Differing Requirements for RAD51 and DMC1 in Meiotic Pairing of Centromeres and Chromosome Arms in
During meiosis homologous chromosomes pair, recombine, and synapse, thus ensuring accurate chromosome segregation and the halving of ploidy necessary for gametogenesis. The processes permitting a chromosome to pair only with its homologue are not fully understood, but successful pairing of homologous chromosomes is tightly linked to recombination. In Arabidopsis thaliana, meiotic prophase of rad51, xrcc3, and rad51C mutants appears normal up to the zygotene/pachytene stage, after which the genome fragments, leading to sterility. To better understand the relationship between recombination and chromosome pairing, we have analysed meiotic chromosome pairing in these and in dmc1 mutant lines. Our data show a differing requirement for these proteins in pairing of centromeric regions and chromosome arms. No homologous pairing of mid-arm or distal regions was observed in rad51, xrcc3, and rad51C mutants. However, homologous centromeres do pair in these mutants and we show that this does depend upon recombination, principally on DMC1. This centromere pairing extends well beyond the heterochromatic centromere region and, surprisingly, does not require XRCC3 and RAD51C. In addition to clarifying and bringing the roles of centromeres in meiotic synapsis to the fore, this analysis thus separates the roles in meiotic synapsis of DMC1 and RAD51 and the meiotic RAD51 paralogs, XRCC3 and RAD51C, with respect to different chromosome domains.
Vyšlo v časopise:
Differing Requirements for RAD51 and DMC1 in Meiotic Pairing of Centromeres and Chromosome Arms in. PLoS Genet 8(4): e32767. doi:10.1371/journal.pgen.1002636
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002636
Souhrn
During meiosis homologous chromosomes pair, recombine, and synapse, thus ensuring accurate chromosome segregation and the halving of ploidy necessary for gametogenesis. The processes permitting a chromosome to pair only with its homologue are not fully understood, but successful pairing of homologous chromosomes is tightly linked to recombination. In Arabidopsis thaliana, meiotic prophase of rad51, xrcc3, and rad51C mutants appears normal up to the zygotene/pachytene stage, after which the genome fragments, leading to sterility. To better understand the relationship between recombination and chromosome pairing, we have analysed meiotic chromosome pairing in these and in dmc1 mutant lines. Our data show a differing requirement for these proteins in pairing of centromeric regions and chromosome arms. No homologous pairing of mid-arm or distal regions was observed in rad51, xrcc3, and rad51C mutants. However, homologous centromeres do pair in these mutants and we show that this does depend upon recombination, principally on DMC1. This centromere pairing extends well beyond the heterochromatic centromere region and, surprisingly, does not require XRCC3 and RAD51C. In addition to clarifying and bringing the roles of centromeres in meiotic synapsis to the fore, this analysis thus separates the roles in meiotic synapsis of DMC1 and RAD51 and the meiotic RAD51 paralogs, XRCC3 and RAD51C, with respect to different chromosome domains.
Zdroje
1. HassoldTHallHHuntP 2007 The origin of human aneuploidy: where we have been, where we are going. Hum Mol Genet 16 Spec No. 2 R203 208
2. BozzaCGPawlowskiWP 2008 The cytogenetics of homologous chromosome pairing in meiosis in plants. Cytogenet Genome Res 120 313 319
3. MooreGShawP 2009 Improving the chances of finding the right partner. Curr Opin Genet Dev 19 99 104
4. OsmanKHigginsJDSanchez-MoranEArmstrongSJFranklinFC 2011 Pathways to meiotic recombination in Arabidopsis thaliana. New Phytologist 190 523 544
5. TsaiJHMcKeeBD 2011 Homologous pairing and the role of pairing centers in meiosis. J Cell Sci 124 1955 1963
6. ZetkaM 2009 Homologue pairing, recombination and segregation in Caenorhabditis elegans. Genome Dyn 5 43 55
7. ScherthanH 2007 Telomere attachment and clustering during meiosis. Cell Mol Life Sci 64 117 124
8. BardhanAChuongHDawsonDS 2010 Meiotic cohesin promotes pairing of nonhomologous centromeres in early meiotic prophase. Molecular Biology of the Cell 21 1799 1809
9. ObesoDDawsonDS 2010 Temporal characterization of homology-independent centromere coupling in meiotic prophase. PloS ONE 5 e10336 doi:10.1371/journal.pone.0010336
10. TsubouchiTMacqueenAJRoederGS 2008 Initiation of meiotic chromosome synapsis at centromeres in budding yeast. Genes Dev 22 3217 3226
11. TsubouchiTRoederGS 2005 A synaptonemal complex protein promotes homology-independent centromere coupling. Science 308 870 873
12. FalkJEChanACHoffmannEHochwagenA 2010 A Mec1- and PP4-dependent checkpoint couples centromere pairing to meiotic recombination. Developmental Cell 19 599 611
13. Martinez-PerezEShawPMooreG 2001 The Ph1 locus is needed to ensure specific somatic and meiotic centromere association. Nature 411 204 207
14. Martinez-PerezEShawPReaderSAragon-AlcaideLMillerT 1999 Homologous chromosome pairing in wheat. J Cell Sci 112 Pt 11 1761 1769
15. RonceretADoutriauxMPGolubovskayaINPawlowskiWP 2009 PHS1 regulates meiotic recombination and homologous chromosome pairing by controlling the transport of RAD50 to the nucleus. Proc Natl Acad Sci U S A 106 20121 20126
16. StewartMNDawsonDS 2008 Changing partners: moving from non-homologous to homologous centromere pairing in meiosis. Trends in Genetics 24 564 573
17. Arabidopsis-Genome-Initiative 2000 Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408 796 815
18. CopenhaverGPNickelKKuromoriTBenitoMIKaulS 1999 Genetic definition and sequence analysis of Arabidopsis centromeres. Science 286 2468 2474
19. MartienssenR 1998 Transposons, DNA methylation and gene control. Trends in genetics : TIG 14 263 264
20. RoundEKFlowersSKRichardsEJ 1997 Arabidopsis thaliana centromere regions: genetic map positions and repetitive DNA structure. Genome Research 7 1045 1053
21. NagakiKWallingJHirschCJiangJMurataM 2009 Structure and evolution of plant centromeres. Progress in Molecular and Subcellular Biology 48 153 179
22. BugreevDVPezzaRJMazinaOMVoloshinONCamerini-OteroRD 2011 The resistance of DMC1 D-loops to dissociation may account for the DMC1 requirement in meiosis. Nature Structural & Molecular Biology 18 56 60
23. NealeMJKeeneyS 2006 Clarifying the mechanics of DNA strand exchange in meiotic recombination. Nature 442 153 158
24. CarballoJAJohnsonALSedgwickSGChaRS 2008 Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination. Cell 132 758 770
25. NiuHWanLBaumgartnerBSchaeferDLoidlJ 2005 Partner choice during meiosis is regulated by Hop1-promoted dimerization of Mek1. Molecular Biology of the Cell 16 5804 5818
26. HoHCBurgessSM 2011 Pch2 acts through Xrs2 and Tel1/ATM to modulate interhomolog bias and checkpoint function during meiosis. PLoS Genet 7 e1002351 doi:10.1371/journal.pgen.1002351
27. BusyginaVSaroDWilliamsGLeungWKSayAF 2011 Novel attributes of Hed1 affect dynamics and activity of the Rad51 presynaptic filament during meiotic recombination. Journal of Biological Chemistry 287 1566 1575
28. BusyginaVSehornMGShiIYTsubouchiHRoederGS 2008 Hed1 regulates Rad51-mediated recombination via a novel mechanism. Genes & Development 22 786 795
29. CouteauFBelzileFHorlowCGrandjeanOVezonD 1999 Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis. Plant Cell 11 1623 1634
30. PradilloMLopezELinaceroRRomeroCCunadoN 2011 Together yes, but not coupled: new insights into the roles of RAD51 and DMC1 in plant meiotic recombination. Plant Journal Online publication. doi: 10.1111/j.1365-1313X.2011.04845.x
31. Sanchez-MoranESantosJLJonesGHFranklinFC 2007 ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Genes Dev 21 2220 2233
32. LiWChenCMarkmann-MulischUTimofejevaLSchmelzerE 2004 The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis. Proc Natl Acad Sci U S A 101 10596 10601
33. SiaudNDrayEGyIGerardETakvorianN 2004 Brca2 is involved in meiosis in Arabidopsis thaliana as suggested by its interaction with Dmc1. EMBO J 23 1392 1401
34. BadieSLiaoCThanasoulaMBarberPHillMA 2009 RAD51C facilitates checkpoint signaling by promoting CHK2 phosphorylation. J Cell Biol 185 587 600
35. BishopDKEarUBhattacharyyaACalderoneCBeckettM 1998 Xrcc3 is required for assembly of Rad51 complexes in vivo. J Biol Chem 273 21482 21488
36. MassonJYTarsounasMCStasiakAZStasiakAShahR 2001 Identification and purification of two distinct complexes containing the five RAD51 paralogs. Genes Dev 15 3296 3307
37. TarsounasMDaviesAAWestSC 2004 RAD51 localization and activation following DNA damage. Philos Trans R Soc Lond B Biol Sci 359 87 93
38. van VeelenLRCervelliTvan de RaktMWTheilAFEssersJ 2005 Analysis of ionizing radiation-induced foci of DNA damage repair proteins. Mutat Res 574 22 33
39. van VeelenLREssersJvan de RaktMWOdijkHPastinkA 2005 Ionizing radiation-induced foci formation of mammalian Rad51 and Rad54 depends on the Rad51 paralogs, but not on Rad52. Mutat Res 574 34 49
40. KuznetsovSPellegriniMShudaKFernandez-CapetilloOLiuY 2007 RAD51C deficiency in mice results in early prophase I arrest in males and sister chromatid separation at metaphase II in females. The Journal of Cell Biology 176 581 592
41. KuznetsovSGHainesDCMartinBKSharanSK 2009 Loss of Rad51c leads to embryonic lethality and modulation of Trp53-dependent tumorigenesis in mice. Cancer Research 69 863 872
42. SharanSKKuznetsovSG 2007 Resolving RAD51C function in late stages of homologous recombination. Cell Division 2 15
43. AbeKOsakabeKNakayamaSEndoMTagiriA 2005 Arabidopsis RAD51C gene is important for homologous recombination in meiosis and mitosis. Plant Physiol 139 896 908
44. BleuyardJYGallegoMESavignyFWhiteCI 2005 Differing requirements for the Arabidopsis Rad51 paralogs in meiosis and DNA repair. Plant J 41 533 545
45. BleuyardJYGallegoMEWhiteCI 2004 The atspo11-1 mutation rescues atxrcc3 meiotic chromosome fragmentation. Plant Mol Biol 56 217 224
46. BleuyardJYWhiteCI 2004 The Arabidopsis homologue of Xrcc3 plays an essential role in meiosis. EMBO J 23 439 449
47. LiWYangXLinZTimofejevaLXiaoR 2005 The AtRAD51C gene is required for normal meiotic chromosome synapsis and double-stranded break repair in Arabidopsis. Plant Physiol 138 965 976
48. LiuYMassonJYShahRO'ReganPWestSC 2004 RAD51C is required for Holliday junction processing in mammalian cells. Science 303 243 246
49. LiuYTarsounasMO'ReganPWestSC 2007 Role of RAD51C and XRCC3 in genetic recombination and DNA repair. J Biol Chem 282 1973 1979
50. VignardJSiwiecTChelyshevaLVrielynckNGonordF 2007 The interplay of RecA-related proteins and the MND1-HOP2 complex during meiosis in Arabidopsis thaliana. PLoS Genet 3 e176 doi:10.1371/journal.pgen.0030176
51. ArmstrongSJFranklinFCJonesGH 2001 Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana. J Cell Sci 114 4207 4217
52. FranszPArmstrongSAlonso-BlancoCFischerTCTorres-RuizRA 1998 Cytogenetics for the model system Arabidopsis thaliana. Plant J 13 867 876
53. PradilloMSantosJL 2011 The template choice decision in meiosis: is the sister important? Chromosoma 120 447 454
54. DernburgAFMcDonaldKMoulderGBarsteadRDresserM 1998 Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94 387 398
55. McKimKSGreen-MarroquinBLSekelskyJJChinGSteinbergC 1998 Meiotic synapsis in the absence of recombination. Science 279 876 878
56. ScherthanH 2001 A bouquet makes ends meet. Nat Rev Mol Cell Biol 2 621 627
57. KempBBoumilRMStewartMNDawsonDS 2004 A role for centromere pairing in meiotic chromosome segregation. Genes Dev 18 1946 1951
58. TakeoSLakeCMMorais-de-SaESunkelCEHawleyRS 2011 Synaptonemal complex-dependent centromeric clustering and the initiation of synapsis in Drosophila oocytes. Curr Biol 21 1845 1851
59. TannetiNSLandyKJoyceEFMcKimKS 2011 A Pathway for Synapsis Initiation during Zygotene in Drosophila Oocytes. Curr Biol 21 1852 1857
60. ChurchKMoensPB 1976 Centromere behavior during interphase and meiotic prophase in Allium fistulosum from 3-D, EM reconstruction. Chromosoma 56 249 263
61. CaiXDongFEdelmannREMakaroffCA 2003 The Arabidopsis SYN1 cohesin protein is required for sister chromatid arm cohesion and homologous chromosome pairing. J Cell Sci 116 2999 3007
62. YangXBoatengKAStrittmatterLBurgessRMakaroffCA 2009 Arabidopsis separase functions beyond the removal of sister chromatid cohesion during meiosis. Plant Physiol 151 323 333
63. YangXTimofejevaLMaHMakaroffCA 2006 The Arabidopsis SKP1 homolog ASK1 controls meiotic chromosome remodeling and release of chromatin from the nuclear membrane and nucleolus. J Cell Sci 119 3754 3763
64. RobertsNYOsmanKArmstrongSJ 2009 Telomere distribution and dynamics in somatic and meiotic nuclei of Arabidopsis thaliana. Cytogenet Genome Res 124 193 201
65. BhallaNDernburgAF 2008 Prelude to a division. Annual Review of Cell and Developmental Biology 24 397 424
66. Howard-TillRALukaszewiczALoidlJ 2011 The recombinases Rad51 and Dmc1 play distinct roles in DNA break repair and recombination partner choice in the meiosis of Tetrahymena. PLoS Genet 7 e1001359 doi:10.1371/journal.pgen.1001359
67. HunterNKlecknerN 2001 The single-end invasion: an asymmetric intermediate at the double-strand break to double-holliday junction transition of meiotic recombination. Cell 106 59 70
68. ShinoharaMGasiorSLBishopDKShinoharaA 2000 Tid1/Rdh54 promotes colocalization of rad51 and dmc1 during meiotic recombination. Proc Natl Acad Sci U S A 97 10814 10819
69. DernburgAFSedatJWHawleyRS 1996 Direct evidence of a role for heterochromatin in meiotic chromosome segregation. Cell 86 135 146
70. KarpenGHLeMHLeH 1996 Centric heterochromatin and the efficiency of achiasmate disjunction in Drosophila female meiosis. Science 273 118 122
71. DaweRKSedatJWAgardDACandeWZ 1994 Meiotic chromosome pairing in maize is associated with a novel chromatin organization. Cell 76 901 912
72. MacQueenAJVilleneuveAM 2001 Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2. Genes Dev 15 1674 1687
73. ColasIShawPPrietoPWanousMSpielmeyerW 2008 Effective chromosome pairing requires chromatin remodeling at the onset of meiosis. Proc Natl Acad Sci U S A 105 6075 6080
74. PrietoPMooreGReaderS 2005 Control of conformation changes associated with homologue recognition during meiosis. Theor Appl Genet 111 505 510
75. PrietoPShawPMooreG 2004 Homologue recognition during meiosis is associated with a change in chromatin conformation. Nat Cell Biol 6 906 908
76. PecinkaASchubertVMeisterAKrethGKlatteM 2004 Chromosome territory arrangement and homologous pairing in nuclei of Arabidopsis thaliana are predominantly random except for NOR-bearing chromosomes. Chromosoma 113 258 269
77. RossKJFranszPJonesGH 1996 A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosome Res 4 507 516
78. KerzendorferCVignardJPedrosa-HarandASiwiecTAkimchevaS 2006 The Arabidopsis thaliana MND1 homologue plays a key role in meiotic homologous pairing, synapsis and recombination. J Cell Sci 119 2486 2496
79. PanoliAPRaviMSebastianJNishalBReddyTV 2006 AtMND1 is required for homologous pairing during meiosis in Arabidopsis. BMC Mol Biol 7 24
80. StronghillPPathanNHaHSupijonoEHasenkampfC 2010 Ahp2 (Hop2) function in Arabidopsis thaliana (Ler) is required for stabilization of close alignment and synaptonemal complex formation except for the two short arms that contain nucleolus organizer regions. Chromosoma 119 443 458
81. SchommerCBevenALawrensonTShawPSablowskiR 2003 AHP2 is required for bivalent formation and for segregation of homologous chromosomes in Arabidopsis meiosis. Plant J 36 1 11
82. GrelonMVezonDGendrotGPelletierG 2001 AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO J 20 589 600
83. Martinez-ZapaterJEstelleMSomervilleC 1986 A highly repeated DNA sequence in Arabidopsis thaliana. Molec Gen Genet 204 417 423
84. LysakMFranszPSchubertI 2006 Cytogenetic analyses of Arabidopsis. Methods Mol Biol 323 173 186
85. PawlowskiWPGolubovskayaINTimofejevaLMeeleyRBSheridanWF 2004 Coordination of meiotic recombination, pairing, and synapsis by PHS1. Science 303 89 92
86. BleuyardJYGallegoMEWhiteCI 2004 Meiotic defects in the Arabidopsis rad50 mutant point to conservation of the MRX complex function in early stages of meiotic recombination. Chromosoma 113 197 203
87. YangXBoatengKAYuanLWuSBaskinTI 2011 The radially swollen 4 separase mutation of Arabidopsis thaliana blocks chromosome disjunction and disrupts the radial microtubule system in meiocytes. PLoS ONE 6 e19459 doi:10.1371/journal.pone.0019459
88. BoatengKAYangXDongFOwenHAMakaroffCA 2008 SWI1 is required for meiotic chromosome remodeling events. Mol Plant 1 620 633
89. MercierRArmstrongSJHorlowCJacksonNPMakaroffCA 2003 The meiotic protein SWI1 is required for axial element formation and recombination initiation in Arabidopsis. Development 130 3309 3318
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 4
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
Najčítanejšie v tomto čísle
- A Coordinated Interdependent Protein Circuitry Stabilizes the Kinetochore Ensemble to Protect CENP-A in the Human Pathogenic Yeast
- Coordinate Regulation of Lipid Metabolism by Novel Nuclear Receptor Partnerships
- Defective Membrane Remodeling in Neuromuscular Diseases: Insights from Animal Models
- Formation of Rigid, Non-Flight Forewings (Elytra) of a Beetle Requires Two Major Cuticular Proteins