Variation of the meiotic recombination landscape and properties over a broad evolutionary distance in yeasts

PLoS Genetics

Volumn 13, Issue 8, 2017, Pages

  Brion, Christian ^a   Legrand, Sylvain ^b   Peter, Jackson ^a   Caradec, Claudia ^a   Pflieger, David ^a   Hou, Jing ^a   Friedrich, Anne ^a   Llorente, Bertrand ^b   Schacherer, Joseph ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALLELE; CHROMOSOME ARM; CLADISTICS; GENUS; LACHANCEA KLUYVERI; LANDSCAPE; MEIOTIC RECOMBINATION; MITOSIS; NONHUMAN; YEAST; BUDDING YEAST; CHROMOSOME; CLASSIFICATION; DNA SEQUENCE; FUNGAL GENOME; GENETICS; HOMOLOGOUS RECOMBINATION; MEIOSIS; METABOLISM; MOLECULAR EVOLUTION; PHYLOGENY; SACCHAROMYCES CEREVISIAE;

FUNGAL DNA; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; SACCHAROMYCES CEREVISIAE PROTEIN; VMA1 PROTEIN, S CEREVISIAE;

CHROMOSOMES, FUNGAL; DNA, FUNGAL; EVOLUTION, MOLECULAR; GENOME, FUNGAL; HOMOLOGOUS RECOMBINATION; MEIOSIS; MITOSIS; PHYLOGENY; PROTON-TRANSLOCATING ATPASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SACCHAROMYCETALES; SEQUENCE ANALYSIS, DNA;

EID: 85028804401     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1006917     Document Type: Article

References (57)

1. Petronczki M, Siomos MF, Nasmyth K, Un ménage à quatre: the molecular biology of chromosome segregation in meiosis. Cell. 2003;112: 423–440. 12600308
2. Haber JE, Evolution of models of homologous recombination. Recombination and meiosis. Springer Berlin Heidelberg; 2007. pp. 1–64.
3. Keeney S, Giroux CN, Kleckner N, Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell. 1997;88: 375–384. 9039264
4. Pan J, Sasaki M, Kniewel R, Murakami H, Blitzblau HG, Tischfield SE, et al. A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell. 2011;144: 719–731. doi: 10.1016/j.cell.2011.02.009 21376234
5. Zickler D, Kleckner N, Meiotic chromosomes: integrating structure and function. Annu Rev Genet. 1999;33: 603–754. doi: 10.1146/annurev.genet.33.1.603 10690419
6. Mancera E, Bourgon R, Brozzi A, Huber W, Steinmetz LM, High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature. 2008;454: 479–485. doi: 10.1038/nature07135 18615017
7. Gerton JL, DeRisi J, Shroff R, Lichten M, Brown PO, Petes TD, Global mapping of meiotic recombination hotspots and coldspots in the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 2000;97: 11383–11390. doi: 10.1073/pnas.97.21.11383 11027339
8. Lichten M, Goldman AS, Meiotic recombination hotspots. Annu Rev Genet. 1995;29: 423–444. doi: 10.1146/annurev.ge.29.120195.002231 8825482
9. Hultén MA, On the origin of crossover interference: A chromosome oscillatory movement (COM) model. Mol Cytogenet. 2011;4: 10. doi: 10.1186/1755-8166-4-10 21477316
10. Wang S, Zickler D, Kleckner N, Zhang L, Meiotic crossover patterns: obligatory crossover, interference and homeostasis in a single process. Cell Cycle Georget Tex. 2015;14: 305–314.
11. Zickler D, Kleckner N, A few of our favorite things: Pairing, the bouquet, crossover interference and evolution of meiosis. Semin Cell Dev Biol. 2016;54: 135–148. doi: 10.1016/j.semcdb.2016.02.024 26927691
12. Boulton A, Myers RS, Redfield RJ, The hotspot conversion paradox and the evolution of meiotic recombination. Proc Natl Acad Sci U S A. 1997;94: 8058–8063. 9223314
13. Berg IL, Neumann R, Lam K-WG, Sarbajna S, Odenthal-Hesse L, May CA, et al. PRDM9 variation strongly influences recombination hot-spot activity and meiotic instability in humans. Nat Genet. 2010;42: 859–863. doi: 10.1038/ng.658 20818382
14. Coop G, Wen X, Ober C, Pritchard JK, Przeworski M, High-resolution mapping of crossovers reveals extensive variation in fine-scale recombination patterns among humans. Science. 2008;319: 1395–1398. doi: 10.1126/science.1151851 18239090
15. Lam I, Keeney S, Nonparadoxical evolutionary stability of the recombination initiation landscape in yeast. Science. 2015;350: 932–937. doi: 10.1126/science.aad0814 26586758
16. Ptak SE, Hinds DA, Koehler K, Nickel B, Patil N, Ballinger DG, et al. Fine-scale recombination patterns differ between chimpanzees and humans. Nat Genet. 2005;37: 429–434. doi: 10.1038/ng1529 15723063
17. Tsai IJ, Burt A, Koufopanou V, Conservation of recombination hotspots in yeast. Proc Natl Acad Sci U S A. 2010;107: 7847–7852. doi: 10.1073/pnas.0908774107 20385822
18. Zanders SE, Eickbush MT, Yu JS, Kang J-W, Fowler KR, Smith GR, et al. Genome rearrangements and pervasive meiotic drive cause hybrid infertility in fission yeast. eLife. 2014;3.
19. Singhal S, Leffler EM, Sannareddy K, Turner I, Venn O, Hooper DM, et al. Stable recombination hotspots in birds. Science. 2015;350: 928–932. doi: 10.1126/science.aad0843 26586757
20. Dujon B, Yeasts illustrate the molecular mechanisms of eukaryotic genome evolution. Trends Genet. 2006;22: 375–387. doi: 10.1016/j.tig.2006.05.007 16730849
21. Kellis M, Birren BW, Lander ES, Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature. 2004;428: 617–624. doi: 10.1038/nature02424 15004568
22. Wolfe KH, Shields DC, Molecular evidence for an ancient duplication of the entire yeast genome. Nature. 1997;387: 708–713. doi: 10.1038/42711 9192896
23. Friedrich A, Jung P, Reisser C, Fischer G, Schacherer J, Population genomics reveals chromosome-scale heterogeneous evolution in a protoploid yeast. Mol Biol Evol. 2015;32: 184–192. doi: 10.1093/molbev/msu295 25349286
24. Martini E, Borde V, Legendre M, Audic S, Regnault B, Soubigou G, et al. Genome-wide analysis of heteroduplex DNA in mismatch repair-deficient yeast cells reveals novel properties of meiotic recombination pathways. PLoS Genet. 2011;7: e1002305. doi: 10.1371/journal.pgen.1002305 21980306
25. Anderson CM, Chen SY, Dimon MT, Oke A, DeRisi JL, Fung JC, ReCombine: a suite of programs for detection and analysis of meiotic recombination in whole-genome datasets. PloS One. 2011;6: e25509. doi: 10.1371/journal.pone.0025509 22046241
26. Sherman F, Roman H, Evidence for two types of allelic recombination in yeast. Genetics. 1963;48: 255–261. 13977170
27. Simchen G, Commitment to meiosis: what determines the mode of division in budding yeast?BioEssays News Rev Mol Cell Dev Biol. 2009;31: 169–177.
28. Tsuchiya D, Yang Y, Lacefield S, Positive Feedback of NDT80 Expression Ensures Irreversible Meiotic Commitment in Budding Yeast. PLOS Genet. 2014;10: e1004398. doi: 10.1371/journal.pgen.1004398 24901499
29. Brion C, Pflieger D, Souali-Crespo S, Friedrich A, Schacherer J, Differences in environmental stress response among yeasts is consistent with species-specific lifestyles. Mol Biol Cell. 2016;27: 1694–1705. doi: 10.1091/mbc.E15-12-0816 27009200
30. Hagman A, Säll T, Compagno C, Piskur J, Yeast “make-accumulate-consume” life strategy evolved as a multi-step process that predates the whole genome duplication. PLoS One. 2013;8(7):e68734. doi: 10.1371/journal.pone.0068734 23869229
31. Laureau R, Loeillet S, Salinas F, Bergström A, Legoix-Né P, Liti G, et al. Extensive recombination of a yeast diploid hybrid through meiotic reversion. PLoS Genet. 2016;12: e1005781. doi: 10.1371/journal.pgen.1005781 26828862
32. Gimble FS, Thorner J, Homing of a DNA endonuclease gene by meiotic gene conversion in Saccharomyces cerevisiae. Nature. 1992;357: 301–306. doi: 10.1038/357301a0 1534148
33. Okuda Y, Sasaki D, Nogami S, Kaneko Y, Ohya Y, Anraku Y, Occurrence, horizontal transfer and degeneration of VDE intein family in Saccharomycete yeasts. Yeast Chichester Engl. 2003;20: 563–573.
34. Clément-Ziza M, Marsellach FX, Codlin S, Papadakis MA, Reinhardt S, Rodríguez-López M, et al. Natural genetic variation impacts expression levels of coding, non-coding, and antisense transcripts in fission yeast. Mol Syst Biol. 2014;10.
35. Mercier R, Mézard C, Jenczewski E, Macaisne N, Grelon M, The molecular biology of meiosis in plants. Annu Rev Plant Biol. 2015;66: 297–327. doi: 10.1146/annurev-arplant-050213-035923 25494464
36. Foulongne-Oriol M, Dufourcq R, Spataro C, Devesse C, Broly A, Rodier A, et al. Comparative linkage mapping in the white button mushroom Agaricus bisporus provides foundation for breeding management. Curr Genet. 2011;57: 39–50. doi: 10.1007/s00294-010-0325-z 21046108
37. Lee J, Jurgenson JE, Leslie JF, Bowden RL, Alignment of genetic and physical maps of Gibberella zeae. Appl Environ Microbiol. 2008;74: 2349–2359. doi: 10.1128/AEM.01866-07 18263740
38. Morin E, Kohler A, Baker AR, Foulongne-Oriol M, Lombard V, Nagy LG, et al. Genome sequence of the button mushroom Agaricus bisporus reveals mechanisms governing adaptation to a humic-rich ecological niche. Proc Natl Acad Sci U S A. 2012;109: 17501–17506. doi: 10.1073/pnas.1206847109 23045686
39. Li W, Freudenberg J, Two-parameter characterization of chromosome-scale recombination rate. Genome Res. 2009;19: 2300–2307. doi: 10.1101/gr.092676.109 19752285
40. Hunter N, Chambers SR, Louis EJ, Borts RH, The mismatch repair system contributes to meiotic sterility in an interspecific yeast hybrid. EMBO J. 1996;15: 1726–1733. 8612597
41. Brion C, Pflieger D, Friedrich A, Schacherer J, Evolution of intraspecific transcriptomic landscapes in yeasts. Nucleic Acids Res. 2015;43: 4558–4568. doi: 10.1093/nar/gkv363 25897111
42. Idnurm A, Hood ME, Johannesson H, Giraud T, Contrasted patterns in mating-type chromosomes in fungi: hotspots versus coldspots of recombination. Fungal Biol Rev. 2015;29: 220–229. doi: 10.1016/j.fbr.2015.06.001 26688691
43. Menkis A, Jacobson DJ, Gustafsson T, Johannesson H, The mating-type chromosome in the filamentous ascomycete Neurospora tetrasperma represents a model for early evolution of sex chromosomes. PLoS Genet. 2008;4: e1000030. doi: 10.1371/journal.pgen.1000030 18369449
44. Charlesworth B, Charlesworth D, The degeneration of Y chromosomes. Philos Trans R Soc Lond B Biol Sci. 2000;355: 1563–1572. doi: 10.1098/rstb.2000.0717 11127901
45. Guacci V, Kaback DB, Distributive disjunction of authentic chromosomes in Saccharomyces cerevisiae. Genetics. 1991;127: 475–488. 2016050
46. Lynn A, Soucek R, Börner GV, ZMM proteins during meiosis: crossover artists at work. Chromosome Res Int J Mol Supramol Evol Asp Chromosome Biol. 2007;15: 591–605.
47. Vakirlis N, Sarilar V, Drillon G, Fleiss A, Agier N, Meyniel J-P, et al. Reconstruction of ancestral chromosome architecture and gene repertoire reveals principles of genome evolution in a model yeast genus. Genome Res. 2016;26: 918–932. doi: 10.1101/gr.204420.116 27247244
48. McPeek MS, Speed TP, Modeling interference in genetic recombination. Genetics. 1995;139: 1031–1044. 7713406
49. Zhao H, Speed TP, McPeek MS, Statistical analysis of crossover interference using the chi-square model. Genetics. 1995;139: 1045–1056. 7713407
50. Sasaki M, Tischfield SE, van Overbeek M, Keeney S, Meiotic recombination initiation in and around retrotransposable elements in Saccharomyces cerevisiae. PLoS Genet. 2013;9: e1003732. doi: 10.1371/journal.pgen.1003732 24009525
51. Robine N, Uematsu N, Amiot F, Gidrol X, Barillot E, Nicolas A, Borde V, Genome-wide redistribution of meiotic double-strand breaks in Saccharomyces cerevisiae. Mol Cell Biol. 2007;27(5):1868–80. doi: 10.1128/MCB.02063-06 17189430
52. Wu TC, Lichten M, Factors that affect the location and frequency of meiosis-induced double-strand breaks in Saccharomyces cerevisiae. Genetics. 1995;140(1):55–66. 7635308
53. Garcia V, Gray S, Allison RM, Cooper TJ, Neale MJ, Tel1(ATM)-mediated interference suppresses clustered meiotic double-strand-break formation. Nature. 2015;520: 114–118. doi: 10.1038/nature13993 25539084
54. Comeron JM, Ratnappan R, Bailin S, The many landscapes of recombination in Drosophila melanogaster. PLoS Genet. 2012;8(10):e1002905doi: 10.1371/journal.pgen.1002905 23071443
55. Sigwalt A, Caradec C, Brion C, Hou J, de Montigny J, Jung P, et al. Dissection of quantitative traits by bulk segregant mapping in a protoploid yeast species. FEMS Yeast Res. 2016; pii: fow056.
56. Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, et al. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. GigaScience. 2012;1: 18. doi: 10.1186/2047-217X-1-18 23587118
57. Delcher AL, Phillippy A, Carlton J, Salzberg SL, Fast algorithms for large-scale genome alignment and comparison. Nucleic Acids Res. 2002;30: 2478–2483. 12034836