Massive changes in genome architecture accompany the transition to self-fertility in the filamentous fungus Neurospora tetrasperma

Genetics

Volumn 189, Issue 1, 2011, Pages 55-69

  Ellison, Christopher E ^a   Stajich, Jason E ^b   Jacobson, David J ^a   Natvig, Donald O ^c   Lapidus, Alla ^d,e   Foster, Brian ^d   Aerts, Andrea ^d   Riley, Robert ^c   Lindquist, Erika A ^d   Grigoriev, Igor V ^d   Taylor, John W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF NEW MEXICO   (United States)

^d DOE JOINT GENOME INSTITUTE   (United States)

^e FOX CHASE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CONTROLLED STUDY; FERTILITY; FUNGAL GENE; FUNGAL GENETICS; FUNGUS; GENE REARRANGEMENT; GENE SEQUENCE; GENE STRUCTURE; GENETIC ANALYSIS; GENETIC RECOMBINATION; NEUROSPORA CRASSA; NEUROSPORA TETRASPERMA; NONHUMAN; PRIORITY JOURNAL; PSEUDOGENE; SELF FERTILITY; TRANSPOSON;

CHROMOSOMES, FUNGAL; CODON; FERTILITY; GENE REARRANGEMENT; GENES, MATING TYPE, FUNGAL; GENOME, FUNGAL; NEUROSPORA; RECOMBINATION, GENETIC;

ANIMALIA; FUNGI; NEUROSPORA TETRASPERMA;

EID: 80052661967     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.111.130690     Document Type: Article

References (99)

1. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman, 1990 Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
2. Argueso, J. L., J. Westmoreland, P. A. Mieczkowski, M. Gawel, T. D. Petes et al., 2008 Double-strand breaks associated with repetitive DNA can reshape the genome. Proc. Natl. Acad. Sci. USA 105: 11845-11850.
3. Ashburner, M., C. A. Ball, J. A. Blake, D. Botstein, H. Butler et al., 2000 Gene Ontology: tool for the unification of biology. Nat. Genet. 25: 25-29.
4. Bachtrog, D., 2003 Protein evolution and codon usage bias on the neo-sex chromosomes of Drosophila miranda. Genetics 165: 1221-1232.
5. Betancourt, A. J., and D. C. Presgraves, 2002 Linkage limits the power of natural selection in Drosophila. Proc. Natl. Acad. Sci. USA 99: 13616-13620.
6. Betancourt, A. J., J. J. Welch, and B. Charlesworth, 2009 Reduced effectiveness of selection caused by a lack of recombination. Curr. Biol. 19: 655-660.
7. Bierne, N., and A. Eyre-Walker, 2003 The problem of counting sites in the estimation of the synonymous and nonsynonymous substitution rates: implications for the correlation between the synonymous substitution rate and codon usage bias. Genetics 165: 1587-1597.
8. Birney, E., and R. Durbin, 2000 Using GeneWise in the Drosophila annotation experiment. Genome Res. 10: 547-548.
9. Boeckmann, B., A. Bairoch, R. Apweiler, M. C. Blatter, A. Estreicher et al., 2003 The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucleic Acids Res. 31: 365-370.
10. Bull, J. J., 1978 Sex chromosomes in haploid dioecy: unique contrast to Muller's theory for diploid dioecy. Am. Nat. 112: 245-250.
11. Casals, F., and A. Navarro, 2007 Inversions: The chicken or the egg? Heredity 99: 479-480.
12. Catcheside, D. G., 1975 Occurrence in wild strains of Neurospora crassa of genes controlling genetic recombination. Aust. J. Biol. Sci. 28: 213-225.
13. Charlesworth, B., and D. Charlesworth, 2000 The degeneration of Y chromosomes. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355: 1563-1572.
14. Charlesworth, D., B. Charlesworth, and G. Marais, 2005 Steps in the evolution of heteromorphic sex chromosomes. Heredity 95: 118-128.
15. Chen, J. M., N. Chuzhanova, P. D. Stenson, C. Ferec, and D. N. Cooper, 2005 Complex gene rearrangements caused by serial replication slippage. Hum. Mutat. 26: 125-134.
16. Connallon, T., and A. G. Clark, 2010 Gene duplication, gene conversion and the evolution of the Y chromosome. Genetics 186: 277-286.
17. Coppin, E., R. Debuchy, S. Arnaise, and M. Picard, 1997 Mating types and sexual development in filamentous ascomycetes. Microbiol. Mol. Biol. Rev. 61: 411-428.
18. Dewey, C. N., 2007 Aligning multiple whole genomes with Mercator and MAVID. Methods Mol. Biol. 395: 221-236.
19. Ellison, C. E., C. Hall, D. Kowbel, J. Welch, R. B. Brem et al., 2011 Population genomics and local adaptation in wild isolates of a model microbial eukaryote. Proc. Natl. Acad. Sci. USA 108: 2831-2836.
20. Enright, A. J., S. Van Dongen, and C. A. Ouzounis, 2002 An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res. 30: 1575-1584.
21. Fraser, J. A., and J. Heitman, 2004 Evolution of fungal sex chromosomes. Mol. Microbiol. 51: 299-306.
22. Fraser, J. A., and J. Heitman, 2005 Chromosomal sex-determining regions in animals, plants and fungi. Curr. Opin. Genet. Dev. 15: 645-651.
23. 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: 2243-2255.
24. Fraser, J. A., Y.-P. Hsueh, K. M. Findley, and J. Heitman, 2007 Evolution of the mating-type locus: the basidiomycetes, pp. 19-34 in Sex in Fungi: Molecular Determination and Evolutionary Implications-Print, edited by Heitman, J., J. W. Kronstad, J. W. Taylor, and L. A. Casselton. ASM Press, Washington, DC.
25. Galagan, J. E., and E. U. Selker, 2004 RIP: the evolutionary cost of genome defense. Trends Genet. 20: 417-423.
26. Gallegos, A., D. J. Jacobson, N. B. Raju, M. P. Skupski, and D. O. Natvig, 2000 Suppressed recombination and a pairing anomaly on the mating-type chromosome of Neurospora tetrasperma. Genetics 154: 623-633.
27. Gasteiger, E., A. Gattiker, C. Hoogland, I. Ivanyi, R. D. Appel et al., 2003 ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 31: 3784-3788.
28. Giraud, T., O. Jonot, and J. A. Shykoff, 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.
29. Haddrill, P. R., D. L. Halligan, D. Tomaras, and B. Charlesworth, 2007 Reduced efficacy of selection in regions of the Drosophila genome that lack crossing over. Genome Biol. 8: R18.
30. Hastings, P. J., G. Ira, and J. R. Lupski, 2009 A microhomologymediated break-induced replication model for the origin of human copy number variation. PLoS Genet. 5: e1000327.
31. Hood, M. E., 2002 Dimorphic mating-type chromosomes in the fungus Microbotryum violaceum. Genetics 160: 457-461.
32. Howe, H. B., and P. Haysman, 1966 Linkage group establishment in Neurospora tetrasperma by interspecific hybridization with N. crassa. Genetics 54: 293-302.
33. Hunter, N., S. R. Chambers, E. J. Louis, and R. H. Borts, 1996 The mismatch repair system contributes to meiotic sterility in an interspecific yeast hybrid. EMBO J. 15: 1726-1733.
34. Idnurm, A., F. J. Walton, A. Floyd, and J. Heitman, 2008 Identification of the sex genes in an early diverged fungus. Nature 451: 193-196.
35. Isono, K., J. D. McIninch, and M. Borodovsky, 1994 Characteristic features of the nucleotide sequences of yeast mitochondrial ribosomal protein genes as analyzed by computer program Gene-Mark. DNA Res. 1: 263-269.
36. Jacobson, D. J., 1995 Sexual dysfunction associated with outcrossing in Neurospora tetrasperma, a pseudohomothallic Ascomycete. Mycologia 87: 604-617.
37. Jacobson, D. J., 2005 Blocked recombination along the matingtype chromosomes of Neurospora tetrasperma involves both structural heterozygosity and autosomal genes. Genetics 171: 839-843.
38. Jurka, J., 2000 Repbase update: a database and an electronic journal of repetitive elements. Trends Genet. 16: 418-420.
39. Kanehisa, M., M. Araki, S. Goto, M. Hattori, M. Hirakawa et al., 2008 KEGG for linking genomes to life and the environment. Nucleic Acids Res. 36: D480-D484.
40. Kapitonov, V. V., and J. Jurka, 2003 Mariner-3_AN, a family of DNA transposons in the Aspergillus nidulans genome. Repbase Rep. 3: 196.
41. Kent, W. J., 2002 BLAT-the BLAST-like alignment tool. Genome Res. 12: 656-664.
42. Kliman, R. M., and J. Hey, 1993 Reduced natural selection associated with low recombination in Drosophila melanogaster. Mol. Biol. Evol. 10: 1239-1258.
43. Kondo, M., U. Hornung, I. Nanda, S. Imai, T. Sasaki et al., 2006 Genomic organization of the sex-determining and adjacent regions of the sex chromosomes of medaka. Genome Res. 16: 815-826.
44. Koonin, E. V., N. D. Fedorova, J. D. Jackson, A. R. Jacobs, D. M. Krylov et al., 2004 A comprehensive evolutionary classification of proteins encoded in complete eukaryotic genomes. Genome Biol. 5: R7.
45. Kurtz, S., A. Phillippy, A. L. Delcher, M. Smoot, M. Shumway et al., 2004 Versatile and open software for comparing large genomes. Genome Biol. 5: R12.
46. Lafontaine, I., and B. Dujon, 2010 Origin and fate of pseudogenes in Hemiascomycetes: a comparative analysis. BMC Genomics 11: 260.
47. Lahn, B. T., and D. C. Page, 1999 Four evolutionary strata on the human X chromosome. Science 286: 964-967.
48. Lee, J. A., C. M. Carvalho, and J. R. Lupski, 2007 A DNA replication mechanism for generating nonrecurrent rearrangements associated with genomic disorders. Cell 131: 1235-1247.
49. 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: 15026-15031.
50. 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.
51. Lewis, Z. A., S. Honda, T. K. Khlafallah, J. K. Jeffress, M. Freitag et al., 2009 Relics of repeat-induced point mutation direct heterochromatin formation in Neurospora crassa. Genome Res. 19: 427-437.
52. Liu, Z., P. H. Moore, H. Ma, C. M. Ackerman, M. Ragiba et al., 2004 A primitive Y chromosome in papaya marks incipient sex chromosome evolution. Nature 427: 348-352.
53. Lowe, T. M., and S. R. Eddy, 1997 TRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25: 955-964.
54. Maloisel, L., and J. L. Rossignol, 1998 Suppression of crossing-over by DNA methylation in Ascobolus. Genes Dev. 12: 1381-1389.
55. Mani, R. S., and A. M. Chinnaiyan, 2010 Triggers for genomic rearrangements: insights into genomic, cellular and environmental influences. Nat. Rev. Genet. 11: 819-829.
56. Mank, J. E., and H. Ellegren, 2007 Parallel divergence and degradation of the avian W sex chromosome. Trends Ecol. Evol. 22: 389-391.
57. Marais, G. A., M. Nicolas, R. Bergero, P. Chambrier, E. Kejnovsky et al., 2008 Evidence for degeneration of the Y chromosome in the dioecious plant Silene latifolia. Curr. Biol. 18: 545-549.
58. Marcou, D., A. Masson, J. M. Simonet, and G. Piquepaille, 1979 Evidence for non-random spatial distribution of meiotic exchanges in Podospora anserina: comparison between linkage groups 1 and 6. Mol. Gen. Genet. 176: 67-79.
59. McClintock, B., 1984 The significance of responses of the genome to challenge. Science 226: 792-801.
60. Melen, K., A. Krogh, and G. von Heijne, 2003 Reliability measures for membrane protein topology prediction algorithms. J. Mol. Biol. 327: 735-744.
61. 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.
62. Menkis, A., E. Bastiaans, D. J. Jacobson, and H. Johannesson, 2009 Phylogenetic and biological species diversity within the Neurospora tetrasperma complex. J. Evol. Biol. 22: 1923-1936.
63. 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.
64. 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.
65. 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.
66. 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.
67. Nielsen, H., J. Engelbrecht, S. Brunak, and G. Von Heijne, 1997 Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10: 1-6.
68. Nygren, K., R. Strandberg, A. Wallberg, B. Nabholz, T. Gustafsson et al., 2011 A comprehensive phylogeny of Neurospora reveals a link between reproductive mode and molecular evolution in fungi. Mol. Phylogenet. Evol. 59: 649-663.
69. O'Meally, D., H. R. Patel, R. Stiglec, S. D. Sarre, A. Georges et al., 2010 Non-homologous sex chromosomes of birds and snakes share repetitive sequences. Chromosome Res. 18: 787-800.
70. Pearson, W. R., T. Wood, Z. Zhang, and W. Miller, 1997 Comparison of DNA sequences with protein sequences. Genomics 46: 24-36.
71. Peichel, C. L., J. A. Ross, C. K. Matson, M. Dickson, J. Grimwood et al., 2004 The master sex-determination locus in threespine sticklebacks is on a nascent Y chromosome. Curr. Biol. 14: 1416-1424.
72. Powell, A. J., D. J. Jacobson, and D. O. Natvig, 2001 Allelic diversity at the het-c locus in Neurospora tetrasperma confirms outcrossing in nature and reveals an evolutionary dilemma for pseudohomothallic ascomycetes. J. Mol. Evol. 52: 94-102.
73. Presgraves, D. C., 2005 Recombination enhances protein adaptation in Drosophila melanogaster. Curr. Biol. 15: 1651-1656.
74. Raju, N. B., 1992 Functional heterothallism resulting from homokaryotic conidia and ascospores in Neurospora tetrasperma. Mycol. Res. 96: 103-116.
75. Raju, N. B., and D. D. Perkins, 1994 Diverse programs of ascus development in pseudohomothallic species of Neurospora, Gelasinospora, and Podospora. Dev. Genet. 15: 104-118.
76. Ranz, J. M., D. Maurin, Y. S. Chan, M. von Grotthuss, L. W. Hillier et al., 2007 Principles of genome evolution in the Drosophila melanogaster species group. PLoS Biol. 5: 1366-1381.
77. Rice, P., I. Longden, and A. Bleasby, 2000 EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 16: 276-277.
78. Rozen, S., H. Skaletsky, J. D. Marszalek, P. J. Minx, H. S. Cordum et al., 2003 Abundant gene conversion between arms of palindromes in human and ape Y chromosomes. Nature 423: 873-876.
79. Saenz, G. S., J. G. Stam, D. J. Jacobson, and D. O. Natvig, 2001 Heteroallelism at the het-c locus contributes to sexual dysfunction in outcrossed strains of Neurospora tetrasperma. Fungal Genet. Biol. 34: 123-129.
80. Salamov, A. A., and V. V. Solovyev, 2000 Ab initio gene finding in Drosophila genomic DNA. Genome Res. 10: 516-522.
81. Sharp, P. M., and W. H. Li, 1987 The Codon Adaptation Index- a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res. 15: 1281-1295.
82. Slater, G. S., and E. Birney, 2005 Automated generation of heuristics for biological sequence comparison. BMC Bioinform. 6: 31.
83. Smit, A., and R. Hubley, 2008-2010 Repeat Modeler Open-1.0. (http://www.repeatmasker.org).
84. Smit, A., R. Hubley, and P. Green, 1996-2010 Repeat Masker Open-3.0. (http://www.repeatmasker.org).
85. Swarbreck, S. M., E. A. Lindquist, D. D. Ackerly, and G. L. Andersen, 2011 Analysis of leaf and root transcriptomes of soil-grown Avena barbata plants. Plant Cell Physiol. 52: 317-332.
86. Veyrunes, F., P. D. Waters, P. Miethke, W. Rens, D. McMillan et al., 2008 Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes. Genome Res. 18: 965-973.
87. Vogel, H. J., 1956 A convenient growth medium for Neurospora (Medium N). Microb. Genet. Bull. 13: 42-43.
88. 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.
89. Votintseva, A. A., and D. A. Filatov, 2011 DNA polymorphism in recombining and non-recombining mating-type-specific loci of the smut fungus Microbotryum. Heredity 106: 936-944.
90. Whittle, C. A., and H. Johannesson, 2011 Evidence of the accumulation of allele-specific non-synonymous substitutions in the young region of recombination suppression within the matingtype chromosomes of Neurospora tetrasperma. Heredity (in press).
91. Whittle, C. A., K. Nygren, and H. Johannesson, 2011a Consequences of reproductive mode on genome evolution in fungi. Fungal Genet. Biol. 48: 661-667.
92. Whittle, C. A., Y. Sun, and H. Johannesson, 2011b Degeneration in codon usage within the region of suppressed recombination in the mating type chromosomes of Neurospora tetrasperma. Eukaryot. Cell 10: 594-603.
93. Whittle, C. A., Y. Sun, and H. Johannesson, 2011c Evolution of synonymous codon usage in Neurospora tetrasperma and Neurospora discreta. Genome Biol. Evol. (in press).
94. Yamato, K. T., K. Ishizaki, M. Fujisawa, S. Okada, S. Nakayama et al., 2007 Gene organization of the liverwort Y chromosome reveals distinct sex chromosome evolution in a haploid system. Proc. Natl. Acad. Sci. USA 104: 6472-6477.
95. Zdobnov, E. M., and R. Apweiler, 2001 InterProScan-an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17: 847-848.
96. Zhang, Z., J. Li, X. Q. Zhao, J. Wang, G. K. Wong et al., 2006 KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. Genomics Proteomics Bioinform. 4: 259-263.
97. Zheng, D., A. Frankish, R. Baertsch, P. Kapranov, A. Reymond et al., 2007 Pseudogenes in the ENCODE regions: consensus annotation, analysis of transcription, and evolution. Genome Res. 17: 839-851.
98. Zhou, Q., J. Wang, L. Huang, W. Nie, Y. Liu et al., 2008 Neo-sex chromosomes in the black muntjac recapitulate incipient evolution of mammalian sex chromosomes. Genome Biol. 9: R98.
99. Zou, C., M. D. Lehti-Shiu, F. Thibaud-Nissen, T. Prakash, C. R. Buell et al., 2009 Evolutionary and expression signatures of pseudogenes in Arabidopsis and rice. Plant Physiol. 151: 3-15.