Recent and massive expansion of the mating-type-specific region in the smut fungus Microbotryum

Genetics

Volumn 199, Issue 3, 2015, Pages 809-816

  Whittle, Carrie A ^a   Votintseva, Antonina ^a   Ridout, Kate ^a,b   Filatov, Dmitry A ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Evolution; Fungi; Mating type; Microbotryum; Sex chromosome

Indexed keywords

CONTIG; PHEROMONE RECEPTOR; MATING HORMONE ALPHA FACTOR RECEPTOR;

AGE; ARTICLE; CHROMOSOME; COMPARATIVE STUDY; DNA POLYMORPHISM; DNA SEQUENCE; EVOLUTION; EXON; FUNGAL GENOME; FUNGAL STRAIN; GENE LOCUS; GENE SEQUENCE; GENETIC CROSS; MATING TYPE; MICROBOTRYUM; MICROBOTRYUM LYCHNIS DIOICAE; MOLECULAR CLOCK; NONHUMAN; PRIORITY JOURNAL; BASIDIOMYCETES; FUNGAL GENE; GENETIC RECOMBINATION; GENETICS; MOLECULAR EVOLUTION;

ANIMALIA; FUNGI; LYCHNIS; MICROBOTRYUM;

BASIDIOMYCOTA; CHROMOSOMES, FUNGAL; EVOLUTION, MOLECULAR; GENES, FUNGAL; RECEPTORS, MATING FACTOR; RECOMBINATION, GENETIC;

EID: 84924955665     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.114.171702     Document Type: Article

References (49)

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. Antonovics, J., and J. Y. Abrams, 2004 Intratetrad mating and the evolution of linkage relationships. Evolution 58: 702–709.
3. Bachtrog, D., 2004 Evidence that positive selection drives Ychromosome degeneration in Drosophila miranda. Nat. Genet. 36: 518–522.
4. Bachtrog, D., 2013 Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat. Rev. Genet. 14: 113–124.
5. Bakkeren, G., J. Kämper, and J. Schirawski, 2008 Sex in smut fungi: structure, function and evolution of mating-type complexes. Fungal Genet. Biol. 45: S15–S21.
6. Berbee, M. L., and J. W. Taylor, 2010 Dating the molecular clock in fungi: How close are we? Fungal Biol. Rev. 24: 1–16.
7. Bergero, R., and D. Charlesworth, 2009 The evolution of restricted recombination in sex chromosomes. Trends Ecol. Evol. 24: 94–102.
8. Bernasconi, G., J. Antonovics, A. Biere, D. Charlesworth, L. F. Delph et al., 2009 Silene as a model system in ecology and evolution. Heredity 103: 5–14.
9. Charlesworth, B., and D. Charlesworth, 2000 The degeneration of Y chromosomes. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355: 1563–1572.
10. Charlesworth, D., 2013 Plant sex chromosome evolution. J. Exp. Bot. 64: 405–420.
11. Charlesworth, D., and B. Charlesworth, 1980 Sex differences in fitness and selection for centric fusions between sex-chromosomes and autosomes. Genet. Res. 35: 205–214.
12. Charlesworth, D., and B. Charlesworth, 2005 Sex chromosomes: evolution of the weird and wonderful. Curr. Biol. 15: R129–R131.
13. Coelho, M. A., J. P. Sampaio, and P. Goncalves, 2010 A deviation from the bipolar-tetrapolar mating paradigm in an early diverged basidiomycete. PLoS Genet. 6: e1001052.
14. Danecek, P., A. Auton, G. Abecasis, C. A. Albers, E. Banks et al., 2011 The variant call format and VCF tools. Bioinformatics 27: 2156–2158.
15. Darling, A. E., B. Mau, and N. T. Perna, 2010 progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 5: e11147.
16. Day, A. W., and J. E. Cummings, 1981 The genetics and cellular biology of sexual development in Ustilago violacea, pp. 379–401 in Sexual Interactions in Eukaryotic Microbes, edited by D. H. O’Day, and P. A. Horgen. Academic Press, New York.
17. 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.
18. Ellison, C. E., J. E. Stajich, D. J. Jacobson, D. O. Natvig, A. Lapidus et al., 2011 Massive changes in genome architecture accompany the transition to self-fertility in the filamentous fungus Neurospora tetrasperma. Genetics 189: 55–69.
19. Ferris, P., B. Olson, P. L. De Hoff, S. Douglass, D. Casero et al., 2010 Evolution of an expanded sex-determining locus in Volvox. Science 328: 351–354.
20. Filatov, D. A., 2009 Processing and population genetic analysis of multigenic datasets with ProSeq3 software. Bioinformatics 25: 3189–3190.
21. Fraser, J. A., S. Diezmann, R. L. Subaran, A. Allen, K. B. Lengeler et al., 2004 Convergent evolution of chromosomal sex-determining regions in the animal and fungal kingdoms. PLoS Biol. 2: e384.
22. Giraud, T., R. Yockteng, M. Lopez-Villavicencio, G. Refregier, and M. E. Hood, 2008 Mating system of the anther smut fungusMicrobotryum violaceum: selfing under heterothallism. Eukaryot. Cell 7: 765–775.
23. Goubet, P. M., H. Bergès, A. Bellec, E. Prat, N. Helmstetter et al., 2012 Contrasted patterns of molecular evolution in dominant and recessive self-incompatibility haplotypes in Arabidopsis. PLoS Genet. 8:e1002495.
24. Guerrero, R. F., M. Kirkpatrick, and N. Perrin, 2012 Cryptic recombination in the ever-young sex chromosomes of Hylid frogs. J. Evol. Biol. 25: 1947–1954.
25. Handley, L. J., H. Ceplitis, and H. Ellegren, 2004 Evolutionary strata on the chicken Z chromosome: implications for sex chromosome evolution. Genetics 167: 367–376.
26. Hood, M. E., 2002 Dimorphic mating-type chromosomes in the fungus Microbotryum violaceum. Genetics 160: 457–461.
27. Hood, M. E., E. Petit, and T. Giraud, 2013 Extensive divergence between mating-type chromosomes of the anther-smut fungus. Genetics 193: 309–315.
28. Kahman, R., and J. Schirawski, 2007 Mating in the smut fungi: from a to b to the downstream cascades, pp. 377–387 in Sex in Fungi, edited by J. Heitman, J. Kronstad, J. Taylor, and L. Casselton. American Society of Microbiology, Washington, DC.
29. Kämper, J., R. Kahmann, M. Bölker, L. J. Ma, T. Brefort et al., 2006 Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444: 97–101.
30. Kasuga, T., T. J. White, and J. W. Taylor, 2002 Estimation of nucleotide substitution rates in Eurotiomycete fungi. Mol. Biol. Evol. 19: 2318–2324.
31. Lahn, B. T., and D. C. Page, 1999 Four evolutionary strata on the human X chromosome. Science 286: 964–967.
32. Laurie, J. D., R. Linning, P. Wong, and G. Bakkeren, 2013 Do TE activity and counteracting genome defenses, RNAi and methylation, shape the sex lives of smut fungi? Plant Signal. Behav. 4: e23853.
33. Lee, N., G. Bakkeren, K. Wong, J. E. Sherwood, and J. W. Kronstad, 1999 The mating-type and pathogenicity locus of the fungus Ustilago hordei spans a 500-kb region. Proc. Natl. Acad. Sci. USA 96: 15026.
34. Lengeler, K. B., D. S. Fox, J. A. Fraser, A. Allen, K. Forrester et al., 2002 Mating-type locus of Cryptococcus neoformans: a step in the evolution of sex chromosomes. Eukaryot. Cell 1: 704–718.
35. 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.
36. Merino, S. T., M. A. Nelson, D. J. Jacobson, and D. O. Natvig, 1996 Pseudohomothallism and evolution of the mating-type chromosome in Neurospora tetrasperma. Genetics 143: 789–799.
37. Nei, M., 1987 Molecular Evolutionary Genetics. Columbia University Press, New York.
38. Nicolas, M., G. Marais, V. Hykelova, B. Janousek, V. Laporte et al., 2005 A gradual process of recombination restriction in the evolutionary history of the sex chromosomes in dioecious plants. PLoS Biol. 3: e4.
39. Nieuwenhuis, B. P. S., S. Billiard, S. Vuilleumier, E. Petit, M. E. Hood et al., 2013 Evolution of uni- and bifactorial sexual compatibility systems in fungi. Heredity 11: 445–455.
40. Petit, E., T. Giraud, D. M. de Vienne, M. A. Coelho, G. Aguileta et al., 2013 Linkage to the mating-type locus across the genus Microbotryum: insights into nonrecombining chromosomes. Evolution 66: 3519–3533.
41. Presgraves, D. C., 2008 Sex chromosomes and speciation in Drosophila. Trends Genet. 24: 336–343.
42. Qiu, S., R. Bergero, and D. Charlesworth, 2013 Testing for the footprint of sexually antagonistic polymorphisms in the pseudoautosomal region of a plant sex chromosome pair. Genetics 194: 663–672.
43. Rice, W. R., 1984 Sex chromosomes and the evolution of sexual dimorphism. Evolution 28: 911–914.
44. 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.
45. Vicoso, B., V. B. Kaiser, and D. Bachtrog, 2013 Sex-biased gene expression at homomorphic sex chromosomes in emus and its implication for sex chromosome evolution. Proc. Natl. Acad. Sci. USA 110: 6453–6458.
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. Whittle, C. A., Y. Sun, and H. Johannesson, 2011a Degeneration in codon usage within the region of suppressed recombination in the mating-type chromosomes of Neurospora tetrasperma. Eukaryot. Cell 10: 594–603.
48. Whittle, C. A., K. Nygren, and H. Johannesson, 2011b Consequences of reproductive mode on genome evolution in fungi. Fungal Genet. Biol. 48: 661–667.
49. Zakharov, I. A., 2005 Intratetrad mating and its genetic and evolutionary consequences. Russ. J. Genet. 41: 402–411.