Dramatically diverse Schizosaccharomyces pombe wtf meiotic drivers all display high gamete-killing efficiency


Autoři: María Angélica Bravo Núñez aff001;  Ibrahim M. Sabbarini aff001;  Michael T. Eickbush aff001;  Yue Liang aff001;  Jeffrey J. Lange aff001;  Aubrey M. Kent aff001;  Sarah E. Zanders aff001
Působiště autorů: Stowers Institute for Medical Research, Kansas City, Missouri, United States of America aff001;  Department of Molecular and Integrative Physiology, University of Kansas Medical Center, Kansas City, Kansas, United States of America aff002
Vyšlo v časopise: Dramatically diverse Schizosaccharomyces pombe wtf meiotic drivers all display high gamete-killing efficiency. PLoS Genet 16(2): e32767. doi:10.1371/journal.pgen.1008350
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008350

Souhrn

Meiotic drivers are selfish alleles that can force their transmission into more than 50% of the viable gametes made by heterozygotes. Meiotic drivers are known to cause infertility in a diverse range of eukaryotes and are predicted to affect the evolution of genome structure and meiosis. The wtf gene family of Schizosaccharomyces pombe includes both meiotic drivers and drive suppressors and thus offers a tractable model organism to study drive systems. Currently, only a handful of wtf genes have been functionally characterized and those genes only partially reflect the diversity of the wtf gene family. In this work, we functionally test 22 additional wtf genes for meiotic drive phenotypes. We identify eight new drivers that share between 30–90% amino acid identity with previously characterized drivers. Despite the vast divergence between these genes, they generally drive into >85% of gametes when heterozygous. We also identify three wtf genes that suppress other wtf drivers, including two that also act as autonomous drivers. Additionally, we find that wtf genes do not underlie a weak (64% allele transmission) meiotic driver on chromosome 1. Finally, we find that some Wtf proteins have expression or localization patterns that are distinct from the poison and antidote proteins encoded by drivers and suppressors, suggesting some wtf genes may have non-meiotic drive functions. Overall, this work expands our understanding of the wtf gene family and the burden selfish driver genes impose on S. pombe.

Klíčová slova:

Fungal spores – Genetic loci – Meiosis – Polymerase chain reaction – Schizosaccharomyces pombe – Suppressor genes – Toxins – Antidotes


Zdroje

1. Abbott S, Fairbanks DJ. Experiments on plant hybrids by Gregor Mendel. Genetics. 2016;204(2):407–22. doi: 10.1534/genetics.116.195198 27729492

2. Sandler L, Novitski E. Meiotic drive as an evolutionary force. The American Naturalist. 1957;91(857):105–10.

3. Zimmering S, Sandler L, Nicoletti B. Mechanisms of meiotic drive. Annu Rev Genet. 1970;4:409–36. doi: 10.1146/annurev.ge.04.120170.002205 4950062

4. Burt A, Trivers R. Genes in conflict: the biology of selfish genetic elements. Cambridge, Mass.: Belknap Press of Harvard University Press; 2006. viii, 602 p., 8 p. of plates p.

5. Lindholm AK, Dyer KA, Firman RC, Fishman L, Forstmeier W, Holman L, et al. The ecology and evolutionary dynamics of meiotic drive. Trends Ecol Evol. 2016;31(4):315–26. doi: 10.1016/j.tree.2016.02.001 26920473

6. Zanders SE, Unckless RL. Fertility costs of meiotic drivers. Current Biology. 2019;29(11):R512–R20. doi: 10.1016/j.cub.2019.03.046 31163165

7. Dyer KA, Charlesworth B, Jaenike J. Chromosome-wide linkage disequilibrium as a consequence of meiotic drive. Proc Natl Acad Sci U S A. 2007;104(5):1587–92. doi: 10.1073/pnas.0605578104 17242362

8. Crow JF. Why is Mendelian segregation so exact? Bioessays. 1991;13(6):305–12. doi: 10.1002/bies.950130609 1909864

9. Price TAR, Wedell N. Selfish genetic elements and sexual selection: their impact on male fertility. Genetica. 2007;132(3):295. doi: 10.1007/s10709-007-9173-2 17647082

10. Sutter A, Lindholm AK. Detrimental effects of an autosomal selfish genetic element on sperm competitiveness in house mice. Proceedings of the Royal Society B: Biological Sciences. 2015;282(1811).

11. Hartl DL. Modifier theory and meiotic drive. Theoretical Population Biology. 1975;7(2):168–74. doi: 10.1016/0040-5809(75)90012-x 1145501

12. McLaughlin RN Jr., Malik HS. Genetic conflicts: the usual suspects and beyond. J Exp Biol. 2017;220(Pt 1):6–17. doi: 10.1242/jeb.148148 28057823

13. Daugherty MD, Malik HS. Rules of engagement: molecular insights from host-virus arms races. Annu Rev Genet. 2012;46:677–700. doi: 10.1146/annurev-genet-110711-155522 23145935

14. Henikoff S, Ahmad K, Malik HS. The centromere paradox: stable inheritance with rapidly evolving DNA. Science. 2001;293(5532):1098–102. doi: 10.1126/science.1062939 11498581

15. Pardo-Manuel de Villena F, Sapienza C. Female meiosis drives karyotypic evolution in mammals. Genetics. 2001;159(3):1179–89. 11729161

16. Nuckolls NL, Bravo Núñez MA, Eickbush MT, Young JM, Lange JJ, Yu JS, et al. wtf genes are prolific dual poison-antidote meiotic drivers. eLIFE. 2017;6:e26033. doi: 10.7554/eLife.26033 28631612

17. Hu W, Jiang Z, Suo F, Zheng J, He W, Du L. A large gene family in fission yeast encodes spore killers that subvert Mendel’s law. eLIFE. 2017;6:e26057. doi: 10.7554/eLife.26057 28631610

18. Bravo Núñez MA, Lange JJ, Zanders SE. A suppressor of a wtf poison-antidote meiotic driver acts via mimicry of the driver’s antidote. PLOS Genetics. 2018;14(11):e1007836. doi: 10.1371/journal.pgen.1007836 30475921

19. Wood V, Gwilliam R, Rajandream MA, Lyne M, Lyne R, Stewart A, et al. The genome sequence of Schizosaccharomyces pombe. Nature. 2002;415(6874):871–80. doi: 10.1038/nature724 11859360

20. Lock A, Rutherford K, Harris MA, Hayles J, Oliver SG, Bahler J, et al. PomBase 2018: user-driven reimplementation of the fission yeast database provides rapid and intuitive access to diverse, interconnected information. Nucleic acids research. 2019;47(D1):D821–d7. doi: 10.1093/nar/gky961 30321395

21. Eickbush MT, Young JM, Zanders SE. Killer meiotic drive and dynamic evolution of the wtf gene family. Molecular Biology and Evolution. 2019;36(6):1201–14. doi: 10.1093/molbev/msz052 30991417

22. Kuang Z, Boeke JD, Canzar S. The dynamic landscape of fission yeast meiosis alternative-splice isoforms. Genome Res. 2016.

23. Jeffares DC, Rallis C, Rieux A, Speed D, Převorovský M, Mourier T, et al. The genomic and phenotypic diversity of Schizosaccharomyces pombe. Nature Genetics. 2015;47:235. doi: 10.1038/ng.3215 25665008

24. Tusso S, Nieuwenhuis BPS, Sedlazeck FJ, Davey JW, Jeffares DC, Wolf JBW. Ancestral admixture is the main determinant of global biodiversity in fission yeast. Molecular biology and evolution. 2019;36(9):1975–89. doi: 10.1093/molbev/msz126 31225876

25. Orr HA, Irving S. Segregation distortion in hybrids between the Bogota and USA subspecies of Drosophila pseudoobscura. Genetics. 2005;169(2):671–82. doi: 10.1534/genetics.104.033274 15654115

26. Kim D-U, Hayles J, Kim D, Wood V, Park H-O, Won M, et al. Analysis of a genome-wide set of gene deletions in the fission yeast Schizosaccharomyces pombe. Nature Biotechnology. 2010;28:617. doi: 10.1038/nbt.1628 20473289

27. Zanders SE, Eickbush MT, Yu JS, Kang JW, Fowler KR, Smith GR, et al. Genome rearrangements and pervasive meiotic drive cause hybrid infertility in fission yeast. eLIFE. 2014;3:e02630. doi: 10.7554/eLife.02630 24963140

28. Coyne JA, Orr HA. Speciation. Sunderland, Mass.: Sinauer Associates; 2004. xiii, 545, 2 p. of plates p.

29. Krapp A, Hamelin R, Armand F, Chiappe D, Krapp L, Cano E, et al. Analysis of the S. pombe meiotic proteome reveals a switch from anabolic to catabolic processes and extensive post-transcriptional regulation. Cell Reports. 2019;26(4):1044–58.e5. doi: 10.1016/j.celrep.2018.12.075 30673600

30. Zhang D, Vjestica A, Oliferenko S. The cortical ER network limits the permissive zone for actomyosin ring assembly. Current Biology. 2010;20(11):1029–34. 20434336

31. Matsuyama A, Arai R, Yashiroda Y, Shirai A, Kamata A, Sekido S, et al. ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe. Nat Biotechnol. 2006;24(7):841–7. doi: 10.1038/nbt1222 16823372

32. Suda Y, Nakanishi H, Mathieson EM, Neiman AM. Alternative modes of organellar segregation during sporulation in Saccharomyces cerevisiae. Eukaryotic Cell. 2007;6(11):2009–17. doi: 10.1128/EC.00238-07 17905927

33. Didion JP, Morgan AP, Clayshulte AM, McMullan RC, Yadgary L, Petkov PM, et al. A multi-megabase copy number gain causes maternal transmission ratio distortion on mouse chromosome 2. PLOS Genetics. 2015;11(2):e1004850. doi: 10.1371/journal.pgen.1004850 25679959

34. Long Y, Zhao L, Niu B, Su J, Wu H, Chen Y, et al. Hybrid male sterility in rice controlled by interaction between divergent alleles of two adjacent genes. Proc Natl Acad Sci U S A. 2008;105(48):18871–6. doi: 10.1073/pnas.0810108105 19033192

35. Hammond TM, Rehard DG, Xiao H, Shiu PK. Molecular dissection of Neurospora spore killer meiotic drive elements. Proc Natl Acad Sci U S A. 2012;109(30):12093–8. doi: 10.1073/pnas.1203267109 22753473

36. Grognet P, Lalucque H, Malagnac F, Silar P. Genes that bias Mendelian segregation. PLOS Genetics. 2014;10(5):e1004387. doi: 10.1371/journal.pgen.1004387 24830502

37. Vogan AA, Ament-Velásquez SL, Granger-Farbos A, Svedberg J, Bastiaans E, Debets AJM, et al. Combinations of Spok genes create multiple meiotic drivers in Podospora. eLIFE. 2019;8:e46454. doi: 10.7554/eLife.46454 31347500

38. Rhoades NA, Harvey AM, Samarajeewa DA, Svedberg J, Yusifov A, Abusharekh A, et al. Identification of rfk-1, a meiotic driver undergoing RNA editing in Neurospora. Genetics. 2019;212(1):93–110. doi: 10.1534/genetics.119.302122 30918007

39. Pieper KE, Unckless RL, Dyer KA. A fast-evolving X-linked duplicate of importin-α2 is overexpressed in sex-ratio drive in Drosophila neotestacea. Molecular Ecology. 2018;27(24):5165–79. doi: 10.1111/mec.14928 30411843

40. Xie Y, Tang J, Xie X, Li X, Huang J, Fei Y, et al. An asymmetric allelic interaction drives allele transmission bias in interspecific rice hybrids. Nature Communications. 2019;10(1):2501. doi: 10.1038/s41467-019-10488-3 31175302

41. Yu X, Zhao Z, Zheng X, Zhou J, Kong W, Wang P, et al. A selfish genetic element confers non-Mendelian inheritance in rice. Science. 2018;360(6393):1130–2. doi: 10.1126/science.aar4279 29880691

42. Yang J, Zhao X, Cheng K, Du H, Ouyang Y, Chen J, et al. A killer-protector system regulates both hybrid sterility and segregation distortion in rice. Science. 2012;337(6100):1336–40. doi: 10.1126/science.1223702 22984070

43. Bauer H, Schindler S, Charron Y, Willert J, Kusecek B, Herrmann BG. The nucleoside diphosphate kinase gene Nme3 acts as quantitative trait locus promoting non-Mendelian inheritance. PLOS Genetics. 2012;8(3):e1002567. doi: 10.1371/journal.pgen.1002567 22438820

44. Chen J, Ding J, Ouyang Y, Du H, Yang J, Cheng K, et al. A triallelic system of S5 is a major regulator of the reproductive barrier and compatibility of indica–japonica hybrids in rice. Proc Natl Acad Sci U S A. 2008;105(32):11436–41. doi: 10.1073/pnas.0804761105 18678896

45. Dalstra HJ, van der Zee R, Swart K, Hoekstra RF, Saupe SJ, Debets AJ. Non-mendelian inheritance of the HET-s prion or HET-s prion domains determines the het-S spore killing system in Podospora anserina. Fungal genetics and biology: FG & B. 2005;42(10):836–47.

46. Tao Y, Hartl DL, Laurie CC. Sex-ratio segregation distortion associated with reproductive isolation in Drosophila. Proc Natl Acad Sci U S A. 2001;98(23):13183–8. doi: 10.1073/pnas.231478798 11687638

47. Tao Y, Araripe L, Kingan SB, Ke Y, Xiao H, Hartl DL. A sex-ratio meiotic drive system in Drosophila simulans. II: An X-linked distorter. PLOS Biology. 2007;5(11):e293. doi: 10.1371/journal.pbio.0050293 17988173

48. Merçot H, Atlan A, Jacques M, Montchamp-Moreau C. Sex-ratio distortion in Drosophila simulans: co-occurence of a meiotic drive and a suppressor of drive. Journal of Evolutionary Biology. 1995;8(3):283–300.

49. Dermitzakis ET, Masly JP, Waldrip HM, Clark AG. Non-Mendelian segregation of sex chromosomes in heterospecific Drosophila males. Genetics. 2000;154(2):687–94. 10655222

50. Lin C-J, Hu F, Dubruille R, Vedanayagam J, Wen J, Smibert P, et al. The hpRNA/RNAi pathway is essential to resolve intragenomic conflict in the Drosophila male germline. Developmental Cell. 2018;46(3):316–26.e5. doi: 10.1016/j.devcel.2018.07.004 30086302

51. Rhoades MM. Preferential segregation in maize. Genetics. 1942;27(4):395–407. 17247049

52. Kato Yamakake TA. Cytological studies of maize [Zea mays L.] and teosinte [Zea mexicana Schrader Kuntze] in relation to their origin and evolution. Amherst, Mass.: Massachusetts Agricultural Experiment Station; 1976. ca. 200 p. p.

53. Dawe RK, Lowry EG, Gent JI, Stitzer MC, Swentowsky KW, Higgins DM, et al. A kinesin-14 motor activates neocentromeres to promote meiotic drive in maize. Cell. 2018;173(4):839–50.e18. doi: 10.1016/j.cell.2018.03.009 29628142

54. Akera T, Chmátal L, Trimm E, Yang K, Aonbangkhen C, Chenoweth DM, et al. Spindle asymmetry drives non-Mendelian chromosome segregation. Science. 2017;358(6363):668–72. doi: 10.1126/science.aan0092 29097549

55. Akera T, Trimm E, Lampson MA. Molecular strategies of meiotic cheating by selfish centromeres. Cell. 2019;178(5):1132–44.e10. doi: 10.1016/j.cell.2019.07.001 31402175

56. Farlow A, Long H, Arnoux S, Sung W, Doak TG, Nordborg M, et al. The spontaneous mutation rate in the fission yeast Schizosaccharomyces pombe. Genetics. 2015;201(2):737–44. doi: 10.1534/genetics.115.177329 26265703

57. Dalstra HJ, Swart K, Debets AJ, Saupe SJ, Hoekstra RF. Sexual transmission of the [Het-S] prion leads to meiotic drive in Podospora anserina. Proc Natl Acad Sci U S A. 2003;100(11):6616–21. doi: 10.1073/pnas.1030058100 12719532

58. Smith GR. Genetic analysis of meiotic recombination in Schizosaccharomyces pombe. Methods Mol Biol. 2009;557:65–76. doi: 10.1007/978-1-59745-527-5_6 19799177

59. Wach A, Brachat A, Pohlmann R, Philippsen P. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast. 1994;10(13):1793–808. doi: 10.1002/yea.320101310 7747518

60. Goldstein AL, McCusker JH. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast. 1999;15(14):1541–53. doi: 10.1002/(SICI)1097-0061(199910)15:14<1541::AID-YEA476>3.0.CO;2-K 10514571

61. Schiestl RH, Gietz RD. High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Current Genetics. 1989;16(5):339–46.

62. Gardner JM, Jaspersen SL. Manipulating the yeast genome: deletion, mutation, and tagging by PCR. In: Smith JS, Burke DJ, editors. Yeast Genetics: Methods and Protocols. New York, NY: Springer New York; 2014. p. 45–78.

63. Chen J, Smoyer CJ, Slaughter BD, Unruh JR, Jaspersen SL. The SUN protein Mps3 controls Ndc1 distribution and function on the nuclear membrane. The Journal of Cell Biology. 2014;204(4):523–39. doi: 10.1083/jcb.201307043 24515347

64. Jacobs JZ, Ciccaglione KM, Tournier V, Zaratiegui M. Implementation of the CRISPR-Cas9 system in fission yeast. Nature Communications. 2014;5:5344. doi: 10.1038/ncomms6344 25352017

65. Sheff MA, Thorn KS. Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae. Yeast. 2004;21(8):661–70. doi: 10.1002/yea.1130 15197731

Štítky
Genetika Reprodukční medicína

Článek vyšel v časopise

PLOS Genetics


2020 Číslo 2

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Kurzy Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

VIRTUÁLNÍ ČEKÁRNA ČR Jste praktický lékař nebo pediatr? Zapojte se! Jste praktik nebo pediatr? Zapojte se!

×