Meiotic Recombination in Arabidopsis Is Catalysed by DMC1, with RAD51 Playing a Supporting Role

English version České info

Recombination establishes the chiasmata that physically link pairs of homologous chromosomes in meiosis, ensuring their balanced segregation at the first meiotic division and generating genetic variation. The visible manifestation of genetic crossing-overs, chiasmata are the result of an intricate and tightly regulated process involving induction of DNA double-strand breaks and their repair through invasion of a homologous template DNA duplex, catalysed by RAD51 and DMC1 in most eukaryotes. We describe here a RAD51-GFP fusion protein that retains the ability to assemble at DNA breaks but has lost its DNA break repair capacity. This protein fully complements the meiotic chromosomal fragmentation and sterility of Arabidopsis rad51, but not rad51 dmc1 mutants. Even though DMC1 is the only active meiotic strand transfer protein in the absence of RAD51 catalytic activity, no effect on genetic map distance was observed in complemented rad51 plants. The presence of inactive RAD51 nucleofilaments is thus able to fully support meiotic DSB repair and normal levels of crossing-over by DMC1. Our data demonstrate that RAD51 plays a supporting role for DMC1 in meiotic recombination in the flowering plant, Arabidopsis.

Vyšlo v časopise: Meiotic Recombination in Arabidopsis Is Catalysed by DMC1, with RAD51 Playing a Supporting Role. PLoS Genet 9(9): e32767. doi:10.1371/journal.pgen.1003787
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003787

Souhrn

Zdroje

1. HunterN (2007) Meiotic recombination. Topics in Current Genetics - Molecular Genetics of Recombination 17: 381–442.

2. OsmanK, HigginsJD, Sanchez-MoranE, ArmstrongSJ, FranklinFC (2011) Pathways to meiotic recombination in Arabidopsis thaliana. The New phytologist 190: 523–544.

3. SheridanSD, YuX, RothR, HeuserJE, SehornMG, et al. (2008) A comparative analysis of Dmc1 and Rad51 nucleoprotein filaments. Nucleic acids research 36: 4057–4066.

4. MassonJY, WestSC (2001) The Rad51 and Dmc1 recombinases: a non-identical twin relationship. Trends in biochemical sciences 26: 131–136.

5. HongEL, ShinoharaA, BishopDK (2001) Saccharomyces cerevisiae Dmc1 protein promotes renaturation of single-strand DNA (ssDNA) and assimilation of ssDNA into homologous super-coiled duplex DNA. The Journal of biological chemistry 276: 41906–41912.

6. LiZ, GolubEI, GuptaR, RaddingCM (1997) Recombination activities of HsDmc1 protein, the meiotic human homolog of RecA protein. Proceedings of the National Academy of Sciences of the United States of America 94: 11221–11226.

7. SungP (1994) Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science 265: 1241–1243.

8. BishopDK, ParkD, XuL, KlecknerN (1992) DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69: 439–456.

9. NealeMJ, KeeneyS (2006) Clarifying the mechanics of DNA strand exchange in meiotic recombination. Nature 442: 153–158.

10. ShinoharaA, OgawaH, OgawaT (1992) Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69: 457–470.

11. AboussekhraA, ChanetR, AdjiriA, FabreF (1992) Semidominant suppressors of Srs2 helicase mutations of Saccharomyces cerevisiae map in the RAD51 gene, whose sequence predicts a protein with similarities to procaryotic RecA proteins. Molecular and cellular biology 12: 3224–3234.

12. GoldfarbT, LichtenM (2010) Frequent and efficient use of the sister chromatid for DNA double-strand break repair during budding yeast meiosis. PLoS biology 8: e1000520.

13. HyppaRW, SmithGR (2010) Crossover invariance determined by partner choice for meiotic DNA break repair. Cell 142: 243–255.

14. PhadnisN, HyppaRW, SmithGR (2011) New and old ways to control meiotic recombination. Trends in genetics 27: 411–421.

15. YoudsJL, BoultonSJ (2011) The choice in meiosis - defining the factors that influence crossover or non-crossover formation. Journal of cell science 124: 501–513.

16. SchwachaA, KlecknerN (1997) Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomolog-only pathway. Cell 90: 1123–1135.

17. BishopDK (1994) RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell 79: 1081–1092.

18. ShinoharaA, GasiorS, OgawaT, KlecknerN, BishopDK (1997) Saccharomyces cerevisiae recA homologues RAD51 and DMC1 have both distinct and overlapping roles in meiotic recombination. Genes to cells : devoted to molecular & cellular mechanisms 2: 615–629.

19. DresserME, EwingDJ, ConradMN, DominguezAM, BarsteadR, et al. (1997) DMC1 functions in a Saccharomyces cerevisiae meiotic pathway that is largely independent of the RAD51 pathway. Genetics 147: 533–544.

20. RockmillB, SymM, ScherthanH, RoederGS (1995) Roles for two RecA homologs in promoting meiotic chromosome synapsis. Genes & development 9: 2684–2695.

21. TsubouchiH, RoederGS (2003) The importance of genetic recombination for fidelity of chromosome pairing in meiosis. Developmental cell 5: 915–925.

22. BishopDK (2012) Rad51, the lead in mitotic recombinational DNA repair, plays a supporting role in budding yeast meiosis. Cell cycle 11: 4105–4106.

23. CloudV, ChanYL, GrubbJ, BudkeB, BishopDK (2012) Rad51 is an accessory factor for Dmc1-mediated joint molecule formation during meiosis. Science 337: 1222–1225.

24. SerrentinoME, BordeV (2012) The spatial regulation of meiotic recombination hotspots: are all DSB hotspots crossover hotspots? Experimental cell research 318: 1347–1352.

25. PittmanDL, CobbJ, SchimentiKJ, WilsonLA, CooperDM, et al. (1998) Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. Molecular cell 1: 697–705.

26. YoshidaK, KondohG, MatsudaY, HabuT, NishimuneY, et al. (1998) The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis. Molecular cell 1: 707–718.

27. CouteauF, BelzileF, HorlowC, GrandjeanO, VezonD, et al. (1999) Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis. The Plant cell 11: 1623–1634.

28. LiW, ChenC, Markmann-MulischU, TimofejevaL, SchmelzerE, et al. (2004) The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis. Proceedings of the National Academy of Sciences of the United States of America 101: 10596–10601.

29. PradilloM, LopezE, LinaceroR, RomeroC, CunadoN, et al. (2012) Together yes, but not coupled: new insights into the roles of RAD51 and DMC1 in plant meiotic recombination. The Plant Journal 69: 921–933.

30. Da InesO, AbeK, GoubelyC, GallegoME, WhiteCI (2012) Differing requirements for RAD51 and DMC1 in meiotic pairing of centromeres and chromosome arms in Arabidopsis thaliana. PLoS genetics 8: e1002636.

31. KurzbauerMT, UanschouC, ChenD, SchlogelhoferP (2012) The recombinases DMC1 and RAD51 are functionally and spatially separated during meiosis in Arabidopsis. The Plant cell 24: 2058–2070.

32. VignardJ, SiwiecT, ChelyshevaL, VrielynckN, GonordF, et al. (2007) The interplay of RecA-related proteins and the MND1-HOP2 complex during meiosis in Arabidopsis thaliana. PLoS genetics 3: 1894–1906.

33. ArmstrongSJ, CarylAP, JonesGH, FranklinFC (2002) Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. Journal of cell science 115: 3645–3655.

34. HigginsJD, Sanchez-MoranE, ArmstrongSJ, JonesGH, FranklinFC (2005) The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes & development 19: 2488–2500.

35. KnollA, HigginsJD, SeeligerK, RehaSJ, DangelNJ, et al. (2012) The Fanconi anemia ortholog FANCM ensures ordered homologous recombination in both somatic and meiotic cells in Arabidopsis. The Plant cell 24: 1448–1464.

36. OrelN, KyrykA, PuchtaH (2003) Different pathways of homologous recombination are used for the repair of double-strand breaks within tandemly arranged sequences in the plant genome. The Plant Journal 35: 604–612.

37. RothN, KlimeschJ, Dukowic-SchulzeS, PacherM, MannussA, et al. (2012) The requirement for recombination factors differs considerably between different pathways of homologous double-strand break repair in somatic plant cells. The Plant Journal 72: 781–790.

38. Da InesO, DegrooteF, AmiardS, GoubelyC, GallegoME, et al. (2013) Effects of XRCC2 and RAD51B mutations on somatic and meiotic recombination in Arabidopsis thaliana. The Plant Journal 74: 959–970.

39. ForgetAL, LoftusMS, McGrewDA, BennettBT, KnightKL (2007) The human Rad51 K133A mutant is functional for DNA double-strand break repair in human cells. Biochemistry 46: 3566–3575.

40. AkamatsuY, TsutsuiY, MorishitaT, SiddiqueMS, KurokawaY, et al. (2007) Fission yeast Swi5/Sfr1 and Rhp55/Rhp57 differentially regulate Rhp51-dependent recombination outcomes. The EMBO journal 26: 1352–1362.

41. StorlazziA, GarganoS, Ruprich-RobertG, FalqueM, DavidM, et al. (2010) Recombination proteins mediate meiotic spatial chromosome organization and pairing. Cell 141: 94–106.

42. TesseS, StorlazziA, KlecknerN, GarganoS, ZicklerD (2003) Localization and roles of Ski8p protein in Sordaria meiosis and delineation of three mechanistically distinct steps of meiotic homolog juxtaposition. Proceedings of the National Academy of Sciences of the United States of America 100: 12865–12870.

43. StorlazziA, TesseS, Ruprich-RobertG, GarganoS, PoggelerS, et al. (2008) Coupling meiotic chromosome axis integrity to recombination. Genes & development 22: 796–809.

44. DoutriauxMP, CouteauF, BergouniouxC, WhiteC (1998) Isolation and characterisation of the RAD51 and DMC1 homologs from Arabidopsis thaliana. Molecular & General Genetics 257: 283–291.

45. KlimyukVI, JonesJD (1997) AtDMC1, the Arabidopsis homologue of the yeast DMC1 gene: characterization, transposon-induced allelic variation and meiosis-associated expression. The Plant Journal 11: 1–14.

46. KagawaW, KurumizakaH (2010) From meiosis to postmeiotic events: uncovering the molecular roles of the meiosis-specific recombinase Dmc1. The FEBS journal 277: 590–598.

47. CrismaniW, PortemerV, FrogerN, ChelyshevaL, HorlowC, et al. (2013) MCM8 is required for a pathway of meiotic double-strand break repair independent of DMC1 in Arabidopsis thaliana. PLoS genetics 9: e1003165.

48. SeeligerK, Dukowic-SchulzeS, Wurz-WildersinnR, PacherM, PuchtaH (2012) BRCA2 is a mediator of RAD51- and DMC1-facilitated homologous recombination in Arabidopsis thaliana. The New phytologist 193: 364–375.

49. WeinerBM, KlecknerN (1994) Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast. Cell 77: 977–991.

50. XuL, WeinerBM, KlecknerN (1997) Meiotic cells monitor the status of the interhomolog recombination complex. Genes & development 11: 106–118.

51. BusyginaV, SaroD, WilliamsG, LeungWK, SayAF, et al. (2012) Novel attributes of Hed1 affect dynamics and activity of the Rad51 presynaptic filament during meiotic recombination. The Journal of biological chemistry 287: 1566–1575.

52. TsubouchiH, RoederGS (2006) Budding yeast Hed1 down-regulates the mitotic recombination machinery when meiotic recombination is impaired. Genes & development 20: 1766–1775.

53. BusyginaV, SehornMG, ShiIY, TsubouchiH, RoederGS, et al. (2008) Hed1 regulates Rad51-mediated recombination via a novel mechanism. Genes & development 22: 786–795.

54. FerdousM, HigginsJD, OsmanK, LambingC, RoitingerE, et al. (2012) Inter-homolog crossing-over and synapsis in Arabidopsis meiosis are dependent on the chromosome axis protein AtASY3. PLoS genetics 8: e1002507.

55. Sanchez-MoranE, SantosJL, JonesGH, FranklinFC (2007) ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Genes & development 21: 2220–2233.

56. KarimiM, DepickerA, HilsonP (2007) Recombinational cloning with plant gateway vectors. Plant physiology 145: 1144–1154.

57. CloughSJ, BentAF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16: 735–743.

58. BleuyardJY, GallegoME, SavignyF, WhiteCI (2005) Differing requirements for the Arabidopsis Rad51 paralogs in meiosis and DNA repair. The Plant Journal 41: 533–545.

59. BleuyardJY, WhiteCI (2004) The Arabidopsis homologue of Xrcc3 plays an essential role in meiosis. The EMBO journal 23: 439–449.

60. RossKJ, FranszP, JonesGH (1996) A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosome research 4: 507–516.

61. FranszP, ArmstrongS, Alonso-BlancoC, FischerTC, Torres-RuizRA, et al. (1998) Cytogenetics for the model system Arabidopsis thaliana. The Plant Journal 13: 867–876.

62. CharbonnelC, GallegoME, WhiteCI (2010) Xrcc1-dependent and Ku-dependent DNA double-strand break repair kinetics in Arabidopsis plants. The Plant Journal 64: 280–290.

63. MercierR, ArmstrongSJ, HorlowC, JacksonNP, MakaroffCA, et al. (2003) The meiotic protein SWI1 is required for axial element formation and recombination initiation in Arabidopsis. Development 130: 3309–3318.

64. HigginsJD, ArmstrongSJ, FranklinFC, JonesGH (2004) The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis. Genes & development 18: 2557–2570.

65. ChelyshevaL, GendrotG, VezonD, DoutriauxMP, MercierR, et al. (2007) Zip4/Spo22 is required for class I CO formation but not for synapsis completion in Arabidopsis thaliana. PLoS genetics 3: e83.