OsHUS1 Facilitates Accurate Meiotic Recombination in Rice

English version České info

Meiosis is a special type of cell division that generates gametes for sexual reproduction. During meiosis, recombination not only occurs between allelic sequences on homologs, but also between non-allelic homologous sequences at dispersed loci. Such ectopic recombination is the main cause of chromosomal alterations and accounts for numerous genomic disorders in humans. To ensure genomic integrity, those ectopic recombinations must be quickly resolved. Despite the importance of ectopic recombination suppression, the mechanism underlying this process still remains largely unknown. Here, using rice as a model system, we identified the rice HUS1 homolog, a member of the RAD9-RAD1-HUS1 (9-1-1) complex, and elucidated its roles in meiotic recombination. In Oshus1, vigorous ectopic interactions occur between nonhomologous chromosomes, and the number of crossovers is reduced. We suspect that OsHUS1 participates in regulating ectopic interactions during meiosis, probably by forming the canonical RAD9-RAD1-HUS1 (9-1-1) complex.

Vyšlo v časopise: OsHUS1 Facilitates Accurate Meiotic Recombination in Rice. PLoS Genet 10(6): e32767. doi:10.1371/journal.pgen.1004405
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004405

Souhrn

Zdroje

1. ZicklerD, KlecknerN (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33 : 603–754.

2. PetronczkiM, SiomosMF, NasmythK (2003) Un menage a quatre: the molecular biology of chromosome segregation in meiosis. Cell 112 : 423–440.

3. HamantO, MaH, CandeW (2006) Genetics of meiotic prophase I in plants. Annu Rev Plant Biol 57 : 267–302.

4. PawlowskiWP, CandeWZ (2005) Coordinating the events of the meiotic prophase. Trends Cell Biol 15 : 674–681.

5. NiuH, WanL, BusyginaV, KwonYH, AllenJA, et al. (2009) Regulation of meiotic recombination via Mek1-mediated Rad54 phosphorylation. Mol Cell 36 : 393–404.

6. PradilloM, SantosJL (2011) The template choice decision in meiosis: is the sister important? Chromosoma 120 : 447–454.

7. ZicklerD (2006) From early homologue recognition to synaptonemal complex formation. Chromosoma 115 : 158–174.

8. BarzelA, KupiecM (2008) Finding a match: how do homologous sequences get together for recombination? Nat Rev Genet 9 : 27–37.

9. StankiewiczP, LupskiJ (2002) Genome architecture, rearrangements and genomic disorders. Trends Genet 18 : 74–82.

10. ChenJ-M, CooperDN, FérecC, Kehrer-SawatzkiH, PatrinosGP (2010) Genomic rearrangements in inherited disease and cancer. Semin Cancer Biol 20 : 222–233.

11. Jinks-RobertsonS, PetesTD (1985) High-frequency meiotic gene conversion between repeated genes on nonhomologous chromosomes in yeast. Proc Natl Acad Sci U S A 82 : 3350–3354.

12. GoldmanASH, LichtenM (1996) The efficiency of meiotic recombination between dispersed sequences in Saccharomyces cerevisiae depends upon their chromosomal location. Genetics 144 : 43–55.

13. SasakiM, LangeJ, KeeneyS (2010) Genome destabilization by homologous recombination in the germ line. Nat Rev Mol Cell Bio 11 : 182–195.

14. MieczkowskiPA, DominskaM, BuckMJ, LiebJD, PetesTD (2007) Loss of a histone deacetylase dramatically alters the genomic distribution of Spo11p-catalyzed DNA breaks in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 104 : 3955–3960.

15. GoldmanASH, LichtenM (2000) Restriction of ectopic recombination by interhomolog interactions during Saccharomyces cerevisiae meiosis. Proc Natl Acad Sci U S A 97 : 9537–9542.

16. HoangML, TanFJ, LaiDC, CelnikerSE, HoskinsRA, et al. (2010) Competitive repair by naturally dispersed repetitive DNA during non-allelic homologous recombination. PLoS Genet 6: e1001228.

17. LichtenM, HaberJE (1989) Position effects in ectopic and allelic mitotic recombination in Saccharomyces cerevisiae. Genetics 123 : 261–268.

18. KupiecM, PetesTD (1988) Allelic and ectopic recombination between Ty elements in yeast. Genetics 119 : 549–559.

19. HoangML, TanFJ, LaiDC, CelnikerSE, HoskinsRA, et al. (2010) Competitive repair by naturally dispersed repetitive DNA during non-allelic homologous recombination. PLoS Genet 6: e1001228.

20. VenclovasC, ThelenMP (2000) Structure-based predictions of Rad1, Rad9, Hus1 and Rad17 participation in sliding clamp and clamp-loading complexes. Nucleic Acids Res 28 : 2481–2493.

21. XuM, BaiL, GongY, XieW, HangH, et al. (2009) Structure and functional implications of the human Rad9-Hus1-Rad1 cell cycle checkpoint complex. J Biol Chem 284 : 20457–20461.

22. HarrisonJC, HaberJE (2006) Surviving the breakup: the DNA damage checkpoint. Annu Rev Genet 40 : 209–235.

23. EichingerCS, JentschS (2011) 9-1-1: PCNA's specialized cousin. Trends Biochem Sci 36 : 563–568.

24. HeltC, WangW, KengP, BambaraR (2005) Evidence that DNA damage detection machinery participates in DNA repair. Cell cycle 4 : 529–532.

25. HongE-JE, RoederGS (2002) A role for Ddc1 in signaling meiotic double-strand breaks at the pachytene checkpoint. Genes Dev 16 : 363–376.

26. GrushcowJM, HolzenTM, ParkKJ, WeinertT, LichtenM, et al. (1999) Saccharomyces cerevisiae checkpoint genes MEC1, RAD17 and RAD24 are required for normal meiotic recombination partner choice. Genetics 153 : 607–620.

27. FreireR, MurguíaJR, TarsounasM, LowndesNF, MoensPB, et al. (1998) Human and mouse homologs of Schizosaccharomyces pombe rad1+ and Saccharomyces cerevisiae RAD17: linkage to checkpoint control and mammalian meiosis. Genes Dev 12 : 2560–2573.

28. PeretzG, ArieLG, BakhratA, AbduU (2009) The Drosophila hus1 gene is required for homologous recombination repair during meiosis. Mech Develop 126 : 677–686.

29. LyndakerA, LimP, MleczkoJ, DigginsC, HollowayJ, et al. (2013) Conditional Inactivation of the DNA Damage Response Gene Hus1 in Mouse Testis Reveals Separable Roles for Components of the RAD9-RAD1-HUS1 Complex in Meiotic Chromosome Maintenance. PLoS Genet 9: e1003320.

30. WangM, WangK, TangD, WeiC, LiM, et al. (2010) The central element protein ZEP1 of the synaptonemal complex regulates the number of crossovers during meiosis in rice. Plant Cell 22 : 417–430.

31. NonomuraK, NakanoM, EiguchiM, SuzukiT, KurataN (2006) PAIR2 is essential for homologous chromosome synapsis in rice meiosis I. J Cell Sci 119 : 217–225.

32. WangK, WangM, TangD, ShenY, QinB, et al. (2011) PAIR3, an axis-associated protein, is essential for the recruitment of recombination elements onto meiotic chromosomes in rice. Mol Biol Cell 22 : 12–19.

33. Sanchez-MoranE, SantosJ-L, JonesGH, FranklinFCH (2007) ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Genes Dev 21 : 2220–2233.

34. WangK, TangD, WangM, LuJ, YuH, et al. (2009) MER3 is required for normal meiotic crossover formation, but not for presynaptic alignment in rice. J Cell Sci 122 : 2055–2063.

35. ShenY, TangD, WangK, WangM, HuangJ, et al. (2012) ZIP4 in homologous chromosome synapsis and crossover formation in rice meiosis. J Cell Sci 125 : 2581–2591.

36. WangK, WangM, TangD, ShenY, MiaoC, et al. (2012) The role of rice HEI10 in the formation of meiotic crossovers. PLoS Genet 8: e1002809.

37. MurakamiH, KeeneyS (2008) Regulating the formation of DNA double-strand breaks in meiosis. Genes Dev 22 : 286–292.

38. LuoQ, LiY, ShenY, ChengZ (2014) Ten years of gene discovery for meiotic event control in rice. J Genet Genomics 41 : 125–137.

39. De MuytA, PereiraL, VezonD, ChelyshevaL, GendrotG, et al. (2009) A high throughput genetic screen identifies new early meiotic recombination functions in Arabidopsis thaliana. PLoS Genet 5: e1000654.

40. De MuytA, VezonD, GendrotG, GalloisJL, StevensR, et al. (2007) AtPRD1 is required for meiotic double strand break formation in Arabidopsis thaliana. EMBO J 26 : 4126–4137.

41. NonomuraK, NakanoM, FukudaT, EiguchiM, MiyaoA, et al. (2004) The novel gene HOMOLOGOUS PAIRING ABERRATION IN RICE MEIOSIS1 of rice encodes a putative coiled-coil protein required for homologous chromosome pairing in meiosis. Plant Cell 16 : 1008–1020.

42. KouY, ChangY, LiX, XiaoJ, WangS (2012) The rice RAD51C gene is required for the meiosis of both female and male gametocytes and the DNA repair of somatic cells. J Exp Bot 63 : 5323–5335.

43. LiW, YangX, LinZ, TimofejevaL, XiaoR, et al. (2005) The AtRAD51C gene is required for normal meiotic chromosome synapsis and double-stranded break repair in Arabidopsis. Plant Physiol 138 : 965–976.

44. 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 Genet 8: e1002636.

45. JiJ, TangD, WangK, WangM, CheL, et al. (2012) The role of OsCOM1 in homologous chromosome synapsis and recombination in rice meiosis. Plant J 72 : 18–30.

46. ShaoT, TangD, WangK, WangM, CheL, et al. (2011) OsREC8 is essential for chromatid cohesion and metaphase I monopolar orientation in rice meiosis. Plant Physiol 156 : 1386–1396.

47. EnochT, CarrA, NurseP (1992) Fission yeast genes involved in coupling mitosis to completion of DNA replication. Genes Dev 6 : 2035–2046.

48. LongheseMP, FraschiniR, PlevaniP, LucchiniG (1996) Yeast pip3/mec3 mutants fail to delay entry into S phase and to slow DNA replication in response to DNA damage, and they define a functional link between Mec3 and DNA primase. Mol Cell Biol 16 : 3235–3244.

49. WeissRS, EnochT, LederP (2000) Inactivation of mouse Hus1 results in genomic instability and impaired responses to genotoxic stress. Genes Dev 14 : 1886–1898.

50. AbduU, KlovstadM, Butin-IsraeliV, BakhratA, SchüpbachT (2007) An essential role for Drosophila hus1 in somatic and meiotic DNA damage responses. J Cell Sci 120 : 1042–1049.

51. BoultonSJ, YeM, HofmannJJ, StergiouL, GartnerA, et al. (2002) Caenorhabditis elegans HUS-1 is a DNA damage checkpoint protein required for genome stability and EGL-1-mediated apoptosis. Curr Biol 12 : 1908–1918.

52. WeinertTA, KiserGL, HartwellLH (1994) Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair. Genes Dev 8 : 652–665.

53. KostrubCF, al-KhodairyF, GhazizadehH, CarrAM, EnochT (1997) Molecular analysis of hus1+, a fission yeast gene required for S-M and DNA damage checkpoints. Mol Gen Genet 254 : 389–399.

54. HeitzebergF, ChenIP, HartungF, OrelN, AngelisKJ, et al. (2004) The Rad17 homologue of Arabidopsis is involved in the regulation of DNA damage repair and homologous recombination. Plant J 38 : 954–968.

55. NagDK, PetesTD (1990) Meiotic recombination between dispersed repeated genes is associated with heteroduplex formation. Mol Cell Biol 10 : 4420–4423.

56. HastingsP (2010) Mechanisms of ectopic gene conversion. Genes 1 : 427–439.

57. HoangML, TanFJ, LaiDC, CelnikerSE, HoskinsRA, et al. (2010) Competitive repair by naturally dispersed repetitive DNA during non-allelic homologous recombination. PLoS genetics 6: e1001228.

58. BornerGV, KlecknerN, HunterN (2004) Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117 : 29–45.

59. BaiH, MadabushiA, GuanX, LuA (2010) Interaction between human mismatch repair recognition proteins and checkpoint sensor Rad9-Rad1-Hus1. DNA repair 9 : 478–487.

60. ZhangW, YiC, BaoW, LiuB, CuiJ, et al. (2005) The transcribed 165-bp CentO satellite is the major functional centromeric element in the wild rice species Oryza punctata. Plant Physiol 139 : 306–315.