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Meiosis-Specific Loading of the Centromere-Specific Histone CENH3 in


Centromere behavior is specialized in meiosis I, so that sister chromatids of homologous chromosomes are pulled toward the same side of the spindle (through kinetochore mono-orientation) and chromosome number is reduced. Factors required for mono-orientation have been identified in yeast. However, comparatively little is known about how meiotic centromere behavior is specialized in animals and plants that typically have large tandem repeat centromeres. Kinetochores are nucleated by the centromere-specific histone CENH3. Unlike conventional histone H3s, CENH3 is rapidly evolving, particularly in its N-terminal tail domain. Here we describe chimeric variants of CENH3 with alterations in the N-terminal tail that are specifically defective in meiosis. Arabidopsis thaliana cenh3 mutants expressing a GFP-tagged chimeric protein containing the H3 N-terminal tail and the CENH3 C-terminus (termed GFP-tailswap) are sterile because of random meiotic chromosome segregation. These defects result from the specific depletion of GFP-tailswap protein from meiotic kinetochores, which contrasts with its normal localization in mitotic cells. Loss of the GFP-tailswap CENH3 variant in meiosis affects recruitment of the essential kinetochore protein MIS12. Our findings suggest that CENH3 loading dynamics might be regulated differently in mitosis and meiosis. As further support for our hypothesis, we show that GFP-tailswap protein is recruited back to centromeres in a subset of pollen grains in GFP-tailswap once they resume haploid mitosis. Meiotic recruitment of the GFP-tailswap CENH3 variant is not restored by removal of the meiosis-specific cohesin subunit REC8. Our results reveal the existence of a specialized loading pathway for CENH3 during meiosis that is likely to involve the hypervariable N-terminal tail. Meiosis-specific CENH3 dynamics may play a role in modulating meiotic centromere behavior.


Vyšlo v časopise: Meiosis-Specific Loading of the Centromere-Specific Histone CENH3 in. PLoS Genet 7(6): e32767. doi:10.1371/journal.pgen.1002121
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002121

Souhrn

Centromere behavior is specialized in meiosis I, so that sister chromatids of homologous chromosomes are pulled toward the same side of the spindle (through kinetochore mono-orientation) and chromosome number is reduced. Factors required for mono-orientation have been identified in yeast. However, comparatively little is known about how meiotic centromere behavior is specialized in animals and plants that typically have large tandem repeat centromeres. Kinetochores are nucleated by the centromere-specific histone CENH3. Unlike conventional histone H3s, CENH3 is rapidly evolving, particularly in its N-terminal tail domain. Here we describe chimeric variants of CENH3 with alterations in the N-terminal tail that are specifically defective in meiosis. Arabidopsis thaliana cenh3 mutants expressing a GFP-tagged chimeric protein containing the H3 N-terminal tail and the CENH3 C-terminus (termed GFP-tailswap) are sterile because of random meiotic chromosome segregation. These defects result from the specific depletion of GFP-tailswap protein from meiotic kinetochores, which contrasts with its normal localization in mitotic cells. Loss of the GFP-tailswap CENH3 variant in meiosis affects recruitment of the essential kinetochore protein MIS12. Our findings suggest that CENH3 loading dynamics might be regulated differently in mitosis and meiosis. As further support for our hypothesis, we show that GFP-tailswap protein is recruited back to centromeres in a subset of pollen grains in GFP-tailswap once they resume haploid mitosis. Meiotic recruitment of the GFP-tailswap CENH3 variant is not restored by removal of the meiosis-specific cohesin subunit REC8. Our results reveal the existence of a specialized loading pathway for CENH3 during meiosis that is likely to involve the hypervariable N-terminal tail. Meiosis-specific CENH3 dynamics may play a role in modulating meiotic centromere behavior.


Zdroje

1. BrarGAAmonA 2008 Emerging roles for centromeres in meiosis I chromosome segregation. Nat Rev Genet 9 12 899 910

2. SakunoTTadaKWatanabeY 2009 Kinetochore geometry defined by cohesion within the centromere. Nature 458 7240 852 858

3. ChelyshevaLDialloSVezonDGendrotGVrielynckN 2005 AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis. J Cell Sci 118 Pt 20 4621 4632

4. LiXDaweRK 2009 Fused sister kinetochores initiate the reductional division in meiosis I. Nat Cell Biol 11 9 1103 1108

5. YokobayashiSWatanabeY 2005 The kinetochore protein Moa1 enables cohesion-mediated monopolar attachment at meiosis I. Cell 123 5 803 817

6. Monje-CasasFPrabhuVRLeeBHBoselliMAmonA 2007 Kinetochore orientation during meiosis is controlled by Aurora B and the monopolin complex. Cell 128 3 477 490

7. ClevelandDWMaoYSullivanKF 2003 Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 112 4 407 421

8. BlackBEBassettEA 2008 The histone variant CENP-A and centromere specification. Curr Opin Cell Biol 20 1 91 100

9. MalikHSHenikoffS 2003 Phylogenomics of the nucleosome. Nat Struct Biol 10 11 882 891

10. VermaakDHaydenHSHenikoffS 2002 Centromere targeting element within the histone fold domain of Cid. Mol Cell Biol 22 21 7553 7561

11. WielandGOrthausSOhndorfSDiekmannSHemmerichP 2004 Functional complementation of human centromere protein A (CENP-A) by Cse4p from Saccharomyces cerevisiae. Mol Cell Biol 24 15 6620 6630

12. BakerRERogersK 2006 Phylogenetic analysis of fungal centromere H3 proteins. Genetics 174 3 1481 1492

13. RaviMKwongPNMenorcaRMValenciaJTRamahiJS 2010 The Rapidly Evolving Centromere-specific Histone Has Stringent Functional Requirements in Arabidopsis thaliana. Genetics 186 461 471

14. RaviMChanSW 2010 Haploid plants produced by centromere-mediated genome elimination. Nature 464 7288 615 618

15. KalitsisPFowlerKJEarleEGriffithsBHowmanE 2003 Partially functional Cenpa-GFP fusion protein causes increased chromosome missegregation and apoptosis during mouse embryogenesis. Chromosome Res 11 4 345 357

16. LermontovaISchubertVFuchsJKlatteSMacasJ 2006 Loading of Arabidopsis centromeric histone CENH3 occurs mainly during G2 and requires the presence of the histone fold domain. Plant Cell 18 10 2443 2451

17. KhodjakovARiederCL 1996 Kinetochores moving away from their associated pole do not exert a significant pushing force on the chromosome. J Cell Biol 135 2 315 327

18. MazumdarMMisteliT 2005 Chromokinesins: multitalented players in mitosis. Trends Cell Biol 15 7 349 355

19. LiuZMakaroffCA 2006 Arabidopsis separase AESP is essential for embryo development and the release of cohesin during meiosis. Plant Cell 18 5 1213 1225

20. GoshimaGKiyomitsuTYodaKYanagidaM 2003 Human centromere chromatin protein hMis12, essential for equal segregation, is independent of CENP-A loading pathway. J Cell Biol 160 1 25 39

21. SalinaDEnarsonPRattnerJBBurkeB 2003 Nup358 integrates nuclear envelope breakdown with kinetochore assembly. J Cell Biol 162 6 991 1001

22. OhsugiMAdachiKHoraiRKakutaSSudoK 2008 Kid-mediated chromosome compaction ensures proper nuclear envelope formation. Cell 132 5 771 782

23. KoduruPRKRaoMK 1981 Cytogenetics of synaptic mutants in higher plants 59 197 214

24. GrelonMVezonDGendrotGPelletierG 2001 AtSPO11-1 is necessary for efficient meiotic recombination in plants. Embo J 20 3 589 600

25. ZhaoDYangXQuanLTimofejevaLRigelNW 2006 ASK1, a SKP1 homolog, is required for nuclear reorganization, presynaptic homolog juxtaposition and the proper distribution of cohesin during meiosis in Arabidopsis. Plant Mol Biol 62 1–2 99 110

26. ChenCFarmerADLangleyRJMudgeJCrowJA 2010 Meiosis-specific gene discovery in plants: RNA-Seq applied to isolated Arabidopsis male meiocytes. BMC Plant Biol 10 280

27. OguraYShibataFSatoHMurataM 2004 Characterization of a CENP-C homolog in Arabidopsis thaliana. Genes Genet Syst 79 3 139 144

28. SatoHShibataFMurataM 2005 Characterization of a Mis12 homologue in Arabidopsis thaliana. Chromosome Res 13 8 827 834

29. CheesemanIMChappieJSWilson-KubalekEMDesaiA 2006 The conserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell 127 5 983 997

30. GoshimaGSaitohSYanagidaM 1999 Proper metaphase spindle length is determined by centromere proteins Mis12 and Mis6 required for faithful chromosome segregation. Genes Dev 13 13 1664 1677

31. OegemaKDesaiARybinaSKirkhamMHymanAA 2001 Functional analysis of kinetochore assembly in Caenorhabditis elegans. J Cell Biol 153 6 1209 1226

32. SorgerPKDohenyKFHieterPKopskiKMHuffakerTC 1995 Two genes required for the binding of an essential Saccharomyces cerevisiae kinetochore complex to DNA. Proc Natl Acad Sci U S A 92 26 12026 12030

33. HealdRTournebizeRBlankTSandaltzopoulosRBeckerP 1996 Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature 382 6590 420 425

34. WatanabeYNurseP 1999 Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature 400 6743 461 464

35. TanakaKChangHLKagamiAWatanabeY 2009 CENP-C functions as a scaffold for effectors with essential kinetochore functions in mitosis and meiosis. Dev Cell 17 3 334 343

36. SasakiYYasudaHOhbaYHaradaH 1990 Isolation and characterization of a novel nuclear protein from pollen mother cells of lily. Plant Physiol 94 3 1467 1471

37. RiggsCDHasenkampfCA 1991 Antibodies directed against a meiosis-specific, chromatin-associated protein identify conserved meiotic epitopes. Chromosoma 101 2 92 98

38. SuzukiTIdeNTanakaI 1997 Immunocytochemical visualization of the centromeres during male and female meiosis in Lilium longiflorum. Chromosoma 106 7 435 445

39. Prymakowska-BosakMPrzewlokaMRSlusarczykJKurasMLichotaJ 1999 Linker histones play a role in male meiosis and the development of pollen grains in tobacco. Plant Cell 11 12 2317 2329

40. JansenLEBlackBEFoltzDRClevelandDW 2007 Propagation of centromeric chromatin requires exit from mitosis. J Cell Biol 176 6 795 805

41. SchuhMLehnerCFHeidmannS 2007 Incorporation of Drosophila CID/CENP-A and CENP-C into centromeres during early embryonic anaphase. Curr Biol 17 3 237 243

42. MaddoxPSHyndmanFMonenJOegemaKDesaiA 2007 Functional genomics identifies a Myb domain-containing protein family required for assembly of CENP-A chromatin. J Cell Biol 176 6 757 763

43. ErhardtSMelloneBGBettsCMZhangWKarpenGH 2008 Genome-wide analysis reveals a cell cycle-dependent mechanism controlling centromere propagation. J Cell Biol 183 5 805 818

44. DunleavyEMRocheDTagamiHLacosteNRay-GalletD 2009 HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres. Cell 137 3 485 497

45. FoltzDRJansenLEBaileyAOYatesJR3rdBassettEA 2009 Centromere-specific assembly of CENP-a nucleosomes is mediated by HJURP. Cell 137 3 472 484

46. MonenJMaddoxPSHyndmanFOegemaKDesaiA 2005 Differential role of CENP-A in the segregation of holocentric C. elegans chromosomes during meiosis and mitosis. Nat Cell Biol 7 12 1248 1255

47. DumontJOegemaKDesaiA 2010 A kinetochore-independent mechanism drives anaphase chromosome separation during acentrosomal meiosis. Nat Cell Biol

48. IngouffMRademacherSHolecSSoljicLXinN 2010 Zygotic resetting of the HISTONE 3 variant repertoire participates in epigenetic reprogramming in Arabidopsis. Curr Biol 20 23 2137 2143

49. DalalYWangHLindsaySHenikoffS 2007 Tetrameric structure of centromeric nucleosomes in interphase Drosophila cells. PLoS Biol 5 e218 doi:10.1371/journal.pbio.0050218

50. FuruyamaTHenikoffS 2009 Centromeric nucleosomes induce positive DNA supercoils. Cell 138 1 104 113

51. DalalYBuiM 2010 Down the rabbit hole of centromere assembly and dynamics. Curr Opin Cell Biol 22 3 392 402

52. CollinsKAFuruyamaSBigginsS 2004 Proteolysis contributes to the exclusive centromere localization of the yeast Cse4/CENP-A histone H3 variant. Curr Biol 14 21 1968 1972

53. ZeitlinSGShelbyRDSullivanKF 2001 CENP-A is phosphorylated by Aurora B kinase and plays an unexpected role in completion of cytokinesis. J Cell Biol 155 7 1147 1157

54. KouzaridesT 2007 Chromatin modifications and their function. Cell 128 4 693 705

55. MalikHSVermaakDHenikoffS 2002 Recurrent evolution of DNA-binding motifs in the Drosophila centromeric histone. Proc Natl Acad Sci U S A 99 3 1449 1454

56. HenikoffSAhmadKMalikHS 2001 The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293 5532 1098 1102

57. FishmanLSaundersA 2008 Centromere-associated female meiotic drive entails male fitness costs in monkeyflowers. Science 322 5907 1559 1562

58. SiddiqiIGaneshGGrossniklausUSubbiahV 2000 The dyad gene is required for progression through female meiosis in Arabidopsis. Development 127 1 197 207

59. RossKJFranszPJonesGH 1996 A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosome Res 4 7 507 516

60. MercierRVezonDBullierEMotamayorJCSellierA 2001 SWITCH1 (SWI1): a novel protein required for the establishment of sister chromatid cohesion and for bivalent formation at meiosis. Genes Dev 15 14 1859 1871

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