Genome rearrangements and pervasive meiotic drive cause hybrid infertility in fission yeast

eLife

Volumn 2014, Issue 3, 2014, Pages

  Zanders, Sarah E ^a   Eickbush, Michael T ^a   Yu, Jonathan S ^a,d   Kang, Ji Won ^a,c   Fowler, Kyle R ^a   Smith, Gerald R ^a   Malik, Harmit Singh ^a,b  

^a Fred Hutchinson Cancer Research Center   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLELE; ANEUPLOIDY; ARTICLE; CHROMOSOME REARRANGEMENT; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; DNA REPAIR; DNA SEQUENCE; DOUBLE STRANDED DNA BREAK; FUNGAL VIABILITY; FUNGUS SPORE; GAMETE; GENE CASSETTE; GENE REARRANGEMENT; GENETIC TRANSFORMATION; GENOME ANALYSIS; HYBRID; INFERTILITY; MEIOSIS; MITOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PULSED FIELD GEL ELECTROPHORESIS; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES KAMBUCHA; SCHIZOSACCHAROMYCES POMBE; SOUTHERN BLOTTING; SPECIES DIFFERENTIATION;

EID: 84903952164     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.02630.001     Document Type: Article

References (68)

1. Alani E, Padmore R, Kleckner N. 1990. Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell 61: 419-436. doi: 10.1016/0092-8674(90)90524-I.
2. Anderson JA, Gilliland WD, Langley CH. 2009. Molecular population genetics and evolution of Drosophila meiosis genes. Genetics 181: 177-185. doi: 10.1534/genetics.108.093807.
3. Angehrn P, Gutz H. 1968. Influence of the mating type on mitotic crossing-over in Schizosaccharomyces pombe. Genetics 60: 158.
4. Baudat F, Buard J, Grey C, Fledel-Alon A, Ober C, Przeworski M, Coop G, de Massy B. 2010. PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327: 836-840. doi: 10.1126/science.1183439.
5. Bayes JJ, Malik HS. 2009. Altered heterochromatin binding by a hybrid sterility protein in Drosophila sibling species. Science 326: 1538-1541. doi: 10.1126/science.1181756.
6. Bhattacharyya T, Gregorova S, Mihola O, Anger M, Sebestova J, Denny P, Simecek P, Forejt J. 2013. Mechanistic basis of infertility of mouse intersubspecific hybrids. Proceedings of the National Academy of Sciences of the United States of America 110: E468-E477. doi: 10.1073/pnas.1219126110.
7. Bomblies K, Lempe J, Epple P, Warthmann N, Lanz C, Dangl JL, Weigel D. 2007. Autoimmune response as a mechanism for a Dobzhansky-Muller-type incompatibility syndrome in plants. PLOS Biology 5: e236. doi: 10.1371/journal.pbio.0050236.
8. Boulton A, Myers RS, Redfield RJ. 1997. The hotspot conversion paradox and the evolution of meiotic recombination. Proceedings of the National Academy of Sciences of the United States of America 94: 8058-8063.
9. Brideau NJ, Flores HA, Wang J, Maheshwari S, Wang X, Barbash DA. 2006. Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science 314: 1292-1295. doi: 10.1126/science.1133953.
10. Brown WR, Liti G, Rosa C, James S, Roberts I, Robert V, Jolly N, Tang W, Baumann P, Green C, Schlegel K, Young J, Hirchaud F, Leek S, Thomas G, Blomberg A, Warringer J. 2011. A geographically diverse collection of Schizosaccharomyces pombe isolates shows limited phenotypic variation but extensive karyotypic diversity. G3 (Bethesda) 1: 615-626. doi: 10.1534/g3.111.001123.
11. Burt A, Trivers R. 2006. Genes in conflict: the biology of selfish genetic elements. Cambridge, Massachusetts: Belknap Press of Harvard University Press. p. viii, 602 p., 608 p. of plates.
12. Colson I, Delneri D, Oliver SG. 2004. Effects of reciprocal chromosomal translocations on the fitness of Saccharomyces cerevisiae. EMBO Reports 5: 392-398. doi: 10.1038/sj.embor.7400123.
13. Coyne JA, Orr HA. 2004. Speciation. Sunderland, Massachusetts: Sinauer Associates. p. xiii, 545, 542 p. of plates.
14. Cromie GA, Hyppa RW, Cam HP, Farah JA, Grewal SI, Smith GR. 2007. A discrete class of intergenic DNA dictates meiotic DNA break hotspots in fission yeast. PLOS Genetics 3: e141. doi: 10.1371/journal.pgen.0030141.
15. Crow JF. 1991. Why is Mendelian segregation so exact? BioEssays 13: 305-312. doi: 10.1002/bies.950130609.
16. Davis L, Smith GR. 2003. Nonrandom homolog segregation at meiosis I in Schizosaccharomyces pombe mutants lacking recombination. Genetics 163: 857-874.
17. Dawe RK, Cande WZ. 1996. Induction of centromeric activity in maize by suppressor of meiotic drive 1. Proceedings of the National Academy of Sciences of the United States of America 93: 8512-8517.
18. Delneri D, Colson I, Grammenoudi S, Roberts IN, Louis EJ, Oliver SG. 2003. Engineering evolution to study speciation in yeasts. Nature 422: 68-72. doi: 10.1038/nature01418.
19. Doll E, Molnar M, Cuanoud G, Octobre G, Latypov V, Ludin K, Kohli J. 2008. Cohesin and recombination proteins influence the G1-to-S transition in azygotic meiosis in Schizosaccharomyces pombe. Genetics 180: 727-740. doi: 10.1534/genetics.108.092619.
20. Dyer KA, Charlesworth B, Jaenike J. 2007. Chromosome-wide linkage disequilibrium as a consequence of meiotic drive. Proceedings of the National Academy of Sciences of the United States of America 104: 1587-1592. doi: 10.1073/pnas.0605578104.
21. Faria R, Navarro A. 2010. Chromosomal speciation revisited: rearranging theory with pieces of evidence. Trends in Ecology & Evolution 25: 660-669. doi: 10.1016/j.tree.2010.07.008.
22. Fischer G, James SA, Roberts IN, Oliver SG, Louis EJ. 2000. Chromosomal evolution in Saccharomyces. Nature 405: 451-454. doi: 10.1038/35013058.
23. Fishman L, Saunders A. 2008. Centromere-associated female meiotic drive entails male fitness costs in monkeyflowers. Science 322: 1559-1562. doi: 10.1126/science.1161406.
24. Fowler KR, Gutierrez-Velasco S, Martin-Castellanos C, Smith GR. 2013. Protein determinants of meiotic DNA break hot spots. Molecular Cell 49: 983-996. doi: 10.1016/j.molcel.2013.01.008.
25. Goldstein AL, McCusker JH. 1999. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15: 1541-1553. doi: 10.1002/(SICI)1097-0061(199910)15: 14<1541:: AID-YEA476>3.0.CO; 2-K.
26. Hammer MF, Schimenti J, Silver LM. 1989. Evolution of mouse chromosome 17 and the origin of inversions associated with t haplotypes. Proceedings of the National Academy of Sciences of the United States of America 86: 3261-3265.
27. Hammond TM, Rehard DG, Xiao H, Shiu PK. 2012. Molecular dissection of Neurospora Spore killer meiotic drive elements. Proceedings of the National Academy of Sciences of the United States of America 109: 12093-12098. doi: 10.1073/pnas.1203267109.
28. Hoffmann AA, Rieseberg LH. 2008. Revisiting the impact of inversions in evolution: from population genetic markers to drivers of adaptive shifts and speciation? Annual review of Ecology, Evolution, and Systematics 39: 21-42. doi: 10.1146/annurev.ecolsys.39.110707.173532.
29. Hunter N, Chambers SR, Louis EJ, Borts RH. 1996. The mismatch repair system contributes to meiotic sterility in an interspecific yeast hybrid. The EMBO Journal 15: 1726-1733.
30. Hyppa RW, Cromie GA, Smith GR. 2008. Indistinguishable landscapes of meiotic DNA breaks in rad50+ and rad50S strains of fission yeast revealed by a novel rad50+ recombination intermediate. PLOS Genetics 4: e1000267. doi: 10.1371/journal.pgen.1000267.
31. Hyppa RW, Smith GR. 2009. Using Schizosaccharomyces pombe meiosis to analyze DNA recombination intermediates. Methods in Molecular Biology 557: 235-252. doi: 10.1007/978-1-59745-527-5_15.
32. Irie S, Tsujimura A, Miyagawa Y, Ueda T, Matsuoka Y, Matsui Y, Okuyama A, Nishimune Y, Tanaka H. 2009. Single-nucleotide polymorphisms of the PRDM9 (MEISETZ) gene in patients with nonobstructive azoospermia. Journal of Andrology 30: 426-431. doi: 10.2164/jandrol.108.006262.
33. Johnson NA. 2010. Hybrid incompatibility genes: remnants of a genomic battlefield? Trends in Genetics 26: 317-325. doi: 10.1016/j.tig.2010.04.005.
34. Keeney S, Giroux CN, Kleckner N. 1997. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88: 375-384.
35. Kerr GW, Sarkar S, Arumugam P. 2012. How to halve ploidy: lessons from budding yeast meiosis. Cellular and Molecular Life Sciences 69: 3037-3051. doi: 10.1007/s00018-012-0974-9.
36. Kim DU, Hayles J, Kim D, Wood V, Park HO, Won M, Yoo HS, Duhig T, Nam M, Palmer G, Han S, Jeffery L, Baek ST, Lee H, Shim YS, Lee M, Kim L, Heo KS, Noh EJ, Lee AR, Jang YJ, Chung KS, Choi SJ, Park JY, Park Y, Kim HM, Park SK, Park HJ, Kang EJ, Kim HB, Kang HS, Park HM, Kim K, Song K, Song KB, Nurse P, Hoe KL. 2010. Analysis of a genome-wide set of gene deletions in the fission yeast Schizosaccharomyces pombe. Nature Biotechnology 28: 617-623. doi: 10.1038/nbt.1628.
37. Kohli J, Hottinger H, Munz P, Strauss A, Thuriaux P. 1977. Genetic mapping in SCHIZOSACCHAROMYCES POMBE by mitotic and meiotic analysis and induced Haploidization. Genetics 87: 471-489.
38. Larracuente AM, Presgraves DC. 2012. The selfish Segregation Distorter gene complex of Drosophila melanogaster. Genetics 192: 33-53. doi: 10.1534/genetics.112.141390.
39. Lee HY, Chou JY, Cheong L, Chang NH, Yang SY, Leu JY. 2008. Incompatibility of nuclear and mitochondrial genomes causes hybrid sterility between two yeast species. Cell 135: 1065-1073. doi: 10.1016/j.cell.2008.10.047.
40. Malone RE, Haring SJ, Foreman KE, Pansegrau ML, Smith SM, Houdek DR, Carpp L, Shah B, Lee KE. 2004. The signal from the initiation of meiotic recombination to the first division of meiosis. Eukaryotic Cell 3: 598-609. doi: 10.1128/EC.3.3.598-609.2004.
41. Masly JP, Jones CD, Noor MA, Locke J, Orr HA. 2006. Gene transposition as a cause of hybrid sterility in Drosophila. Science 313: 1448-1450. doi: 10.1126/science.1128721.
42. Mihola O, Trachtulec Z, Vlcek C, Schimenti JC, Forejt J. 2009. A mouse speciation gene encodes a meiotic histone H3 methyltransferase. Science 323: 373-375. doi: 10.1126/science.1163601.
43. Myers S, Bowden R, Tumian A, Bontrop RE, Freeman C, MacFie TS, McVean G, Donnelly P. 2010. Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science 327: 876-879. doi: 10.1126/science.1182363.
44. 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 Biology 11: e1001653. doi: 10.1371/journal.pbio.1001653.
45. Niwa O, Tange Y, Kurabayashi A. 2006. Growth arrest and chromosome instability in aneuploid yeast. Yeast 23: 937-950. doi: 10.1002/yea.1411.
46. Noor MA, Grams KL, Bertucci LA, Reiland J. 2001. Chromosomal inversions and the reproductive isolation of species. Proceedings of the National Academy of Sciences of the United States of America 98: 12084-12088. doi: 10.1073/pnas.221274498.
47. Otto SP, Whitton J. 2000. Polyploid incidence and evolution. Annual Review of Genetics 34: 401-437. doi: 10.1146/annurev.genet.34.1.401.
48. Pardo-Manuel de Villena F, Sapienza C. 2001. Female meiosis drives karyotypic evolution in mammals. Genetics 159: 1179-1189.
49. Pavelka N, Rancati G, Zhu J, Bradford WD, Saraf A, Florens L, Sanderson BW, Hattem GL, Li R. 2010. Aneuploidy confers quantitative proteome changes and phenotypic variation in budding yeast. Nature 468: 321-325. doi: 10.1038/nature09529.
50. Presgraves DC. 2010. The molecular evolutionary basis of species formation. Nature Reviews Genetics 11: 175-180. doi: 10.1038/nrg2718.
51. Rhind N, Chen Z, Yassour M, Thompson DA, Haas BJ, Habib N, Wapinski I, Roy S, Lin MF, Heiman DI, Young SK, Furuya K, Guo Y, Pidoux A, Chen HM, Robbertse B, Goldberg JM, Aoki K, Bayne EH, Berlin AM, Desjardins CA, Dobbs E, Dukaj L, Fan L, FitzGerald MG, French C, Gujja S, Hansen K, Keifenheim D, Levin JZ, Mosher RA, Müller CA, Pfiffner J, Priest M, Russ C, Smialowska A, Swoboda P, Sykes SM, Vaughn M, Vengrova S, Yoder R, Zeng Q, Allshire R, Baulcombe D, Birren BW, Brown W, Ekwall K, Kellis M, Leatherwood J, Levin H, Margalit H, Martienssen R, Nieduszynski CA, Spatafora JW, Friedman N, Dalgaard JZ, Baumann P, Niki H, Regev A, Nusbaum C. 2011. Comparative functional genomics of the fission yeasts. Science 332: 930-936. doi: 10.1126/science.1203357.
52. Rieseberg LH. 2001. Chromosomal rearrangements and speciation. Trends in Ecology & Evolution 16: 351-358.
53. Sandler L, Novitski E. 1957. Meiotic drive as an evolutionary force. The American Naturalist 41: 105-110. doi: 10.1086/281969.
54. Sawyer SL, Malik HS. 2006. Positive selection of yeast nonhomologous end-joining genes and a retrotransposon conflict hypothesis. Proceedings of the National Academy of Sciences of the United States of America 103: 17614-17619. doi: 10.1073/pnas.0605468103.
55. Schimenti J. 2000. Segregation distortion of mouse t haplotypes the molecular basis emerges. Trends in Genetics 16: 240-243. doi: 10.1016/S0168-9525(00)02020-5.
56. Segurel L, Leffler EM, Przeworski M. 2011. The case of the fickle fingers: how the PRDM9 zinc finger protein specifies meiotic recombination hotspots in humans. PLOS Biology 9: e1001211. doi: 10.1371/journal.pbio.1001211.
57. Singh G, Klar AJ. 2002. The 2.1-kb inverted repeat DNA sequences flank the mat2,3 silent region in two species of Schizosaccharomyces and are involved in epigenetic silencing in Schizosaccharomyces pombe. Genetics 162: 591-602.
58. Smith GR. 2009. Genetic analysis of meiotic recombination in Schizosaccharomyces pombe. Methods in Molecular Biology 557: 65-76. doi: 10.1007/978-1-59745-527-5_6.
59. Tange Y, Kurabayashi A, Goto B, Hoe KL, Kim DU, Park HO, Hayles J, Chikashige Y, Tsutumi C, Hiraoka Y, Yamao F, Nurse P, Niwa O. 2012. The CCR4-NOT complex is implicated in the viability of aneuploid yeasts. PLOS Genetics 8: e1002776. doi: 10.1371/journal.pgen.1002776.
60. Teresa Avelar A, Perfeito L, Gordo I, Godinho Ferreira M. 2013. Genome architecture is a selectable trait that can be maintained by antagonistic pleiotropy. Nature Communications 4: 2235. doi: 10.1038/ncomms3235.
61. Torres EM, Dephoure N, Panneerselvam A, Tucker CM, Whittaker CA, Gygi SP, Dunham MJ, Amon A. 2010. Identification of aneuploidy-tolerating mutations. Cell 143: 71-83. doi: 10.1016/j.cell.2010.08.038.
62. Torres EM, Sokolsky T, Tucker CM, Chan LY, Boselli M, Dunham MJ, Amon A. 2007. Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 317: 916-924. doi: 10.1126/science.1142210.
63. White MJD. 1978. Modes of speciation. A Series of books in biology. San Francisco: W. H. Freeman. p. 455.
64. Wolf K, Del Giudice L. 1980. Effect of ethidium bromide on transmission of mitochondrial genomes and DNA synthesis in the petite negative yeast Schizosaccharomyces pomhe. Current Genetics 1: 193-197. doi: 10.1007/BF00390943.
65. Yona AH, Manor YS, Herbst RH, Romano GH, Mitchell A, Kupiec M, Pilpel Y, Dahan O. 2012. Chromosomal duplication is a transient evolutionary solution to stress. Proceedings of the National Academy of Sciences of the United States of America 109: 21010-21015. doi: 10.1073/pnas.1211150109.
66. Young JA, Schreckhise RW, Steiner WW, Smith GR. 2002. Meiotic recombination remote from prominent DNA break sites in S. pombe. Molecular Cell 9: 253-263. doi: 10.1016/S1097-2765(02)00452-5.
67. Zerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Research 18: 821-829. doi: 10.1101/gr.074492.107.
68. Zimmering S, Sandler L, Nicoletti B. 1970. Mechanisms of meiotic drive. Annual Review of Genetics 4: 409-436. doi: 10.1146/annurev.ge.04.120170.002205.