Linkage To The Mating-Type Locus Across The Genus Microbotryum: Insights Into Nonrecombining Chromosomes

Evolution

Volumn 66, Issue 11, 2012, Pages 3519-3533

  Petit, Elsa ^a   Giraud, Tatiana ^b   de Vienne, Damien M ^c   Coelho, Marco A ^d   Aguileta, Gabriela ^c   Amselem, Joëlle ^e   Kreplak, Jonathan ^e   Poulain, Julie ^f   Gavory, Frédérick ^f   Wincker, Patrick ^f   Young, Sarah K ^g   Cuomo, Christina ^g   Perlin, Michael H ^h   Hood, Michael E ^a  

^a AMHERST COLLEGE   (United States)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^d UNIVERSIDADE NOVA DE LISBOA   (Portugal)

^e Centre de recherche de Versailles   (France)

^f CENTRE NATIONAL DE SÉQUENÇAGE   (France)

^g BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^h UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

Evolutionary strata; Gene conversion; Mating type chromosome; Recombination; Sex chromosome

Indexed keywords

COMPLEMENTARY DNA; FUNGAL DNA; FUNGAL PROTEIN; PHEROMONE RECEPTOR;

ALLELE; CHROMOSOME; DIVERGENCE; FUNGUS; MATING BEHAVIOR; PHYLOGENETICS; POLYMORPHISM; RECOMBINATION; TAXONOMY;

ALLELE; ARTICLE; BASIDIOMYCETES; DNA SEQUENCE; FUNGAL GENE; GENETIC LINKAGE; GENETIC POLYMORPHISM; GENETIC RECOMBINATION; GENETICS; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; SPECIES DIFFERENCE;

ALLELES; BASIDIOMYCOTA; DNA, COMPLEMENTARY; DNA, FUNGAL; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; GENES, MATING TYPE, FUNGAL; GENETIC LINKAGE; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMERASE CHAIN REACTION; POLYMORPHISM, GENETIC; RECEPTORS, PHEROMONE; RECOMBINATION, GENETIC; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY;

ANIMALIA; BASIDIOMYCOTA; FUNGI; MICROBOTRYUM;

EID: 84868107898     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2012.01703.x     Document Type: Article

References (48)

1. Abbate, J. L., and M. E. Hood. 2010. Dynamic linkage relationships to the mating-type locus in automictic fungi of the genus Microbotryum. J. Evol. Biol. 23:1800-1805.
2. Bakkeren, G., and J. W. Kronstad. 1994. Linkage of mating-type loci distinguishes bipolar from tetrapolar mating in basidiomycetous smut fungi. Proc. Natl. Acad. Sci. USA 91:7085-7089.
3. Bakkeren, G., J. Kämper, and J. Schirawski. 2008. Sex in smut fungi: structure, function and evolution of mating-type complexes. Fungal Genet. Biol. 45(Suppl. 1):S15-S21.
4. Bergero, R., and D. Charlesworth. 2009. The evolution of restricted recombination in sex chromosomes. Trends Ecol. Evol. 24:94-102.
5. Billiard, S., M. López-Villavicencio, B. Devier, M. E. Hood, C. Fairhead, and T. Giraud. 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.
6. Bölker, M., and R. Kahmann. 1993. Sexual pheromones and mating responses in fungi. Plant Cell 5:1461-1469.
7. Charlesworth, D., B. Charlesworth, and G. Marais. 2005. Steps in the evolution of heteromorphic sex chromosomes. Heredity 95:118-128.
8. Coelho, M. A., A. Rosa, N. Rodrigues, A. Fonseca, and P. Gonçalves. 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.
9. Coelho, M. A., J. P. Sampaio, and P. Gonçalves. 2010. A deviation from the bipolar-tetrapolar mating paradigm in an early diverged basidiomycete. PLoS Genet. 6:e1001052.
10. Day, A. W. 1979. Mating type and morphogenesis in Ustilago violacea. Bot. Gaz. 140:94-101.
11. Denchev, C. M. 2007. Microbotryum lagerheimii sp. nov. (Microbotryaceae). Mycol. Balc. 4:61-67.
12. Denchev, C. M., T. Giraud, and M. E. Hood. 2009. Three new species of anthericolous smut fungi on Caryophyllaceae. Mycol. Balc. 6:79-84.
13. Devier, B., G. Aguileta, M. E. Hood, and T. Giraud. 2009. Ancient trans-specific polymorphism at pheromone receptor genes in basidiomycetes. Genetics 181:209-223.
14. Ellison, C. E., J. E. Stajich, D. J. Jacobson, D. O. Natvig, A. Lapidus, B. Foster, A. Aerts, R. Riley, E. A. Lindquist, I. V. Grigoriev, et al. 2011. Massive changes in genome architecture accompany the transition to self-fertility in the filamentous fungus Neurospora tetrasperma. Genetics 189:55-69.
15. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-791.
16. Fraser, J. A., S. Diezmann, R. L. Subaran, A. Allen, K. B. Lengeler, F. S. Dietrich, and J. Heitman. 2004. Convergent evolution of chromosomal sex-determining regions in the animal and fungal kingdoms. PLoS Biol. 2:e384.
17. Le Gac, M., M. E. Hood, E. Fournier, and T. Giraud. 2007. Phylogenetic evidence of host-specific cryptic species in the anther smut fungus. Evolution 61:15-26.
18. Giraud, T., R. Yockteng, M. López-Villavicencio, G. Refrégier, and M. E. Hood. 2008. Mating system of the anther smut fungus Microbotryum violaceum: selfing under heterothallism. Eukaryot. Cell 7:765-775.
19. Hood, M. E. 2002. Dimorphic mating-type chromosomes in the fungus Microbotryum violaceum. Genetics 160:457-461.
20. Hood, M. E. 2005. Repetitive DNA in the automictic fungus Microbotryum violaceum. Genetica 124:1-10.
21. Hood, M. E., and J. Antonovics. 1998. Two-celled promycelia and mating-type segregation in Ustilago violacea (Microbotryum violaceum). Int. J. Plant Sci. 159:199-205.
22. Hood, M. E., and J. Antonovics. 2000. Intratetrad mating, heterozygosity, and the maintenance of deleterious alleles in Microbotryum violaceum (=Ustilago violacea). Heredity 8:231-241.
23. Hood, M. E., J. Antonovics, and B. Koskella. 2004. Shared forces of sex chromosome evolution in haploid-mating and diploid-mating organisms: Microbotryum violaceum and other model organisms. Genetics 168:141-146.
24. Ironside, J. E. 2010. No amicable divorce? Challenging the notion that sexual antagonism drives sex chromosome evolution. Bioessays 32:718-726.
25. James, T. Y., P. Srivilai, U. Kües, and R. Vilgalys. 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.
26. James, T. Y., M. Lee, and L. T. A. van Diepen. 2011. A single mating-type locus composed of homeodomain genes promotes nuclear migration and heterokaryosis in the white-rot fungus Phanerochaete chrysosporium. Eukaryotic Cell 10:249-261.
27. Kemler, M., M. Göker, F. Oberwinkler, and D. Begerow. 2006. Implications of molecular characters for the phylogeny of the Microbotryaceae (Basidiomycota: Urediniomycetes). BMC Evol. Biol. 6:35.
28. Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16:111-120.
29. Kniep, H. 1919. Untersuchungen uber den Antherenbrand (Ustilago violacea Pers.). Ein Beitrag zum sexualitatproblem. Z. Botanik 11:257-284.
30. Lahn, B. T., and D. C. Page. 1999. Four evolutionary strata on the human X chromosome. Science 286:964-967.
31. Lee, S., M. Ni, W. Li, C. Shertz, and J. Heitman. 2010. The evolution of sex: a perspective from the fungal kingdom. Microbiol. Mol. Biol. Rev. 74:298-340.
32. Lutz, M., M. Piatek, M. Kemler, A. Chlebicki, and F. Oberwinkler. 2008. Anther smuts of Caryophyllaceae: molecular analyses reveal further new species. Mycol. Res. 112:1280-1296.
33. Menkis, A., D. J. Jacobson, T. Gustafsson, and H. Johannesson. 2008. The mating-type chromosome in the filamentous ascomycete Neurospora tetrasperma represents a model for early evolution of sex chromosomes. PLoS Genet. 4:e1000030.
34. Menkis, A., C. A. Whittle, and H. Johannesson. 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. 10:234.
35. Metin, B., K. Findley, and J. Heitman. 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.
36. Raudaskoski, M., and E. Kothe. 2010. Basidiomycete mating type genes and pheromone signaling. Eukaryot. Cell 9:847-859.
37. Rice, W. R. 1987. The accumulation of sexually antagonistic genes as a selective agent promoting the evolution of reduced recombination between primitive sex-chromosomes. Evolution 41:911-914.
38. Saitou, N., and M. Nei. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
39. Sampaio, J. P., M. Ali, R. Bauer, and M. Weiß. 2003. Taxonomic studies in the Microbotryomycetidae: Leucosporidium golubevii sp. nov., Leucosporidiella gen. nov. and the new orders Leucosporidiales and Sporidiobolales. Mycol. Prog. 2:53-68.
40. Shi, J., S. E. Wolf, J. M. Burke, G. G. Presting, J. Ross-Ibarra, and R. K. Dawe. 2010. Widespread gene conversion in centromere cores. PLoS Biol. 8:e1000327.
41. Stanke, M., R. Steinkamp, S. Waack, and B. Morgenstern. 2004. AUGUSTUS: a web server for gene finding in eukaryotes. Nucleic Acids Res. 32:W309-W312.
42. Szostak, J. W., T. L. Orr-Weaver, R. J. Rothstein, and F. W. Stahl. 1983. The double-strand-break repair model for recombination. Cell 33:25-35.
43. Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739.
44. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
45. van Peer, A. F., S. Y. Park, P. G. Shin, K. Y. Jang, Y. B. Yoo, Y. J. Park, B. M. Lee, G. H. Sung, T. Y. James, and W. S. Kong. 2011. Comparative genomics of the mating-type loci of the mushroom Flammulina velutipes reveals widespread synteny and recent inversions. PLoS ONE 6:e22249.
46. Votintseva, A. A., and D. A. Filatov. 2009. Evolutionary strata in a small mating-type-specific region of the smut fungus Microbotryum violaceum. Genetics 182:1391-1396.
47. Yockteng, R., S. Marthey, H. Chiapello, A. Gendrault, M. E. Hood, F. Rodolphe, B. Devier, P. Wincker, C. Dossat, and T. Giraud. 2007. Expressed sequences tags of the anther smut fungus, Microbotryum violaceum, identify mating and pathogenicity genes. BMC Genomics 8:272.
48. Zakharov, I. A. 1986. Various characteristics of gene localization in eukaryotic chromosomes. Formulation of a problem and analysis of non-random localization of mating type loci in fungi. Genetika 22:2620-2624.