
    Zoom in
    Zoomout

    Fungal Sex: The Basidiomycota, Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/5/3/FUNK-0046-2016-1.gif /docserver/preview/fulltext/microbiolspec/5/3/FUNK-0046-2016-2.gif

  • Abstract:

    Fungi of the Basidiomycota, representing major pathogen lineages and mushroom-forming species, exhibit diverse means to achieve sexual reproduction, with particularly varied mechanisms to determine compatibilities of haploid mating partners. For species that require mating between distinct genotypes, discrimination is usually based on both the reciprocal exchange of diffusible mating pheromones, rather than sexes, and the interactions of homeodomain protein signals after cell fusion. Both compatibility factors must be heterozygous in the product of mating, and genetic linkage relationships of the mating pheromone/receptor and homeodomain genes largely determine the complex patterns of mating-type variation. Independent segregation of the two compatibility factors can create four haploid mating genotypes from meiosis, referred to as tetrapolarity. This condition is thought to be ancestral to the basidiomycetes. Alternatively, cosegregation by linkage of the two mating factors, or in some cases the absence of the pheromone-based discrimination, yields only two mating types from meiosis, referred to as bipolarity. Several species are now known to have large and highly rearranged chromosomal regions linked to mating-type genes. At the population level, polymorphism of the mating-type genes is an exceptional aspect of some basidiomycete fungi, where selection under outcrossing for rare, intercompatible allelic variants is thought to be responsible for numbers of mating types that may reach several thousand. Advances in genome sequencing and assembly are yielding new insights by comparative approaches among and within basidiomycete species, with the promise to resolve the evolutionary origins and dynamics of mating compatibility genetics in this major eukaryotic lineage.

  • Citation: Coelho M, Bakkeren G, Sun S, Hood M, Giraud T. 2017. Fungal Sex: The Basidiomycota. Microbiol Spectrum 5(3):FUNK-0046-2016. doi:10.1128/microbiolspec.FUNK-0046-2016.

References

1. Raper JR. 1966. Genetics of Sexuality in Higher Fungi. Roland Press, New York, NY. [PubMed]
2. Morrow CA, Fraser JA. 2009. Sexual reproduction and dimorphism in the pathogenic basidiomycetes. FEMS Yeast Res 9:161–177 http://dx.doi.org/10.1111/j.1567-1364.2008.00475.x.
3. Hibbett DS, et al. 2007. A higher-level phylogenetic classification of the Fungi. Mycol Res 111:509–547 http://dx.doi.org/10.1016/j.mycres.2007.03.004.
4. Kirk MP, Cannon PF, Minter DW, Stalpers JA. 2008. Dictionary of the Fungi, 10th ed. CABI, Oxon, United Kingdom.
5. Hibbett DS. 2006. A phylogenetic overview of the Agaricomycotina. Mycologia 98:917–925 http://dx.doi.org/10.3852/mycologia.98.6.917.
6. Begerow D, Bauer R, Boekhout T. 2000. Phylogenetic placements of ustilaginomycetous anamorphs as deduced from nuclear LSU rDNA sequences. Mycol Res 104:53–60 http://dx.doi.org/10.1017/S0953756299001161.
7. Begerow D, Schäfer AM, Kellner R, Yurkov A, Kemler M, Oberwinkler F, Bauer R. 2014. Ustilaginomycotina, p 295–329. In McLaughlin DJ, Spatafora JW (ed), Systematics and Evolution: Part A. Springer, Heidelberg, Germany. http://dx.doi.org/10.1007/978-3-642-55318-9_11
8. Aime MC, Toome M, McLaughlin DJ. 2014. Pucciniomycotina, p 271–294. In McLaughlin DJ, Spatafora JW (ed), Systematics and Evolution: Part A. Springer. Heidelberg, Germany. http://dx.doi.org/10.1007/978-3-642-55318-9_10
9. Aime MC, Matheny PB, Henk DA, Frieders EM, Nilsson RH, Piepenbring M, McLaughlin DJ, Szabo LJ, Begerow D, Sampaio JP, Bauer R, Weiss M, Oberwinkler F, Hibbett D. 2006. An overview of the higher level classification of Pucciniomycotina based on combined analyses of nuclear large and small subunit rDNA sequences. Mycologia 98:896–905 http://dx.doi.org/10.3852/mycologia.98.6.896.
10. Bary A, Balfour BI, Garnser HEF. 1887. Comparative Morphology and Biology of the Fungi, Mycetozoa and Bacteria. Clarendon Press, Oxford, United Kingdom. http://dx.doi.org/10.5962/bhl.title.56861
11. Kniep H. 1928. Die Sexualität der Niederen Pflanzen. G. Fischer, Jena, Germany.
12. Buller AHR. 1930. The biological significance of conjugate nuclei in Coprinus lagopus and other hymenomycetes. Nature 126:686–689 http://dx.doi.org/10.1038/126686a0.
13. Whitehouse HLK. 1949. Multiple-allelomorph heterothallism in the fungi. New Phytol 48:212–244 http://dx.doi.org/10.1111/j.1469-8137.1949.tb05120.x.
14. Meinhardt F, Esser K, Lemke PA. 1990. Sex determination and sexual differentiation in filamentous fungi. Crit Rev Plant Sci 9:329–341 http://dx.doi.org/10.1080/07352689009382294.
15. Billiard S, López-Villavicencio M, Devier B, Hood ME, Fairhead C, Giraud T. 2011. Having sex, yes, but with whom? Inferences from fungi on the evolution of anisogamy and mating types. Biol Rev Camb Philos Soc 86:421–442 http://dx.doi.org/10.1111/j.1469-185X.2010.00153.x. [PubMed]
16. James TY. 2015. Why mushrooms have evolved to be so promiscuous: insights from evolutionary and ecological patterns. Fungal Biol Rev 29:167–178 http://dx.doi.org/10.1016/j.fbr.2015.10.002.
17. Nieuwenhuis BPS, Billiard S, Vuilleumier S, Petit E, Hood ME, Giraud T. 2013. Evolution of uni- and bifactorial sexual compatibility systems in fungi. Hered (Edinb) 111:445–455 http://dx.doi.org/10.1038/hdy.2013.67.
18. Casselton LA, Olesnicky NS. 1998. Molecular genetics of mating recognition in basidiomycete fungi. Microbiol Mol Biol Rev 62:55–70. [PubMed]
19. 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 74:298–340 http://dx.doi.org/10.1128/MMBR.00005-10.
20. Kües U. 2015. From two to many: multiple mating types in Basidiomycetes. Fungal Biol Rev 29:126–166 http://dx.doi.org/10.1016/j.fbr.2015.11.001.
21. Kües U, Casselton LA. 1992. Fungal mating type genes: regulators of sexual development. Mycol Res 96:993–1006 http://dx.doi.org/10.1016/S0953-7562(09)80107-X.
22. Kothe E. 1996. Tetrapolar fungal mating types: sexes by the thousands. FEMS Microbiol Rev 18:65–87 http://dx.doi.org/10.1111/j.1574-6976.1996.tb00227.x.
23. Raper J, Flexer A. 1971. Mating systems and evolution of the Basidiomycetes, p 149–167. In Petersen RH (ed), Evolution in the Higher Basidiomycetes. University of Tennessee Press, Knoxville, TN.
24. Whitehouse HLK. 1951. A survey of heterothallism in the Ustilaginales. Trans Br Mycol Soc 34:340–355 http://dx.doi.org/10.1016/S0007-1536(51)80061-5.
25. Buller AHR. 1950. Researches on Fungi: the Sexual Process in the Uredinales. University of Toronto Press, Toronto, Canada.
26. Bölker M, Urban M, Kahmann R. 1992. The a mating type locus of U. maydis specifies cell signaling components. Cell 68:441–450 http://dx.doi.org/10.1016/0092-8674(92)90182-C.
27. Manolaridis I, Kulkarni K, Dodd RB, Ogasawara S, Zhang Z, Bineva G, O’Reilly N, Hanrahan SJ, Thompson AJ, Cronin N, Iwata S, Barford D. 2013. Mechanism of farnesylated CAAX protein processing by the intramembrane protease Rce1. Nature 504:301–305 http://dx.doi.org/10.1038/nature12754.
28. Raudaskoski M, Kothe E. 2010. Basidiomycete mating type genes and pheromone signaling. Eukaryot Cell 9:847–859 http://dx.doi.org/10.1128/EC.00319-09.
29. Xue C, Hsueh YP, Heitman J. 2008. Magnificent seven: roles of G protein-coupled receptors in extracellular sensing in fungi. FEMS Microbiol Rev 32:1010–1032 http://dx.doi.org/10.1111/j.1574-6976.2008.00131.x.
30. Kamiya Y, Sakurai A, Tamura S, Takahashi N, Abe K, Tsuchiya E, Fukui S, Kitada C, Fujino M. 1978. Structure of rhodotorucine A, a novel lipopeptide, inducing mating tube formation in Rhodosporidium toruloides. Biochem Biophys Res Commun 83:1077–1083 http://dx.doi.org/10.1016/0006-291X(78)91505-X.
31. Kamiya Y, Sakurai A, Tamura S, Takahashi N, Abe K, Tsuchiya E, Fukui S. 1978. Isolation of rhodotorucine A, a peptidyl factor inducing the mating tube formation in Rhodosporidium toruloides. Agric Biol Chem 42:1239–1243.
32. Miyakawa T, Tabata M, Tsuchiya E, Fukui S. 1985. Biosynthesis and secretion of tremerogen A-10, a polyisoprenyl peptide mating pheromone of Tremella mesenterica. Eur J Biochem 147:489–493 http://dx.doi.org/10.1111/j.0014-2956.1985.00489.x.
33. Spellig T, Bölker M, Lottspeich F, Frank RW, Kahmann R. 1994. Pheromones trigger filamentous growth in Ustilago maydis. EMBO J 13:1620–1627. [PubMed]
34. Moore TD, Edman JC. 1993. The α-mating type locus of Cryptococcus neoformans contains a peptide pheromone gene. Mol Cell Biol 13:1962–1970 http://dx.doi.org/10.1128/MCB.13.3.1962.
35. Wendland J, Vaillancourt LJ, Hegner J, Lengeler KB, Laddison KJ, Specht CA, Raper CA, Kothe E. 1995. The mating-type locus B α 1 of Schizophyllum commune contains a pheromone receptor gene and putative pheromone genes. EMBO J 14:5271–5278. [PubMed]
36. O’Shea SF, Chaure PT, Halsall JR, Olesnicky NS, Leibbrandt A, Connerton IF, Casselton LA. 1998. A large pheromone and receptor gene complex determines multiple B mating type specificities in Coprinus cinereus. Genetics 148:1081–1090. [PubMed]
37. Caldwell GA, Naider F, Becker JM. 1995. Fungal lipopeptide mating pheromones: a model system for the study of protein prenylation. Microbiol Rev 59:406–422. [PubMed]
38. Michaelis S, Barrowman J. 2012. Biogenesis of the Saccharomyces cerevisiae pheromone a-factor, from yeast mating to human disease. Microbiol Mol Biol Rev 76:626–651 http://dx.doi.org/10.1128/MMBR.00010-12.
39. Coelho MA, Rosa A, Rodrigues N, Fonseca A, Gonçalves P. 2008. Identification of mating type genes in the bipolar basidiomycetous yeast Rhodosporidium toruloides: first insight into the MAT locus structure of the Sporidiobolales. Eukaryot Cell 7:1053–1061 http://dx.doi.org/10.1128/EC.00025-08.
40. Duplessis S, Cuomo CA, Lin YC, Aerts A, Tisserant E, Veneault-Fourrey C, Joly DL, Hacquard S, Amselem J, Cantarel BL, Chiu R, Coutinho PM, Feau N, Field M, Frey P, Gelhaye E, Goldberg J, Grabherr MG, Kodira CD, Kohler A, Kües U, Lindquist EA, Lucas SM, Mago R, Mauceli E, Morin E, Murat C, Pangilinan JL, Park R, Pearson M, Quesneville H, Rouhier N, Sakthikumar S, Salamov AA, Schmutz J, Selles B, Shapiro H, Tanguay P, Tuskan GA, Henrissat B, Van de Peer Y, Rouzé P, Ellis JG, Dodds PN, Schein JE, Zhong S, Hamelin RC, Grigoriev IV, Szabo LJ, Martin F. 2011. Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc Natl Acad Sci USA 108:9166–9171 http://dx.doi.org/10.1073/pnas.1019315108.
41. Kües U, James TY, Heitman J. 2011. Mating type in basidiomycetes: unipolar, bipolar, and tetrapolar patterns of sexuality, p 97–160. In Pöggeler S, Wöstemeyer J (ed), Evolution of Fungi and Fungal-Like Organisms, vol 6. Springer, Heidelberg, Germany. http://dx.doi.org/10.1007/978-3-642-19974-5_6
42. Maia TM, Lopes ST, Almeida JM, Rosa LH, Sampaio JP, Gonçalves P, Coelho MA. 2015. Evolution of mating systems in basidiomycetes and the genetic architecture underlying mating-type determination in the yeast Leucosporidium scottii. Genetics 201:75–89 http://dx.doi.org/10.1534/genetics.115.177717.
43. Xu L, Petit E, Hood ME. 2016. Variation in mate-recognition pheromones of the fungal genus Microbotryum. Hered (Edinb) 116:44–51 http://dx.doi.org/10.1038/hdy.2015.68.
44. Akada R, Minomi K, Kai J, Yamashita I, Miyakawa T, Fukui S. 1989. Multiple genes coding for precursors of rhodotorucine A, a farnesyl peptide mating pheromone of the basidiomycetous yeast Rhodosporidium toruloides. Mol Cell Biol 9:3491–3498 http://dx.doi.org/10.1128/MCB.9.8.3491.
45. Coelho MA, Sampaio JP, Gonçalves P. 2010. A deviation from the bipolar-tetrapolar mating paradigm in an early diverged basidiomycete. PLoS Genet 6:e1001052 http://dx.doi.org/10.1371/journal.pgen.1001052.
46. Abe K, Kusaka I, Fukui S. 1975. Morphological change in the early stages of the mating process of Rhodosporidium toruloides. J Bacteriol 122:710–718. [PubMed]
47. Day AW. 1976. Communication through fimbriae during conjugation in a fungus. Nature 262:583–584 http://dx.doi.org/10.1038/262583a0.
48. Feldbrügge M, Kämper J, Steinberg G, Kahmann R. 2004. Regulation of mating and pathogenic development in Ustilago maydis. Curr Opin Microbiol 7:666–672 http://dx.doi.org/10.1016/j.mib.2004.10.006. [PubMed]
49. Zarnack K, Eichhorn H, Kahmann R, Feldbrügge M. 2008. Pheromone-regulated target genes respond differentially to MAPK phosphorylation of transcription factor Prf1. Mol Microbiol 69:1041–1053.
50. Nadal M, García-Pedrajas MD, Gold SE. 2008. Dimorphism in fungal plant pathogens. FEMS Microbiol Lett 284:127–134 http://dx.doi.org/10.1111/j.1574-6968.2008.01173.x.
51. Hartmann HA, Kahmann R, Bölker M. 1996. The pheromone response factor coordinates filamentous growth and pathogenicity in Ustilago maydis. EMBO J 15:1632–1641. [PubMed]
52. Urban M, Kahmann R, Bölker M. 1996. Identification of the pheromone response element in Ustilago maydis. Mol Gen Genet 251:31–37. [PubMed]
53. Banham AH, Asante-Owusu RN, Göttgens B, Thompson S, Kingsnorth CS, Mellor E, Casselton LA. 1995. An N-terminal dimerization domain permits homeodomain proteins to choose compatible partners and initiate sexual development in the mushroom Coprinus cinereus. Plant Cell 7:773–783 http://dx.doi.org/10.1105/tpc.7.6.773.
54. Kämper J, Reichmann M, Romeis T, Bölker M, Kahmann R. 1995. Multiallelic recognition: nonself-dependent dimerization of the bE and bW homeodomain proteins in Ustilago maydis. Cell 81:73–83 http://dx.doi.org/10.1016/0092-8674(95)90372-0.
55. Kahmann R, Bölker M. 1996. Self/nonself recognition in fungi: old mysteries and simple solutions. Cell 85:145–148 http://dx.doi.org/10.1016/S0092-8674(00)81091-0.
56. Badrane H, May G. 1999. The divergence-homogenization duality in the evolution of the b1 mating type gene of Coprinus cinereus. Mol Biol Evol 16:975–986 http://dx.doi.org/10.1093/oxfordjournals.molbev.a026187.
57. Yee AR, Kronstad JW. 1993. Construction of chimeric alleles with altered specificity at the b incompatibility locus of Ustilago maydis. Proc Natl Acad Sci USA 90:664–668 http://dx.doi.org/10.1073/pnas.90.2.664.
58. Yee AR, Kronstad JW. 1998. Dual sets of chimeric alleles identify specificity sequences for the bE and bW mating and pathogenicity genes of Ustilago maydis. Mol Cell Biol 18:221–232 http://dx.doi.org/10.1128/MCB.18.1.221.
59. Schulz B, Banuett F, Dahl M, Schlesinger R, Schäfer W, Martin T, Herskowitz I, Kahmann R. 1990. The b alleles of U. maydis, whose combinations program pathogenic development, code for polypeptides containing a homeodomain-related motif. Cell 60:295–306 http://dx.doi.org/10.1016/0092-8674(90)90744-Y.
60. Wahl R, Zahiri A, Kämper J. 2010. The Ustilago maydis b mating type locus controls hyphal proliferation and expression of secreted virulence factors in planta. Mol Microbiol 75:208–220 http://dx.doi.org/10.1111/j.1365-2958.2009.06984.x.
61. Giraud T, Yockteng R, López-Villavicencio M, Refrégier G, Hood ME. 2008. Mating system of the anther smut fungus Microbotryum violaceum: selfing under heterothallism. Eukaryot Cell 7:765–775 http://dx.doi.org/10.1128/EC.00440-07.
62. Kahmann R, Kämper J. 2004. Ustilago maydis: how its biology relates to pathogenic development. New Phytol 164:31–42 http://dx.doi.org/10.1111/j.1469-8137.2004.01156.x.
63. Fedler M, Luh KS, Stelter K, Nieto-Jacobo F, Basse CW. 2009. The a2 mating-type locus genes lga2 and rga2 direct uniparental mitochondrial DNA (mtDNA) inheritance and constrain mtDNA recombination during sexual development of Ustilago maydis. Genetics 181:847–860 http://dx.doi.org/10.1534/genetics.108.096859.
64. Schirawski J, Heinze B, Wagenknecht M, Kahmann R. 2005. Mating type loci of Sporisorium reilianum: novel pattern with three a and multiple b specificities. Eukaryot Cell 4:1317–1327 http://dx.doi.org/10.1128/EC.4.8.1317-1327.2005.
65. Kellner R, Vollmeister E, Feldbrügge M, Begerow D. 2011. Interspecific sex in grass smuts and the genetic diversity of their pheromone-receptor system. PLoS Genet 7:e1002436 http://dx.doi.org/10.1371/journal.pgen.1002436. (Erratum, doi:10.1371/annotation/5febc52b-339c-4f47-82c0-03d417516446.)
66. Riess K, Schön ME, Lutz M, Butin H, Oberwinkler F, Garnica S. 2016. On the evolutionary history of Uleiella chilensis, a smut fungus parasite of Araucaria araucana in South America: uleiellales ord. nov. in Ustilaginomycetes. PLoS One 11:e0147107 http://dx.doi.org/10.1371/journal.pone.0147107.
67. Gillissen B, Bergemann J, Sandmann C, Schroeer B, Bölker M, Kahmann R. 1992. A two-component regulatory system for self/non-self recognition in Ustilago maydis. Cell 68:647–657 http://dx.doi.org/10.1016/0092-8674(92)90141-X.
68. Puhalla JE. 1970. Genetic studies of the b incompatability locus of Ustilago maydis. Genet Res 16:229–232 http://dx.doi.org/10.1017/S0016672300002457.
69. Wong GJ, Wells K. 1985. Modified bifactorial incompatibility in Tremella mesenterica. Trans Br Mycol Soc 84:95–109 http://dx.doi.org/10.1016/S0007-1536(85)80223-0.
70. Metin B, Findley K, Heitman J. 2010. The mating type locus ( MAT) and sexual reproduction of Cryptococcus heveanensis: insights into the evolution of sex and sex-determining chromosomal regions in fungi. PLoS Genet 6:e1000961 http://dx.doi.org/10.1371/journal.pgen.1000961.
71. Findley K, Sun S, Fraser JA, Hsueh Y-P, Averette AF, Li W, Dietrich FS, Heitman J. 2012. Discovery of a modified tetrapolar sexual cycle in Cryptococcus amylolentus and the evolution of MAT in the Cryptococcus species complex. PLoS Genet 8:e1002528 http://dx.doi.org/10.1371/journal.pgen.1002528.
72. Guerreiro MA, Springer DJ, Rodrigues JA, Rusche LN, Findley K, Heitman J, Fonseca A. 2013. Molecular and genetic evidence for a tetrapolar mating system in the basidiomycetous yeast Kwoniella mangrovensis and two novel sibling species. Eukaryot Cell 12:746–760 http://dx.doi.org/10.1128/EC.00065-13.
73. Hood ME, Scott M, Hwang M. 2015. Breaking linkage between mating compatibility factors: tetrapolarity in Microbotryum. Evolution 69:2561–2572 http://dx.doi.org/10.1111/evo.12765.
74. Yurkov A, Guerreiro MA, Sharma L, Carvalho C, Fonseca Á. 2015. Multigene assessment of the species boundaries and sexual status of the basidiomycetous yeasts Cryptococcus flavescens and C. terrestris (Tremellales). PLoS One 10:e0120400 http://dx.doi.org/10.1371/journal.pone.0120400. (Erratum, 10.1371/journal.pone.0126996.)
75. Koh CM, Liu Y, Moehninsi, Du M, Ji L. 2014. Molecular characterization of KU70 and KU80 homologues and exploitation of a KU70-deficient mutant for improving gene deletion frequency in Rhodosporidium toruloides. BMC Microbiol 14:50 http://dx.doi.org/10.1186/1471-2180-14-50.
76. Nichols CB, Fraser JA, Heitman J. 2004. PAK kinases Ste20 and Pak1 govern cell polarity at different stages of mating in Cryptococcus neoformans. Mol Biol Cell 15:4476–4489 http://dx.doi.org/10.1091/mbc.E04-05-0370.
77. Smith DG, Garcia-Pedrajas MD, Hong W, Yu Z, Gold SE, Perlin MH. 2004. An ste20 homologue in Ustilago maydis plays a role in mating and pathogenicity. Eukaryot Cell 3:180–189 http://dx.doi.org/10.1128/EC.3.1.180-189.2004.
78. Coelho MA, Gonçalves P, Sampaio JP. 2011. Evidence for maintenance of sex determinants but not of sexual stages in red yeasts, a group of early diverged basidiomycetes. BMC Evol Biol 11:249 http://dx.doi.org/10.1186/1471-2148-11-249. [PubMed]
79. Billiard S, López-Villavicencio M, Hood ME, Giraud T. 2012. Sex, outcrossing and mating types: unsolved questions in fungi and beyond. J Evol Biol 25:1020–1038 http://dx.doi.org/10.1111/j.1420-9101.2012.02495.x.
80. Riquelme M, Challen MP, Casselton LA, Brown AJ. 2005. The origin of multiple B mating specificities in Coprinus cinereus. Genetics 170:1105–1119 http://dx.doi.org/10.1534/genetics.105.040774.
81. Day PR. 1960. The structure of the A mating type locus in Coprinus lagopus. Genetics 45:641–650. [PubMed]
82. Lukens L, Yicun H, May G. 1996. Correlation of genetic and physical maps at the A mating-type locus of Coprinus cinereus. Genetics 144:1471–1477. [PubMed]
83. Kües U, Casselton LA. 1993. The origin of multiple mating types in mushrooms. J Cell Sci 104:227–230.
84. Kües U, Richardson WV, Tymon AM, Mutasa ES, Göttgens B, Gaubatz S, Gregoriades A, Casselton LA. 1992. The combination of dissimilar alleles of the A α and A β gene complexes, whose proteins contain homeo domain motifs, determines sexual development in the mushroom Coprinus cinereus. Genes Dev 6:568–577 http://dx.doi.org/10.1101/gad.6.4.568.
85. Pardo EH, O’Shea SF, Casselton LA. 1996. Multiple versions of the A mating type locus of Coprinus cinereus are generated by three paralogous pairs of multiallelic homeobox genes. Genetics 144:87–94. [PubMed]
86. Stajich JE, Wilke SK, Ahrén D, Au CH, Birren BW, Borodovsky M, Burns C, Canbäck B, Casselton LA, Cheng CK, Deng J, Dietrich FS, Fargo DC, Farman ML, Gathman AC, Goldberg J, Guigó R, Hoegger PJ, Hooker JB, Huggins A, James TY, Kamada T, Kilaru S, Kodira C, Kües U, Kupfer D, Kwan HS, Lomsadze A, Li W, Lilly WW, Ma LJ, Mackey AJ, Manning G, Martin F, Muraguchi H, Natvig DO, Palmerini H, Ramesh MA, Rehmeyer CJ, Roe BA, Shenoy N, Stanke M, Ter-Hovhannisyan V, Tunlid A, Velagapudi R, Vision TJ, Zeng Q, Zolan ME, Pukkila PJ. 2010. Insights into evolution of multicellular fungi from the assembled chromosomes of the mushroom Coprinopsis cinerea ( Coprinus cinereus). Proc Natl Acad Sci USA 107:11889–11894 http://dx.doi.org/10.1073/pnas.1003391107.
87. Fowler TJ, Mitton MF, Rees EI, Raper CA. 2004. Crossing the boundary between the Bα and Bβ mating-type loci in Schizophyllum commune. Fungal Genet Biol 41:89–101 http://dx.doi.org/10.1016/j.fgb.2003.08.009.
88. Kües U, Nelson DR, Liu C, Yu G-J, Zhang J, Li J, Wang X-C, Sun H. 2015. Genome analysis of medicinal Ganoderma spp. with plant-pathogenic and saprotrophic life-styles. Phytochemistry 114:18–37 http://dx.doi.org/10.1016/j.phytochem.2014.11.019.
89. Kamada T. 2002. Molecular genetics of sexual development in the mushroom Coprinus cinereus. BioEssays 24:449–459 http://dx.doi.org/10.1002/bies.10083.
90. Kües U. 2000. Life history and developmental processes in the basidiomycete Coprinus cinereus. Microbiol Mol Biol Rev 64:316–353 http://dx.doi.org/10.1128/MMBR.64.2.316-353.2000.
91. Casselton LA, Kües U. 2007. The origin of multiple mating types in the model mushrooms Coprinopsis cinerea and Schizophyllum commune, p 283–300. In Heitman J, Kronstad JW, Taylor JW, Casselton LA (ed), Sex in Fungi: Molecular Determination and Evolutionary Implications. ASM Press, Washington, DC. http://dx.doi.org/10.1128/9781555815837.ch17
92. Tymon AM, Kües U, Richardson WV, Casselton LA. 1992. A fungal mating type protein that regulates sexual and asexual development contains a POU-related domain. EMBO J 11:1805–1813. [PubMed]
93. Swiezynski KM, Day PR. 1960. Heterokaryon formation in Coprinus lagopus. Genet Res 1:114–128 http://dx.doi.org/10.1017/S0016672300000112.
94. James TY, Lee M, van Diepen LT. 2011. A single mating-type locus composed of homeodomain genes promotes nuclear migration and heterokaryosis in the white-rot fungus Phanerochaete chrysosporium. Eukaryot Cell 10:249–261 http://dx.doi.org/10.1128/EC.00212-10.
95. van Peer AF, Park S-Y, Shin P-G, Jang K-Y, Yoo Y-B, Park Y-J, Lee B-M, Sung G-H, James TY, Kong W-S. 2011. Comparative genomics of the mating-type loci of the mushroom Flammulina velutipes reveals widespread synteny and recent inversions. PLoS One 6:e22249 http://dx.doi.org/10.1371/journal.pone.0022249.
96. Freihorst D, Fowler TJ, Bartholomew K, Raudaskoski M, Horton JS, Kothe E. 2016. The mating-type genes of the basidiomycetes, p 329–349. In Wendland J (ed), Growth, Differentiation and Sexuality, 3rd ed, vol 13. Springer International Publishing, Cham, Switzerland. http://dx.doi.org/10.1007/978-3-319-25844-7_13
97. Martinez D, Larrondo LF, Putnam N, Gelpke MD, Huang K, Chapman J, Helfenbein KG, Ramaiya P, Detter JC, Larimer F, Coutinho PM, Henrissat B, Berka R, Cullen D, Rokhsar D. 2004. Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat Biotechnol 22:695–700 http://dx.doi.org/10.1038/nbt967.
98. Niculita-Hirzel H, Labbé J, Kohler A, le Tacon F, Martin F, Sanders IR, Kües U. 2008. Gene organization of the mating type regions in the ectomycorrhizal fungus Laccaria bicolor reveals distinct evolution between the two mating type loci. New Phytol 180:329–342 http://dx.doi.org/10.1111/j.1469-8137.2008.02525.x.
99. Martinez D, et al. 2009. Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci USA 106:1954–1959 http://dx.doi.org/10.1073/pnas.0809575106.
100. James TY, Sun S, Li W, Heitman J, Kuo H-C, Lee Y-H, Asiegbu FO, Olson A. 2013. Polyporales genomes reveal the genetic architecture underlying tetrapolar and bipolar mating systems. Mycologia 105:1374–1390 http://dx.doi.org/10.3852/13-162.
101. Hsueh YP, Xue C, Heitman J. 2009. A constitutively active GPCR governs morphogenic transitions in Cryptococcus neoformans. EMBO J 28:1220–1233 http://dx.doi.org/10.1038/emboj.2009.68.
102. James TY. 2007. Analysis of mating-type locus organization and synteny in mushroom fungi: beyond model species, p 317–331. In Heitman J, Kronstad JW, Taylor JW, Casselton LA (ed), Sex in Fungi: Molecular Determination and Evolutionary Implications. ASM Press, Washington, DC. http://dx.doi.org/10.1128/9781555815837.ch19
103. Ohm RA, de Jong JF, Lugones LG, Aerts A, Kothe E, Stajich JE, de Vries RP, Record E, Levasseur A, Baker SE, Bartholomew KA, Coutinho PM, Erdmann S, Fowler TJ, Gathman AC, Lombard V, Henrissat B, Knabe N, Kües U, Lilly WW, Lindquist E, Lucas S, Magnuson JK, Piumi F, Raudaskoski M, Salamov A, Schmutz J, Schwarze FW, vanKuyk PA, Horton JS, Grigoriev IV, Wösten HA. 2010. Genome sequence of the model mushroom Schizophyllum commune. Nat Biotechnol 28:957–963 http://dx.doi.org/10.1038/nbt.1643.
104. Raper JR, Baxter MG, Ellingboe AH. 1960. The genetic structure of the incompatibility factors of Schizophyllum commune: the A-factor. Proc Natl Acad Sci USA 46:833–842 http://dx.doi.org/10.1073/pnas.46.6.833.
105. Díaz-Valderrama JR, Aime MC. 2016. The cacao pathogen Moniliophthora roreri (Marasmiaceae) possesses biallelic A and B mating loci but reproduces clonally. Hered (Edinb) 116:491–501 http://dx.doi.org/10.1038/hdy.2016.5.
106. Au CH, Wong MC, Bao D, Zhang M, Song C, Song W, Law PTW, Kües U, Kwan HS. 2014. The genetic structure of the A mating-type locus of Lentinula edodes. Gene 535:184–190 http://dx.doi.org/10.1016/j.gene.2013.11.036.
107. Hsueh YP, Fraser JA, Heitman J. 2008. Transitions in sexuality: recapitulation of an ancestral tri- and tetrapolar mating system in Cryptococcus neoformans. Eukaryot Cell 7:1847–1855 http://dx.doi.org/10.1128/EC.00271-08.
108. Heitman J, Sun S, James TY. 2013. Evolution of fungal sexual reproduction. Mycologia 105:1–27 http://dx.doi.org/10.3852/12-253.
109. Hibbett DS, Donoghue MJ. 2001. Analysis of character correlations among wood decay mechanisms, mating systems, and substrate ranges in homobasidiomycetes. Syst Biol 50:215–242 http://dx.doi.org/10.1080/10635150151125879.
110. Wang QM, Begerow D, Groenewald M, Liu XZ, Theelen B, Bai FY, Boekhout T. 2015. Multigene phylogeny and taxonomic revision of yeasts and related fungi in the Ustilaginomycotina. Stud Mycol 81:55–83 http://dx.doi.org/10.1016/j.simyco.2015.10.004.
111. Froeliger EH, Leong SA. 1991. The a mating-type alleles of Ustilago maydis are idiomorphs. Gene 100:113–122 http://dx.doi.org/10.1016/0378-1119(91)90356-G.
112. Kronstad JW, Leong SA. 1989. Isolation of two alleles of the b locus of Ustilago maydis. Proc Natl Acad Sci USA 86:978–982 http://dx.doi.org/10.1073/pnas.86.3.978. [PubMed]
113. Bakkeren G, Kronstad JW. 1994. Linkage of mating-type loci distinguishes bipolar from tetrapolar mating in basidiomycetous smut fungi. Proc Natl Acad Sci USA 91:7085–7089 http://dx.doi.org/10.1073/pnas.91.15.7085.
114. Bakkeren G, Kronstad JW. 1996. The pheromone cell signaling components of the Ustilago a mating-type loci determine intercompatibility between species. Genetics 143:1601–1613. [PubMed]
115. Lee N, Bakkeren G, Wong K, Sherwood JE, Kronstad JW. 1999. The mating-type and pathogenicity locus of the fungus Ustilago hordei spans a 500-kb region. Proc Natl Acad Sci USA 96:15026–15031 http://dx.doi.org/10.1073/pnas.96.26.15026.
116. Kämper J, et al. 2006. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444:97–101 http://dx.doi.org/10.1038/nature05248.
117. Schirawski J, Mannhaupt G, Münch K, Brefort T, Schipper K, Doehlemann G, Di Stasio M, Rössel N, Mendoza-Mendoza A, Pester D, Müller O, Winterberg B, Meyer E, Ghareeb H, Wollenberg T, Münsterkötter M, Wong P, Walter M, Stukenbrock E, Güldener U, Kahmann R. 2010. Pathogenicity determinants in smut fungi revealed by genome comparison. Science 330:1546–1548 http://dx.doi.org/10.1126/science.1195330.
118. Laurie JD, Ali S, Linning R, Mannhaupt G, Wong P, Güldener U, Münsterkötter M, Moore R, Kahmann R, Bakkeren G, Schirawski J. 2012. Genome comparison of barley and maize smut fungi reveals targeted loss of RNA silencing components and species-specific presence of transposable elements. Plant Cell 24:1733–1745 http://dx.doi.org/10.1105/tpc.112.097261.
119. Que Y, Xu L, Wu Q, Liu Y, Ling H, Liu Y, Zhang Y, Guo J, Su Y, Chen J, Wang S, Zhang C. 2014. Genome sequencing of Sporisorium scitamineum provides insights into the pathogenic mechanisms of sugarcane smut. BMC Genomics 15:996 http://dx.doi.org/10.1186/1471-2164-15-996. (Erratum, 16:244, doi:10.1186/s12864-015-1336-4.)
120. Taniguti LM, Schaker PDC, Benevenuto J, Peters LP, Carvalho G, Palhares A, Quecine MC, Nunes FRS, Kmit MCP, Wai A, Hausner G, Aitken KS, Berkman PJ, Fraser JA, Moolhuijzen PM, Coutinho LL, Creste S, Vieira MLC, Kitajima JP, Monteiro-Vitorello CB. 2015. Complete genome sequence of Sporisorium scitamineum and biotrophic interaction transcriptome with sugarcane. PLoS One 10:e0129318 http://dx.doi.org/10.1371/journal.pone.0129318.
121. Rabe F, Bosch J, Stirnberg A, Guse T, Bauer L, Seitner D, Rabanal FA, Czedik-Eysenberg A, Uhse S, Bindics J, Genenncher B, Navarrete F, Kellner R, Ekker H, Kumlehn J, Vogel JP, Gordon SP, Marcel TC, Münsterkötter M, Walter MC, Sieber CMK, Mannhaupt G, Güldener U, Kahmann R, Djamei A. 2016. A complete toolset for the study of Ustilago bromivora and Brachypodium sp. as a fungal-temperate grass pathosystem. eLife 5:e20522 http://dx.doi.org/10.7554/eLife.20522.
122. Gray YH. 2000. It takes two transposons to tango: transposable-element-mediated chromosomal rearrangements. Trends Genet 16:461–468 http://dx.doi.org/10.1016/S0168-9525(00)02104-1.
123. Gioti A, Nystedt B, Li W, Xu J, Andersson A, Averette AF, Münch K, Wang X, Kappauf C, Kingsbury JM, Kraak B, Walker LA, Johansson HJ, Holm T, Lehtiö J, Stajich JE, Mieczkowski P, Kahmann R, Kennell JC, Cardenas ME, Lundeberg J, Saunders CW, Boekhout T, Dawson TL, Munro CA, de Groot PW, Butler G, Heitman J, Scheynius A. 2013. Genomic insights into the atopic eczema-associated skin commensal yeast Malassezia sympodialis. MBio 4:e00572-12 http://dx.doi.org/10.1128/mBio.00572-12.
124. Wu G, Zhao H, Li C, Rajapakse MP, Wong WC, Xu J, Saunders CW, Reeder NL, Reilman RA, Scheynius A, Sun S, Billmyre BR, Li W, Averette AF, Mieczkowski P, Heitman J, Theelen B, Schröder MS, De Sessions PF, Butler G, Maurer-Stroh S, Boekhout T, Nagarajan N, Dawson TL Jr. 2015. Genus-wide comparative genomics of Malassezia delineates its phylogeny, physiology, and niche adaptation on human skin. PLoS Genet 11:e1005614 http://dx.doi.org/10.1371/journal.pgen.1005614.
125. Xu J, Saunders CW, Hu P, Grant RA, Boekhout T, Kuramae EE, Kronstad JW, Deangelis YM, Reeder NL, Johnstone KR, Leland M, Fieno AM, Begley WM, Sun Y, Lacey MP, Chaudhary T, Keough T, Chu L, Sears R, Yuan B, Dawson TL Jr. 2007. Dandruff-associated Malassezia genomes reveal convergent and divergent virulence traits shared with plant and human fungal pathogens. Proc Natl Acad Sci USA 104:18730–18735 http://dx.doi.org/10.1073/pnas.0706756104.
126. Hagen F, Khayhan K, Theelen B, Kolecka A, Polacheck I, Sionov E, Falk R, Parnmen S, Lumbsch HT, Boekhout T. 2015. Recognition of seven species in the Cryptococcus gattii/ Cryptococcus neoformans species complex. Fungal Genet Biol 78:16–48 http://dx.doi.org/10.1016/j.fgb.2015.02.009.
127. Hull CM, Boily MJ, Heitman J. 2005. Sex-specific homeodomain proteins Sxi1α and Sxi2a coordinately regulate sexual development in Cryptococcus neoformans. Eukaryot Cell 4:526–535 http://dx.doi.org/10.1128/EC.4.3.526-535.2005.
128. Hsueh YP, Idnurm A, Heitman J. 2006. Recombination hotspots flank the Cryptococcus mating-type locus: implications for the evolution of a fungal sex chromosome. PLoS Genet 2:e184 http://dx.doi.org/10.1371/journal.pgen.0020184.
129. Sun S, Billmyre RB, Mieczkowski PA, Heitman J. 2014. Unisexual reproduction drives meiotic recombination and phenotypic and karyotypic plasticity in Cryptococcus neoformans. PLoS Genet 10:e1004849 http://dx.doi.org/10.1371/journal.pgen.1004849.
130. Janbon G, et al. 2014. Analysis of the genome and transcriptome of Cryptococcus neoformans var. grubii reveals complex RNA expression and microevolution leading to virulence attenuation. PLoS Genet 10:e1004261 http://dx.doi.org/10.1371/journal.pgen.1004261.
131. Sun S, Xu J. 2009. Chromosomal rearrangements between serotype A and D strains in Cryptococcus neoformans. PLoS One 4:e5524 http://dx.doi.org/10.1371/journal.pone.0005524.
132. Kourist R, Bracharz F, Lorenzen J, Kracht ON, Chovatia M, Daum C, Deshpande S, Lipzen A, Nolan M, Ohm RA, Grigoriev IV, Sun S, Heitman J, Brück T, Nowrousian M. 2015. Genomics and transcriptomics analyses of the oil-accumulating basidiomycete yeast Trichosporon oleaginosus: insights into substrate utilization and alternative evolutionary trajectories of fungal mating systems. MBio 6:e00918-15 http://dx.doi.org/10.1128/mBio.00918-15.
133. Idnurm A, Hood ME, Johannesson H, Giraud T. 2015. Contrasted patterns in mating-type chromosomes in fungi: hotspots versus coldspots of recombination. Fungal Biol Rev 29:220–229 http://dx.doi.org/10.1016/j.fbr.2015.06.001.
134. Le Gac M, Hood ME, Fournier E, Giraud T. 2007. Phylogenetic evidence of host-specific cryptic species in the anther smut fungus. Evolution 61:15–26 http://dx.doi.org/10.1111/j.1558-5646.2007.00002.x.
135. Le Gac M, Hood ME, Giraud T. 2007. Evolution of reproductive isolation within a parasitic fungal species complex. Evolution 61:1781–1787 http://dx.doi.org/10.1111/j.1558-5646.2007.00144.x.
136. Bernasconi G, Antonovics J, Biere A, Charlesworth D, Delph LF, Filatov D, Giraud T, Hood ME, Marais GA, McCauley D, Pannell JR, Shykoff JA, Vyskot B, Wolfe LM, Widmer A. 2009. Silene as a model system in ecology and evolution. Hered (Edinb) 103:5–14 http://dx.doi.org/10.1038/hdy.2009.34.
137. Devier B, Aguileta G, Hood ME, Giraud T. 2009. Ancient trans-specific polymorphism at pheromone receptor genes in basidiomycetes. Genetics 181:209–223 http://dx.doi.org/10.1534/genetics.108.093708.
138. Kniep H. 1919. Untersuchungen über den Antherenbrand ( Ustilago violacea Pers.). Ein Beitrag zum Sexualitätsproblem. Ztschr Bot 11:257–284.
139. Hood ME. 2002. Dimorphic mating-type chromosomes in the fungus Microbotryum violaceum. Genetics 160:457–461. [PubMed]
140. Giraud T, Jonot O, Shykoff JA. 2005. Selfing propensity under choice conditions in a parasitic fungus, Microbotryum violaceum, and parameters influencing infection success in artificial inoculations. Int J Plant Sci 166:649–657 http://dx.doi.org/10.1086/430098.
141. Hood ME, Antonovics J. 2000. Intratetrad mating, heterozygosity, and the maintenance of deleterious alleles in Microbotryum violaceum (= Ustilago violacea). Hered (Edinb) 85:231–241 http://dx.doi.org/10.1046/j.1365-2540.2000.00748.x.
142. Hood ME, Antonovics J, Koskella B. 2004. Shared forces of sex chromosome evolution in haploid-mating and diploid-mating organisms: Microbotryum violaceum and other model organisms. Genetics 168:141–146 http://dx.doi.org/10.1534/genetics.104.029900.
143. Giraud T. 2004. Patterns of within population dispersal and mating of the fungus Microbotryum violaceum parasitising the plant Silene latifolia. Hered (Edinb) 93:559–565 http://dx.doi.org/10.1038/sj.hdy.6800554.
144. Gladieux P, Vercken E, Fontaine MC, Hood ME, Jonot O, Couloux A, Giraud T. 2011. Maintenance of fungal pathogen species that are specialized to different hosts: allopatric divergence and introgression through secondary contact. Mol Biol Evol 28:459–471 http://dx.doi.org/10.1093/molbev/msq235.
145. Badouin H, Hood ME, Gouzy J, Aguileta G, Siguenza S, Perlin MH, Cuomo CA, Fairhead C, Branca A, Giraud T. 2015. Chaos of rearrangements in the mating-type chromosomes of the anther-smut fungus Microbotryum lychnidis-dioicae. Genetics 200:1275–1284 http://dx.doi.org/10.1534/genetics.115.177709.
146. Hood ME, Petit E, Giraud T. 2013. Extensive divergence between mating-type chromosomes of the anther-smut fungus. Genetics 193:309–315 http://dx.doi.org/10.1534/genetics.112.146266.
147. Bachtrog D. 2013. Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat Rev Genet 14:113–124 http://dx.doi.org/10.1038/nrg3366.
148. Fontanillas E, Hood ME, Badouin H, Petit E, Barbe V, Gouzy J, de Vienne DM, Aguileta G, Poulain J, Wincker P, Chen Z, Toh SS, Cuomo CA, Perlin MH, Gladieux P, Giraud T. 2015. Degeneration of the nonrecombining regions in the mating-type chromosomes of the anther-smut fungi. Mol Biol Evol 32:928–943 http://dx.doi.org/10.1093/molbev/msu396.
149. Kües U, Göttgens B, Stratmann R, Richardson WV, O’Shea SF, Casselton LA. 1994. A chimeric homeodomain protein causes self-compatibility and constitutive sexual development in the mushroom Coprinus cinereus. EMBO J 13:4054–4059. [PubMed]
150. Haylock RW, Economou A, Casselton LA. 1980. Dikaryon formation in Coprinus cinereus: selection and identification of B factor mutants. J Gen Microbiol 121:17–26.
151. Olesnicky NS, Brown AJ, Honda Y, Dyos SL, Dowell SJ, Casselton LA. 2000. Self-compatible B mutants in coprinus with altered pheromone-receptor specificities. Genetics 156:1025–1033. [PubMed]
152. James TY, Srivilai P, Kües U, Vilgalys R. 2006. Evolution of the bipolar mating system of the mushroom Coprinellus disseminatus from its tetrapolar ancestors involves loss of mating-type-specific pheromone receptor function. Genetics 172:1877–1891 http://dx.doi.org/10.1534/genetics.105.051128. [PubMed]
153. Aimi T, Yoshida R, Ishikawa M, Bao D, Kitamoto Y. 2005. Identification and linkage mapping of the genes for the putative homeodomain protein ( hox1) and the putative pheromone receptor protein homologue ( rcb1) in a bipolar basidiomycete, Pholiota nameko. Curr Genet 48:184–194 http://dx.doi.org/10.1007/s00294-005-0012-7.
154. Yi R, Tachikawa T, Ishikawa M, Mukaiyama H, Bao D, Aimi T. 2009. Genomic structure of the A mating-type locus in a bipolar basidiomycete, Pholiota nameko. Mycol Res 113:240–248 http://dx.doi.org/10.1016/j.mycres.2008.11.002.
155. Olson A, et al. 2012. Insight into trade-off between wood decay and parasitism from the genome of a fungal forest pathogen. New Phytol 194:1001–1013 http://dx.doi.org/10.1111/j.1469-8137.2012.04128.x.
156. Perrin N. 2012. What uses are mating types? The “developmental switch” model. Evolution 66:947–956 http://dx.doi.org/10.1111/j.1558-5646.2011.01562.x.
157. Wilson AM, Wilken PM, van der Nest MA, Steenkamp ET, Wingfield MJ, Wingfield BD. 2015. Homothallism: an umbrella term for describing diverse sexual behaviours. IMA Fungus 6:207–214 http://dx.doi.org/10.5598/imafungus.2015.06.01.13.
158. Roach KC, Feretzaki M, Sun S, Heitman J. 2014. Unisexual Reproduction, p 255–305. In Friedmann T, Dunlap JC, Goodwin SF (ed), Advances in Genetics, vol 85. Academic Press, San Diego, CA.
159. Raju NB, Perkins DD. 1994. Diverse programs of ascus development in pseudohomothallic species of Neurospora, Gelasinospora, and Podospora. Dev Genet 15:104–118 http://dx.doi.org/10.1002/dvg.1020150111.
160. Merino ST, Nelson MA, Jacobson DJ, Natvig DO. 1996. Pseudohomothallism and evolution of the mating-type chromosome in Neurospora tetrasperma. Genetics 143:789–799. [PubMed]
161. Callac P, Spataro C, Caille A, Imbernon M. 2006. Evidence for outcrossing via the Buller phenomenon in a substrate simultaneously inoculated with spores and mycelium of Agaricus bisporus. Appl Environ Microbiol 72:2366–2372 http://dx.doi.org/10.1128/AEM.72.4.2366-2372.2006.
162. Lin X, Heitman J. 2007. Mechanisms of homothallism in fungi and transitions between heterothallism and homothallism, p 35–57. In Heitman J, Kronstad JW, Taylor JW, Casselton LA (ed), Sex in Fungi: Molecular Determination and Evolutionary Implications. ASM Press, Washington, DC. http://dx.doi.org/10.1128/9781555815837.ch3
163. Ullrich RC, Raper JR. 1975. Primary homothallism-relation to heterothallism in the regulation of sexual morphogenesis in Sistotrema. Genetics 80:311–321. [PubMed]
164. Griffith GW, Hedger JN. 1994. The breeding biology of biotypes of the witches’ broom pathogen of cocoa, Crinipellis perniciosa. Heredity 72:278–289 http://dx.doi.org/10.1038/hdy.1994.38.
165. Kües U, Navarro-González M. 2010. Mating-type orthologous genes in the primarily homothallic Moniliophthora perniciosa, the causal agent of witches’ broom disease in cacao. J Basic Microbiol 50:442–451 http://dx.doi.org/10.1002/jobm.201000013.
166. David-Palma M, Libkind D, Sampaio JP. 2014. Global distribution, diversity hot spots and niche transitions of an astaxanthin-producing eukaryotic microbe. Mol Ecol 23:921–932 http://dx.doi.org/10.1111/mec.12642.
167. Bellora N, Moline M, David-Palma M, Coelho MA, Hittinger CT, Sampaio JP, Goncalves P, Libkind D. 2016. Comparative genomics provides new insights into the diversity, physiology, and sexuality of the only industrially exploited tremellomycete: Phaffia rhodozyma. BMC Genomics 17:901. doi:10.1186/s12864-016-3244-7.
168. David-Palma M, Sampaio JP, Gonçalves P. 2016. Genetic dissection of sexual reproduction in a primary homothallic basidiomycete. PLoS Genet 12:e1006110 http://dx.doi.org/10.1371/journal.pgen.1006110.
169. Lin X, Hull CM, Heitman J. 2005. Sexual reproduction between partners of the same mating type in Cryptococcus neoformans. Nature 434:1017–1021 http://dx.doi.org/10.1038/nature03448.
170. Ni M, Feretzaki M, Li W, Floyd-Averette A, Mieczkowski P, Dietrich FS, Heitman J. 2013. Unisexual and heterosexual meiotic reproduction generate aneuploidy and phenotypic diversity de novo in the yeast Cryptococcus neoformans. PLoS Biol 11:e1001653 http://dx.doi.org/10.1371/journal.pbio.1001653.
171. Heitman J, Kozel TR, Kwon-Chung KJ, Perfect JR, Casadevall A. 2011. Cryptococcus: from Human Pathogen to Model Yeast. ASM Press, Washington, DC.
172. Alby K, Bennett RJ. 2011. Interspecies pheromone signaling promotes biofilm formation and same-sex mating in Candida albicans. Proc Natl Acad Sci USA 108:2510–2515 http://dx.doi.org/10.1073/pnas.1017234108.
173. Alby K, Schaefer D, Bennett RJ. 2009. Homothallic and heterothallic mating in the opportunistic pathogen Candida albicans. Nature 460:890–893 http://dx.doi.org/10.1038/nature08252.
174. Wilson AM, Godlonton T, van der Nest MA, Wilken PM, Wingfield MJ, Wingfield BD. 2015. Unisexual reproduction in Huntiella moniliformis. Fungal Genet Biol 80:1–9 http://dx.doi.org/10.1016/j.fgb.2015.04.008.
175. Whitehouse HLK. 1949. Heterothallism and sex in the fungi. Biol Rev Camb Philos Soc 24:411–447 http://dx.doi.org/10.1111/j.1469-185X.1949.tb00582.x.
176. Aanen DK, Hoekstra RF. 2007. Why sex is good: on fungi and beyond, p 527–534. In Heitman J, Kronstad JW, Taylor JW, Casselton LA (ed), Sex in Fungi: Molecular Determination and Evolutionary Implications. ASM Press, Washington, DC. http://dx.doi.org/10.1128/9781555815837.ch32
177. Roach KC, Heitman J. 2014. Unisexual reproduction reverses Muller’s ratchet. Genetics 198:1059–1069 http://dx.doi.org/10.1534/genetics.114.170472.
178. Attanayake RN, Tennekoon V, Johnson DA, Porter LD, del Río-Mendoza L, Jiang D, Chen W. 2014. Inferring outcrossing in the homothallic fungus Sclerotinia sclerotiorum using linkage disequilibrium decay. Hered (Edinb) 113:353–363 http://dx.doi.org/10.1038/hdy.2014.37.
179. Talas F, McDonald BA. 2015. Genome-wide analysis of Fusarium graminearum field populations reveals hotspots of recombination. BMC Genomics 16:996 http://dx.doi.org/10.1186/s12864-015-2166-0.
180. López-Villavicencio M, Debets AJ, Slakhorst M, Giraud T, Schoustra SE. 2013. Deleterious effects of recombination and possible nonrecombinatorial advantages of sex in a fungal model. J Evol Biol 26:1968–1978 http://dx.doi.org/10.1111/jeb.12196.
181. Otto SP. 2009. The evolutionary enigma of sex. Am Nat 174(Suppl 1) :S1–S14 http://dx.doi.org/10.1086/599084.
182. Selker EU. 1991. Repeat-induced point mutation and DNA methylation, p 258–265. In Bennett JW, Lasure LL (ed), More Gene Manipulations in Fungi. Academic Press, San Diego, CA. http://dx.doi.org/10.1016/B978-0-12-088642-5.50018-1
183. Shiu PK, Raju NB, Zickler D, Metzenberg RL. 2001. Meiotic silencing by unpaired DNA. Cell 107:905–916 http://dx.doi.org/10.1016/S0092-8674(01)00609-2.
184. Grigoriev IV, Nikitin R, Haridas S, Kuo A, Ohm R, Otillar R, Riley R, Salamov A, Zhao X, Korzeniewski F, Smirnova T, Nordberg H, Dubchak I, Shabalov I. 2014. MycoCosm portal: gearing up for 1000 fungal genomes. Nucleic Acids Res 42(D1) :D699–D704 http://dx.doi.org/10.1093/nar/gkt1183.
185. Cuomo CA, Birren BW. 2010. The Fungal Genome Initiative and lessons learned from genome sequencing. Methods Enzymol 470:833–855.
186. Cuomo CA, Bakkeren G, Khalil HB, Panwar V, Joly D, Linning R, Sakthikumar S, Song X, Adiconis X, Fan L, Goldberg JM, Levin JZ, Young S, Zeng Q, Anikster Y, Bruce M, Wang M, Yin C, McCallum B, Szabo LJ, Hulbert S, Chen X, Fellers JP. 2017. Comparative analysis highlights variable genome content of wheat rusts and divergence of the mating loci. G3 (Bethesda) 7:361–376 http://dx.doi.org/10.1534/g3.116.032797.
187. Anikster Y, Eilam T, Mittelman L, Szabo LJ, Bushnell WR. 1999. Pycnial nectar of rust fungi induces cap formation on pycniospores of opposite mating type. Mycologia 91:858–870 http://dx.doi.org/10.2307/3761539.
188. Lawrence GJ. 1980. Multiple mating-type specificities in the flax rust Melampsora lini. Science 209:501–503 http://dx.doi.org/10.1126/science.209.4455.501.
189. Narisawa K, Yamaoka Y, Katsuya K. 1994. Mating type of isolates derived from the spermogonial state of Puccinia coronata var. coronata. Mycoscience 35:131–135 http://dx.doi.org/10.1007/BF02318489.
190. Raper JR. 1960. The control of sex in fungi. Am J Bot 47:794–808 http://dx.doi.org/10.2307/2439117.
191. Travis J. 2006. Is it what we know or who we know? Choice of organism and robustness of inference in ecology and evolutionary biology: (American Society of Naturalists Presidential Address). Am Nat 167:303–314.
192. Wang Z, Nilsson RH, James TY, Dai Y, Townsend JP. 2016. Future perspectives and challenges of fungal systematics in the age of big data, p 25–46. In Li D-W (ed), Biology of Microfungi. Springer International Publishing, Cham, Switzerland. http://dx.doi.org/10.1007/978-3-319-29137-6_3
193. Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274 http://dx.doi.org/10.1093/molbev/msu300.
194. Coelho MA, Gonçalves C, Sampaio JP, Gonçalves P. 2013. Extensive intra-kingdom horizontal gene transfer converging on a fungal fructose transporter gene. PLoS Genet 9:e1003587 http://dx.doi.org/10.1371/journal.pgen.1003587.
195. Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780 http://dx.doi.org/10.1093/molbev/mst010.
196. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. 2009. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973 http://dx.doi.org/10.1093/bioinformatics/btp348.
197. Bennett RJ, Turgeon BG. 2017. Fungal sex: the Ascomycota. Microbiol Spectrum 4(5) :FUNK-0005-2016. doi:10.1128/microbiolspec.FUNK-0005-2016.
Loading

Article metrics loading...

/content/journal/microbiolspec/10.1128/microbiolspec.FUNK-0046-2016
2017-06-09
2021-04-12

Abstract:

Fungi of the Basidiomycota, representing major pathogen lineages and mushroom-forming species, exhibit diverse means to achieve sexual reproduction, with particularly varied mechanisms to determine compatibilities of haploid mating partners. For species that require mating between distinct genotypes, discrimination is usually based on both the reciprocal exchange of diffusible mating pheromones, rather than sexes, and the interactions of homeodomain protein signals after cell fusion. Both compatibility factors must be heterozygous in the product of mating, and genetic linkage relationships of the mating pheromone/receptor and homeodomain genes largely determine the complex patterns of mating-type variation. Independent segregation of the two compatibility factors can create four haploid mating genotypes from meiosis, referred to as tetrapolarity. This condition is thought to be ancestral to the basidiomycetes. Alternatively, cosegregation by linkage of the two mating factors, or in some cases the absence of the pheromone-based discrimination, yields only two mating types from meiosis, referred to as bipolarity. Several species are now known to have large and highly rearranged chromosomal regions linked to mating-type genes. At the population level, polymorphism of the mating-type genes is an exceptional aspect of some basidiomycete fungi, where selection under outcrossing for rare, intercompatible allelic variants is thought to be responsible for numbers of mating types that may reach several thousand. Advances in genome sequencing and assembly are yielding new insights by comparative approaches among and within basidiomycete species, with the promise to resolve the evolutionary origins and dynamics of mating compatibility genetics in this major eukaryotic lineage.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

/deliver/fulltext/microbiolspec/5/3/FUNK-0046-2016.html?itemId=/content/journal/microbiolspec/10.1128/microbiolspec.FUNK-0046-2016&mimeType=html&fmt=ahah

Figures

Fungal Sex: The Basidiomycota
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0046-2016-1,webId=/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0046-2016-1,properties={foaf_givenname=Marco A., foaf_name=Marco A. Coelho, foaf_surname=Coelho, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.FUNK-0046-2016-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0046-2016-2,webId=/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0046-2016-2,properties={foaf_givenname=Guus, foaf_name=Guus Bakkeren, foaf_surname=Bakkeren, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.FUNK-0046-2016-aff2]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0046-2016-3,webId=/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0046-2016-3,properties={foaf_givenname=Sheng, foaf_name=Sheng Sun, foaf_surname=Sun, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.FUNK-0046-2016-aff3]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0046-2016-4,webId=/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0046-2016-4,properties={foaf_givenname=Michael E., foaf_name=Michael E. Hood, foaf_surname=Hood, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.FUNK-0046-2016-aff4]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0046-2016-5,webId=/content/author/microbiolspec/10.1128/microbiolspec.FUNK-0046-2016-5,properties={foaf_givenname=Tatiana, foaf_name=Tatiana Giraud, foaf_surname=Giraud, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.FUNK-0046-2016-aff5]]}]]
Citation: Coelho M, Bakkeren G, Sun S, Hood M, Giraud T. 2017. Fungal sex: the basidiomycota. microbiolspec 5(3): doi:10.1128/microbiolspec.FUNK-0046-2016
/content/microbiolspec/10.1128/microbiolspec.FUNK-0046-2016.fig1
FIGURE 1
General life cycles of dimorphic and mushroom-forming basidiomycetes. Three basidiomycetes are pictured where sexual reproduction and a dimorphic switch between a yeast cell and a hyphal form are crucial to infection of plant (A, B) or animal (C) hosts. The haploid yeast forms of the maize smut (A) and the anther smut spp. (B) are nonpathogenic and can undergo asexual mitotic vegetative growth. In , the yeast stage is, however, short-lived because mating occurs mostly between cells within the same tetrad. Upon mating with a compatible partner, both fungi switch to an enduring infection hyphal form (dikaryon; n + n) that can invade the host plant. Proliferation and differentiation of in the plant culminates with the production of masses of wind-dispersing diploid spores (teliospores; 2n) in large tumor-like tissues, whereas in , teliospores are formed in the anthers of infected flowers and transmitted by pollinators onto healthy plants. In the case of , the single-celled yeast form may be free-living or mycoparasitic. A similar dimorphic switch occurs upon mating of yeast cells of opposite mating type ( or α), ultimately resulting in the infectious propagules (basidiospores) that potentially infect an animal host after dispersal. These infectious structures may also be generated by haploid selfing (depicted with gray background), where fusion occurs between homothallic cells carrying identical alleles (α/α diploid is depicted) and form monokaryotic hyphae with unfused clamp connections (see text for details). In mushroom-forming fungi such as , germination of haploid spores yields haploid monokaryons capable of independent growth. When two compatible monokaryons meet, a fertile clamped dikaryon is formed which develops into fruiting bodies (mushrooms) triggered upon suitable environmental cues, where basidia arise. In all these and other basidiomycetes, nuclear fusion (karyogamy) is usually delayed until the formation of basidia (or teliospores). Meiosis ensues, generating four haploid nuclei, which give rise to basidiospores to complete the cycle. Adapted from Morrow and Fraser ( 2 ) and Nieuwenhuis et al. ( 17 ) with permission of the publishers.
microbiolspec/5/3/FUNK-0046-2016-fig1_thmb.gif
microbiolspec/5/3/FUNK-0046-2016-fig1.gif
Image of FIGURE 1

Click to view

FIGURE 1

General life cycles of dimorphic and mushroom-forming basidiomycetes. Three basidiomycetes are pictured where sexual reproduction and a dimorphic switch between a yeast cell and a hyphal form are crucial to infection of plant (A, B) or animal (C) hosts. The haploid yeast forms of the maize smut (A) and the anther smut spp. (B) are nonpathogenic and can undergo asexual mitotic vegetative growth. In , the yeast stage is, however, short-lived because mating occurs mostly between cells within the same tetrad. Upon mating with a compatible partner, both fungi switch to an enduring infection hyphal form (dikaryon; n + n) that can invade the host plant. Proliferation and differentiation of in the plant culminates with the production of masses of wind-dispersing diploid spores (teliospores; 2n) in large tumor-like tissues, whereas in , teliospores are formed in the anthers of infected flowers and transmitted by pollinators onto healthy plants. In the case of , the single-celled yeast form may be free-living or mycoparasitic. A similar dimorphic switch occurs upon mating of yeast cells of opposite mating type ( or α), ultimately resulting in the infectious propagules (basidiospores) that potentially infect an animal host after dispersal. These infectious structures may also be generated by haploid selfing (depicted with gray background), where fusion occurs between homothallic cells carrying identical alleles (α/α diploid is depicted) and form monokaryotic hyphae with unfused clamp connections (see text for details). In mushroom-forming fungi such as , germination of haploid spores yields haploid monokaryons capable of independent growth. When two compatible monokaryons meet, a fertile clamped dikaryon is formed which develops into fruiting bodies (mushrooms) triggered upon suitable environmental cues, where basidia arise. In all these and other basidiomycetes, nuclear fusion (karyogamy) is usually delayed until the formation of basidia (or teliospores). Meiosis ensues, generating four haploid nuclei, which give rise to basidiospores to complete the cycle. Adapted from Morrow and Fraser ( 2 ) and Nieuwenhuis et al. ( 17 ) with permission of the publishers.

Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0046-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.FUNK-0046-2016.fig2
FIGURE 2
Phylogeny of the Basidiomycota indicating the breeding system and the number of genes across representative species of the three subphyla. The breeding system and the different taxonomic lineages are color-coded as given in the key and are kept consistent in all figures. Gene numbers shown for each species were obtained either from previous reports ( 20 , 41 , 100 ) or from newly surveyed genome data (marked with a hash sign after the species name). In the Agaricomycetes, values shown in parentheses are putative non-mating-type pheromone receptors. A question mark indicates cases where information on the breeding system is not available or is uncertain (e.g., because the sexual stage of a species is unknown). A schematic representation of the and loci is given in Fig. 3 for representative species of each lineage marked with numbers enclosed in white circles. Letters in superscript next to the number of pheromone precursor genes indicate that (a) all genes encode the same mature pheromone peptide or that (b) no CAAX motif was detected in one of the putative pheromone precursors. The species phylogenetic tree was constructed in IQ-TREE ( 193 ) using a previously described approach ( 194 ). Branch support values are shown in the tree nodes as given in the key and were assessed with the ultrafast bootstrap approximation (UFBoot) and the approximate likelihood ratio test (SH-aLRT), each with 1,000 replicates. The basidiomycete clade is rooted with sequences from Ascomycete fungi.
microbiolspec/5/3/FUNK-0046-2016-fig2_thmb.gif
microbiolspec/5/3/FUNK-0046-2016-fig2.gif
Image of FIGURE 2

Click to view

FIGURE 2

Phylogeny of the Basidiomycota indicating the breeding system and the number of genes across representative species of the three subphyla. The breeding system and the different taxonomic lineages are color-coded as given in the key and are kept consistent in all figures. Gene numbers shown for each species were obtained either from previous reports ( 20 , 41 , 100 ) or from newly surveyed genome data (marked with a hash sign after the species name). In the Agaricomycetes, values shown in parentheses are putative non-mating-type pheromone receptors. A question mark indicates cases where information on the breeding system is not available or is uncertain (e.g., because the sexual stage of a species is unknown). A schematic representation of the and loci is given in Fig. 3 for representative species of each lineage marked with numbers enclosed in white circles. Letters in superscript next to the number of pheromone precursor genes indicate that (a) all genes encode the same mature pheromone peptide or that (b) no CAAX motif was detected in one of the putative pheromone precursors. The species phylogenetic tree was constructed in IQ-TREE ( 193 ) using a previously described approach ( 194 ). Branch support values are shown in the tree nodes as given in the key and were assessed with the ultrafast bootstrap approximation (UFBoot) and the approximate likelihood ratio test (SH-aLRT), each with 1,000 replicates. The basidiomycete clade is rooted with sequences from Ascomycete fungi.

Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0046-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.FUNK-0046-2016.fig3
FIGURE 3a
Schematic showing the genomic structure and diversity of loci in representative basidiomycete lineages. The genomic organization of the homeodomain () and pheromone/receptor () loci is shown for selected species of the Agaricomycotina and the Ustilaginomycotina and Pucciniomycotina. Arrows indicate genes and their direction of transcription. Putative loci are shaded in light brown, and genes are colored as indicated in the key with different color grades representing different alleles (or paralogs). When known, conserved genes flanking loci (colored light yellow or light blue) are shown within each lineage. Genes that encode components of the pheromone response pathway are shown in pink and are in many cases within the locus. Putative homologs of a protein required for posttranslational modification of pheromone precursors (isoprenyl cysteine methyltransferase [ICMT]) are colored purple and appear near the locus in some species. loci no longer determining mating-type specificity in bipolar Agaricomycetes are depicted with a gray background. In , the two mating-type chromosomes are highly rearranged and enriched in transposable elements, so that only a small number of genes is depicted. Of note, whereas in and genes are far apart on the same chromosome, in and the two sets of genes are closer together. Other genes or genomic features are colored or represented as given in the key. For citations and additional details, see text. Gene names or their associated protein accession numbers are shown as they appear in their respective genome databases, except in species of Ustilaginomycotina and Tremellomycetes, where names were given based on sequence identity to the closest homolog in and , respectively.
microbiolspec/5/3/FUNK-0046-2016-fig3a_thmb.gif
microbiolspec/5/3/FUNK-0046-2016-fig3a.gif
Image of FIGURE 3a

Click to view

FIGURE 3a

Schematic showing the genomic structure and diversity of loci in representative basidiomycete lineages. The genomic organization of the homeodomain () and pheromone/receptor () loci is shown for selected species of the Agaricomycotina and the Ustilaginomycotina and Pucciniomycotina. Arrows indicate genes and their direction of transcription. Putative loci are shaded in light brown, and genes are colored as indicated in the key with different color grades representing different alleles (or paralogs). When known, conserved genes flanking loci (colored light yellow or light blue) are shown within each lineage. Genes that encode components of the pheromone response pathway are shown in pink and are in many cases within the locus. Putative homologs of a protein required for posttranslational modification of pheromone precursors (isoprenyl cysteine methyltransferase [ICMT]) are colored purple and appear near the locus in some species. loci no longer determining mating-type specificity in bipolar Agaricomycetes are depicted with a gray background. In , the two mating-type chromosomes are highly rearranged and enriched in transposable elements, so that only a small number of genes is depicted. Of note, whereas in and genes are far apart on the same chromosome, in and the two sets of genes are closer together. Other genes or genomic features are colored or represented as given in the key. For citations and additional details, see text. Gene names or their associated protein accession numbers are shown as they appear in their respective genome databases, except in species of Ustilaginomycotina and Tremellomycetes, where names were given based on sequence identity to the closest homolog in and , respectively.

Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0046-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.FUNK-0046-2016.fig3b
FIGURE 3b
Schematic showing the genomic structure and diversity of loci in representative basidiomycete lineages. The genomic organization of the homeodomain () and pheromone/receptor () loci is shown for selected species of the Agaricomycotina and the Ustilaginomycotina and Pucciniomycotina. Arrows indicate genes and their direction of transcription. Putative loci are shaded in light brown, and genes are colored as indicated in the key with different color grades representing different alleles (or paralogs). When known, conserved genes flanking loci (colored light yellow or light blue) are shown within each lineage. Genes that encode components of the pheromone response pathway are shown in pink and are in many cases within the locus. Putative homologs of a protein required for posttranslational modification of pheromone precursors (isoprenyl cysteine methyltransferase [ICMT]) are colored purple and appear near the locus in some species. loci no longer determining mating-type specificity in bipolar Agaricomycetes are depicted with a gray background. In , the two mating-type chromosomes are highly rearranged and enriched in transposable elements, so that only a small number of genes is depicted. Of note, whereas in and genes are far apart on the same chromosome, in and the two sets of genes are closer together. Other genes or genomic features are colored or represented as given in the key. For citations and additional details, see text. Gene names or their associated protein accession numbers are shown as they appear in their respective genome databases, except in species of Ustilaginomycotina and Tremellomycetes, where names were given based on sequence identity to the closest homolog in and , respectively.
microbiolspec/5/3/FUNK-0046-2016-fig3b_thmb.gif
microbiolspec/5/3/FUNK-0046-2016-fig3b.gif
Image of FIGURE 3b

Click to view

FIGURE 3b

Schematic showing the genomic structure and diversity of loci in representative basidiomycete lineages. The genomic organization of the homeodomain () and pheromone/receptor () loci is shown for selected species of the Agaricomycotina and the Ustilaginomycotina and Pucciniomycotina. Arrows indicate genes and their direction of transcription. Putative loci are shaded in light brown, and genes are colored as indicated in the key with different color grades representing different alleles (or paralogs). When known, conserved genes flanking loci (colored light yellow or light blue) are shown within each lineage. Genes that encode components of the pheromone response pathway are shown in pink and are in many cases within the locus. Putative homologs of a protein required for posttranslational modification of pheromone precursors (isoprenyl cysteine methyltransferase [ICMT]) are colored purple and appear near the locus in some species. loci no longer determining mating-type specificity in bipolar Agaricomycetes are depicted with a gray background. In , the two mating-type chromosomes are highly rearranged and enriched in transposable elements, so that only a small number of genes is depicted. Of note, whereas in and genes are far apart on the same chromosome, in and the two sets of genes are closer together. Other genes or genomic features are colored or represented as given in the key. For citations and additional details, see text. Gene names or their associated protein accession numbers are shown as they appear in their respective genome databases, except in species of Ustilaginomycotina and Tremellomycetes, where names were given based on sequence identity to the closest homolog in and , respectively.

Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0046-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.FUNK-0046-2016.fig4
FIGURE 4
Phylogeny of Basidiomycota pheromone receptor proteins. Amino acid sequences identified by BLAST from publicly available databases or from genome projects were retrieved for representative species of the tree subphyla of the Basidiomycota. A total of 106 sequences were manually inspected, amended where necessary, and aligned with MAFFT ( 195 ), and poorly aligned regions were trimmed with trimAl ( 196 ). The phylogenetic tree and branch support were obtained as in Fig. 2 , and the tree was rooted with Ste3p. GenBank accession numbers (*), Joint Genome Institute protein identifiers (**), and RIKEN/NBRP identifiers (***) are given after the strain name, with letters in superscript indicating (a) genomes assembled from available raw sequencing data and inspected locally, (b) genomic contigs/scaffolds lacking gene annotation, and (c) genes whose annotation was corrected. Species highlighted in boldface are shown in Fig. 3 , with arrows before their names indicating the allelic version (or paralog) of the pheromone receptor as colored in Fig. 3 . Of note, the and alleles in the Microbotryomycetes (Pucciniomycotina) displayed the deepest allelic divergence and trans-specific polymorphism, with the alleles of the different species branching together rather than each of these alleles clustering with the allele from the same species ( 42 , 45 , 137 ).
microbiolspec/5/3/FUNK-0046-2016-fig4_thmb.gif
microbiolspec/5/3/FUNK-0046-2016-fig4.gif
Image of FIGURE 4

Click to view

FIGURE 4

Phylogeny of Basidiomycota pheromone receptor proteins. Amino acid sequences identified by BLAST from publicly available databases or from genome projects were retrieved for representative species of the tree subphyla of the Basidiomycota. A total of 106 sequences were manually inspected, amended where necessary, and aligned with MAFFT ( 195 ), and poorly aligned regions were trimmed with trimAl ( 196 ). The phylogenetic tree and branch support were obtained as in Fig. 2 , and the tree was rooted with Ste3p. GenBank accession numbers (*), Joint Genome Institute protein identifiers (**), and RIKEN/NBRP identifiers (***) are given after the strain name, with letters in superscript indicating (a) genomes assembled from available raw sequencing data and inspected locally, (b) genomic contigs/scaffolds lacking gene annotation, and (c) genes whose annotation was corrected. Species highlighted in boldface are shown in Fig. 3 , with arrows before their names indicating the allelic version (or paralog) of the pheromone receptor as colored in Fig. 3 . Of note, the and alleles in the Microbotryomycetes (Pucciniomycotina) displayed the deepest allelic divergence and trans-specific polymorphism, with the alleles of the different species branching together rather than each of these alleles clustering with the allele from the same species ( 42 , 45 , 137 ).

Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0046-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.FUNK-0046-2016.fig5
FIGURE 5
Roles of and genes on the formation and maintenance of the dikaryon in . Pheromone signaling is not required to attract mates, and hyphal fusion is mating-type independent (diagram 1). Upon fusion, nuclei enter the mycelium of the other mate and migrate until they reach a hyphal tip cell (diagram 2). During hyphal tip elongation, the two types of haploid nuclei (depicted in white and black, representing different genotypes) pair at the tip cell (diagram 3), and at the place where mitosis will take place, a hook-like structure (called a clamp connection) is formed (diagram 4). The two nuclei divide synchronously: one of the nuclei divides in the direction of the clamp cell that is growing backward toward the main hyphae, while the other divides along the main hyphal axis (diagram 5). Septa are generated between the dividing nuclei. This way one nucleus stays temporarily entrapped in the clamp cell, one nucleus of the other type is enclosed in the newly formed subapical cell, and a nucleus of each type is maintained in the emerging hyphal tip cell (diagram 6). The clamp cell fuses with the subapical cell and releases the entrapped nucleus from the clamp cell, restoring the dikaryotic state of the subapical cell (diagram 7). In , steps controlled by (diagrams 2 and 7) and (diagrams 3 to 6) genes are colored red and green, respectively. See Casselton et al. ( 18 ) and Kües ( 90 ) for details. The micrograph at the bottom was obtained from Stajich et al. ( 86 ), with permission.
microbiolspec/5/3/FUNK-0046-2016-fig5_thmb.gif
microbiolspec/5/3/FUNK-0046-2016-fig5.gif
Image of FIGURE 5

Click to view

FIGURE 5

Roles of and genes on the formation and maintenance of the dikaryon in . Pheromone signaling is not required to attract mates, and hyphal fusion is mating-type independent (diagram 1). Upon fusion, nuclei enter the mycelium of the other mate and migrate until they reach a hyphal tip cell (diagram 2). During hyphal tip elongation, the two types of haploid nuclei (depicted in white and black, representing different genotypes) pair at the tip cell (diagram 3), and at the place where mitosis will take place, a hook-like structure (called a clamp connection) is formed (diagram 4). The two nuclei divide synchronously: one of the nuclei divides in the direction of the clamp cell that is growing backward toward the main hyphae, while the other divides along the main hyphal axis (diagram 5). Septa are generated between the dividing nuclei. This way one nucleus stays temporarily entrapped in the clamp cell, one nucleus of the other type is enclosed in the newly formed subapical cell, and a nucleus of each type is maintained in the emerging hyphal tip cell (diagram 6). The clamp cell fuses with the subapical cell and releases the entrapped nucleus from the clamp cell, restoring the dikaryotic state of the subapical cell (diagram 7). In , steps controlled by (diagrams 2 and 7) and (diagrams 3 to 6) genes are colored red and green, respectively. See Casselton et al. ( 18 ) and Kües ( 90 ) for details. The micrograph at the bottom was obtained from Stajich et al. ( 86 ), with permission.

Source: microbiolspec June 2017 vol. 5 no. 3 doi:10.1128/microbiolspec.FUNK-0046-2016
Permissions and Reprints Request Permissions
Download as Powerpoint

Supplemental Material

No supplementary material available for this content.

Back to top
This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error