Point Mutations in Centromeric Histone Induce Post-zygotic Incompatibility and Uniparental Inheritance

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The centromeric histone protein, CENH3, plays an important role in chromosome segregation during mitosis and meiosis. Here we show that single amino acid changes in CENH3, while producing no obvious effect on mitosis or meiosis, affect segregation postzygotically upon outcrossing to plants carrying wild-type centromeres. This results in uniparental inheritance among some progeny, and seed death in a larger fraction of progeny. Interestingly, changes competent to induce haploid in Arabidopsis existed in a TILLING population and in unrelated plant species. Our findings have two major consequences. First, uniparental inheritance facilitates the production of haploid plants that can easily be doubled to produce completely homozygous lines in a single generation. Secondly, our findings suggest that natural variation in CENH3 may result in partial reproductive isolation, because chromosomes of the mutant parent from F1 hybrid progeny are culled during embryonic development, while no reproductive defects are observed in self-pollinated plants. We do not know if the same mutations are haploid-inducing in other species, but uniparental chromosome loss, and the seed abortion that accompanies it results in an outcrossing-specific penalty that could potentially be involved in reproductive isolation.

Vyšlo v časopise: Point Mutations in Centromeric Histone Induce Post-zygotic Incompatibility and Uniparental Inheritance. PLoS Genet 11(9): e32767. doi:10.1371/journal.pgen.1005494
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005494

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Zdroje

1. Steiner FA, Henikoff S. Diversity in the organization of centromeric chromatin. Current Opinion in Genetics & Development. 2015;31(0):28–35. doi: http://dx.doi.org/10.1016/j.gde.2015.03.010.

2. Fukagawa T, Earnshaw William C. The Centromere: Chromatin Foundation for the Kinetochore Machinery. Developmental Cell. 30(5):496–508. doi: 10.1016/j.devcel.2014.08.016 25203206

3. Cheeseman IM. The Kinetochore. Cold Spring Harbor Perspectives in Biology. 2014;6(7). doi: 10.1101/cshperspect.a015826

4. Duro E, Marston AL. From equator to pole: splitting chromosomes in mitosis and meiosis. Genes & Development. 2015;29(2):109–22. doi: 10.1101/gad.255554.114

5. Allshire RC, Karpen GH. Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nat Rev Genet. 2008;9(12):923–37. doi: 10.1038/nrg2466 19002142

6. Sekulic N, Black BE. Molecular underpinnings of centromere identity and maintenance. Trends in Biochemical Sciences. 37(6):220–9. doi: 10.1016/j.tibs.2012.01.003 22410197

7. Palmer DK, O'Day K, Trong HL, Charbonneau H, Margolis RL. Purification of the centromere-specific protein CENP-A and demonstration that it is a distinctive histone. Proceedings of the National Academy of Sciences. 1991;88(9):3734–8. doi: 10.1073/pnas.88.9.3734

8. Earnshaw W, Migeon B. Three related centromere proteins are absent from the inactive centromere of a stable isodicentric chromosome. Chromosoma. 1985;92(4):290–6. doi: 10.1007/BF00329812 2994966

9. Talbert PB, Masuelli R, Tyagi AP, Comai L, Henikoff S. Centromeric Localization and Adaptive Evolution of an Arabidopsis Histone H3 Variant. The Plant Cell Online. 2002;14(5):1053–66. doi: 10.1105/tpc.010425

10. Dalal Y, Furuyama T, Vermaak D, Henikoff S. Structure, dynamics, and evolution of centromeric nucleosomes. Proceedings of the National Academy of Sciences. 2007;104(41):15974–81. doi: 10.1073/pnas.0707648104

11. Maheshwari S, Tan EH, West A, Franklin FCH, Comai L, Chan SWL. Naturally Occurring Differences in CENH3 Affect Chromosome Segregation in Zygotic Mitosis of Hybrids. Plos Genet. 2015;11(1):e1004970. doi: 10.1371/journal.pgen.1004970 25622028

12. Malik HS, Henikoff S. Phylogenomics of the nucleosome. Nat Struct Mol Biol. 2003;10(11):882–91.

13. Stoler S, Keith KC, Curnick KE, Fitzgerald-Hayes M. A mutation in CSE4, an essential gene encoding a novel chromatin-associated protein in yeast, causes chromosome nondisjunction and cell cycle arrest at mitosis. Genes & Development. 1995;9(5):573–86. doi: 10.1101/gad.9.5.573

14. Buchwitz BJ, Ahmad K, Moore LL, Roth MB, Henikoff S. Cell division: A histone-H3-like protein in C. elegans. Nature. 1999;401(6753):547–8. 10524621

15. Howman EV, Fowler KJ, Newson AJ, Redward S, MacDonald AC, Kalitsis P, et al. Early disruption of centromeric chromatin organization in centromere protein A (Cenpa) null mice. Proceedings of the National Academy of Sciences. 2000;97(3):1148–53. doi: 10.1073/pnas.97.3.1148

16. Ravi M, Kwong PN, Menorca RMG, Valencia JT, Ramahi JS, Stewart JL, et al. The Rapidly Evolving Centromere-Specific Histone Has Stringent Functional Requirements in Arabidopsis thaliana. Genetics. 2010;186(2):461–71. doi: 10.1534/genetics.110.120337 20628040

17. Dunleavy EM, Roche D, Tagami H, Lacoste N, Ray-Gallet D, Nakamura Y, et al. HJURP Is a Cell-Cycle-Dependent Maintenance and Deposition Factor of CENP-A at Centromeres. Cell. 2009;137(3):485–97. doi: http://dx.doi.org/10.1016/j.cell.2009.02.040. doi: 10.1016/j.cell.2009.02.040 19410545

18. Mishra PK, Au W-C, Choy JS, Kuich PH, Baker RE, Foltz DR, et al. Misregulation of Scm3p/HJURP Causes Chromosome Instability in Saccharomyces cerevisiae and Human Cells. Plos Genet. 2011;7(9):e1002303. doi: 10.1371/journal.pgen.1002303 PMC3183075. 21980305

19. Lermontova I, Kuhlmann M, Friedel S, Rutten T, Heckmann S, Sandmann M, et al. Arabidopsis KINETOCHORE NULL2 is an upstream component for centromeric histone H3 variant cenH3 deposition at centromeres. The Plant Cell. 2013;25(9):3389–404. doi: 10.1105/tpc.113.114736 24014547

20. Tan EH, Henry IM, Ravi M, Bradnam KR, Mandakova T, Marimuthu MP, et al. Catastrophic chromosomal restructuring during genome elimination in plants. eLife. 2015:e06516.

21. Ravi M, Chan SWL. Haploid plants produced by centromere-mediated genome elimination. Nature. 2010;464(7288):615–8. doi: http://www.nature.com/nature/journal/v464/n7288/suppinfo/nature08842_S1.html. doi: 10.1038/nature08842 20336146

22. Lermontova I, Koroleva O, Rutten T, Fuchs J, Schubert V, Moraes I, et al. Knockdown of CENH3 in Arabidopsis reduces mitotic divisions and causes sterility by disturbed meiotic chromosome segregation. The Plant Journal. 2011;68(1):40–50. doi: 10.1111/j.1365-313X.2011.04664.x 21635586

23. Forster BP, Thomas WTB. Doubled Haploids in Genetics and Plant Breeding. Plant Breeding Reviews: John Wiley & Sons, Inc.; 2010. p. 57–88.

24. Wędzony M, Forster BP, Żur I, Golemiec E, Szechyńska-Hebda M, Dubas E, et al. Progress in Doubled Haploid Technology in Higher Plants. In: Touraev A, Forster B, Jain SM, editors. Advances in Haploid Production in Higher Plants: Springer Netherlands; 2009. p. 1–33.

25. Tester M, Langridge P. Breeding Technologies to Increase Crop Production in a Changing World. Science. 2010;327(5967):818–22. doi: 10.1126/science.1183700 20150489

26. Ng PC, Henikoff S. Predicting the Effects of Amino Acid Substitutions on Protein Function. Annual Review of Genomics and Human Genetics. 2006;7(1):61–80. doi: 10.1146/annurev.genom.7.080505.115630 16824020.

27. Kumar P, Henikoff S, Ng PC. Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protocols. 2009;4(8):1073–81.

28. Henry IM, Dilkes BP, Miller ES, Burkart-Waco D, Comai L. Phenotypic Consequences of Aneuploidy in Arabidopsis thaliana. Genetics. 2010;186(4):1231–45. doi: 10.1534/genetics.110.121079 20876566

29. Cifuentes M, Rivard M, Pereira L, Chelysheva L, Mercier R. Haploid Meiosis in Arabidopsis: Double-Strand Breaks Are Formed and Repaired but Without Synapsis and Crossovers. PLoS ONE. 2013;8(8):e72431. doi: 10.1371/journal.pone.0072431 23951324

30. Till BJ, Reynolds SH, Greene EA, Codomo CA, Enns LC, Johnson JE, et al. Large-scale discovery of induced point mutations with high-throughput TILLING. Genome research. 2003;13(3):524–30. 12618384

31. Ravi M, Marimuthu MPA, Tan EH, Maheshwari S, Henry IM, Marin-Rodriguez B, et al. A haploid genetics toolbox for Arabidopsis thaliana. Nat Commun. 2014;5. doi: 10.1038/ncomms6334

32. Cao J, Schneeberger K, Ossowski S, Gunther T, Bender S, Fitz J, et al. Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat Genet. 2011;43(10):956–63. doi: http://www.nature.com/ng/journal/v43/n10/abs/ng.911.html—supplementary-information. doi: 10.1038/ng.911 21874002

33. Hirsch CD, Wu Y, Yan H, Jiang J. Lineage-Specific Adaptive Evolution of the Centromeric Protein CENH3 in Diploid and Allotetraploid Oryza Species. Molecular Biology and Evolution. 2009;26(12):2877–85. doi: 10.1093/molbev/msp208 19741004

34. Tachiwana H, Kagawa W, Shiga T, Osakabe A, Miya Y, Saito K, et al. Crystal structure of the human centromeric nucleosome containing CENP-A. Nature. 2011;476(7359):232–5. doi: http://www.nature.com/nature/journal/v476/n7359/abs/nature10258.html—supplementary-information. doi: 10.1038/nature10258 21743476

35. Sekulic N, Bassett EA, Rogers DJ, Black BE. The structure of (CENP-A-H4)2 reveals physical features that mark centromeres. Nature. 2010;467(7313):347–51. doi: http://www.nature.com/nature/journal/v467/n7313/abs/nature09323.html—supplementary-information. doi: 10.1038/nature09323 20739937

36. Zhang W, Colmenares Serafin U, Karpen Gary H. Assembly of Drosophila Centromeric Nucleosomes Requires CID Dimerization. Molecular Cell. 2012;45(2):263–9. doi: http://dx.doi.org/10.1016/j.molcel.2011.12.010. doi: 10.1016/j.molcel.2011.12.010 22209075

37. Bassett Emily A, DeNizio J, Barnhart-Dailey Meghan C, Panchenko T, Sekulic N, Rogers Danielle J, et al. HJURP Uses Distinct CENP-A Surfaces to Recognize and to Stabilize CENP-A/Histone H4 for Centromere Assembly. Developmental Cell. 2012;22(4):749–62. doi: http://dx.doi.org/10.1016/j.devcel.2012.02.001. doi: 10.1016/j.devcel.2012.02.001 22406139

38. Ingouff M, Rademacher S, Holec S, Šoljić L, Xin N, Readshaw A, et al. Zygotic Resetting of the HISTONE 3 Variant Repertoire Participates in Epigenetic Reprogramming in Arabidopsis. Current Biology. 2010;20(23):2137–43. doi: http://dx.doi.org/10.1016/j.cub.2010.11.012. doi: 10.1016/j.cub.2010.11.012 21093266

39. Sanei M, Pickering R, Kumke K, Nasuda S, Houben A. Loss of centromeric histone H3 (CENH3) from centromeres precedes uniparental chromosome elimination in interspecific barley hybrids. Proceedings of the National Academy of Sciences. 2011;108(33):E498–E505. doi: 10.1073/pnas.1103190108

40. Forster BP, Heberle-Bors E, Kasha KJ, Touraev A. The resurgence of haploids in higher plants. Trends in Plant Science. 2007;12(8):368–75. doi: http://dx.doi.org/10.1016/j.tplants.2007.06.007. 17629539

41. Chan SWL. Chromosome engineering: power tools for plant genetics. Trends in Biotechnology. 28(12):605–10. doi: 10.1016/j.tibtech.2010.09.002 20933291

42. Dunwell JM. Haploids in flowering plants: Origins and exploitation. Plant Biotechnol Journal. 2010; 8 : 377–424.

43. Murovec J, Bohanec B. Haploids and Doubled Haploids in Plant Breeding. In: Abdurakhmonov I, editor. Plant Breeding2012.

44. Feuillet C, Leach JE, Rogers J, Schnable PS, Eversole K. Crop genome sequencing: lessons and rationales. Trends in Plant Science. 2011;16(2):77–88. doi: http://dx.doi.org/10.1016/j.tplants.2010.10.005. doi: 10.1016/j.tplants.2010.10.005 21081278

45. Seymour DK, Filiault DL, Henry IM, Monson-Miller J, Ravi M, Pang A, et al. Rapid creation of Arabidopsis doubled haploid lines for quantitative trait locus mapping. Proceedings of the National Academy of Sciences. 2012 : 4227–32. doi: 10.1073/pnas.1117277109

46. Wijnker E, van Dun K, de Snoo CB, Lelivelt CLC, Keurentjes JJB, Naharudin NS, et al. Reverse breeding in Arabidopsis thaliana generates homozygous parental lines from a heterozygous plant. Nat Genet. 2012;44(4):467–70. doi: http://www.nature.com/ng/journal/v44/n4/abs/ng.2203.html—supplementary-information. doi: 10.1038/ng.2203 22406643

47. Marimuthu MPA, Jolivet S, Ravi M, Pereira L, Davda JN, Cromer L, et al. Synthetic Clonal Reproduction Through Seeds. Science. 2011;331(6019):876. doi: 10.1126/science.1199682 21330535

48. Ravi M, Marimuthu MPA, Tan EH, Maheshwari S. A haploid genetics toolbox for Arabidopsis thaliana. Nature Communications. In Press.

49. Comai L, Henikoff S. TILLING: practical single-nucleotide mutation discovery. The Plant Journal. 2006;45(4):684–94. doi: 10.1111/j.1365-313X.2006.02670.x 16441355

50. Ravi M, Shibata F, Ramahi JS, Nagaki K, Chen CB, Murata M, et al. Meiosis-Specific Loading of the Centromere-Specific Histone CENH3 in Arabidopsis thaliana. Plos Genet. 2011;7(6). doi: Artn E1002121 doi: 10.1371/Journal.Pgen.1002121 WOS:000292386300037.

51. Clough SJ, Bent AF. Floral dip: a simplified method forAgrobacterium‐mediated transformation ofArabidopsis thaliana. The plant journal. 1998;16(6):735–43. 10069079

52. Henry IM, Dilkes BP, Young K, Watson B, Wu H, Comai L. Aneuploidy and Genetic Variation in the Arabidopsis thaliana Triploid Response. Genetics. 2005;170(4):1979–88. doi: 10.1534/genetics.104.037788 15944363

53. Armstrong SJ, Franklin FCH, Jones GH. Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana. Journal of Cell Science. 2001;114(23):4207–17.

54. Peterson R, Slovin JP, Chen C. A simplified method for differential staining of aborted and non-aborted pollen grains. International Journal of Plant Biology. 2010;1(2):13.

55. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28(12):1647–9. doi: 10.1093/bioinformatics/bts199 22543367