#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

The Role of Rice HEI10 in the Formation of Meiotic Crossovers


HEI10 was first described in human as a RING domain-containing protein that regulates cell cycle and cell invasion. Mice HEI10mei4 mutant displays no obvious defect other than meiotic failure from an absence of chiasmata. In this study, we characterize rice HEI10 by map-based cloning and explore its function during meiotic recombination. In the rice hei10 mutant, chiasma frequency is markedly reduced, and those remaining chiasmata exhibit a random distribution among cells, suggesting possible involvement of HEI10 in the formation of interference-sensitive crossovers (COs). However, mutation of HEI10 does not affect early recombination events and synaptonemal complex (SC) formation. HEI10 protein displays a highly dynamic localization on the meiotic chromosomes. It initially appears as distinct foci and co-localizes with MER3. Thereafter, HEI10 signals elongate along the chromosomes and finally restrict to prominent foci that specially localize to chiasma sites. The linear HEI10 signals always localize on ZEP1 signals, indicating that HEI10 extends along the chromosome in the wake of synapsis. Together our results suggest that HEI10 is the homolog of budding yeast Zip3 and Caenorhabditis elegans ZHP-3, and may specifically promote class I CO formation through modification of various meiotic components.


Vyšlo v časopise: The Role of Rice HEI10 in the Formation of Meiotic Crossovers. PLoS Genet 8(7): e32767. doi:10.1371/journal.pgen.1002809
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002809

Souhrn

HEI10 was first described in human as a RING domain-containing protein that regulates cell cycle and cell invasion. Mice HEI10mei4 mutant displays no obvious defect other than meiotic failure from an absence of chiasmata. In this study, we characterize rice HEI10 by map-based cloning and explore its function during meiotic recombination. In the rice hei10 mutant, chiasma frequency is markedly reduced, and those remaining chiasmata exhibit a random distribution among cells, suggesting possible involvement of HEI10 in the formation of interference-sensitive crossovers (COs). However, mutation of HEI10 does not affect early recombination events and synaptonemal complex (SC) formation. HEI10 protein displays a highly dynamic localization on the meiotic chromosomes. It initially appears as distinct foci and co-localizes with MER3. Thereafter, HEI10 signals elongate along the chromosomes and finally restrict to prominent foci that specially localize to chiasma sites. The linear HEI10 signals always localize on ZEP1 signals, indicating that HEI10 extends along the chromosome in the wake of synapsis. Together our results suggest that HEI10 is the homolog of budding yeast Zip3 and Caenorhabditis elegans ZHP-3, and may specifically promote class I CO formation through modification of various meiotic components.


Zdroje

1. KumarRBourbonHMde MassyB 2010 Functional conservation of Mei4 for meiotic DNA double-strand break formation from yeasts to mice. Genes Dev 24 1266 1280

2. YoudsJLBoultonSJ 2011 The choice in meiosis - defining the factors that influence crossover or non-crossover formation. J Cell Sci 124 501 513

3. HollingsworthNMBrillSJ 2004 The Mus81 solution to resolution: generating meiotic crossovers without Holliday junctions. Genes & Dev 18 117 125

4. de los SantosTHunterNLeeCLarkinBLoidlJ 2003 The Mus81/Mms4 endonuclease acts independently of double-Holliday junction resolution to promote a distinct subset of crossovers during meiosis in budding yeast. Genetics 164 81 94

5. BornerGVKlecknerNHunterN 2004 Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117 29 45

6. FungJCRockmillBOdellMRoederGS 2004 Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes. Cell 116 795 802

7. RockmillBFungJCBrandaSSRoederGS 2003 The Sgs1 helicase regulates chromosome synapsis and meiotic crossing over. Curr Biol 13 1954 1962

8. SymMEngebrechtJARoederGS 1993 ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72 365 378

9. NakagawaTFlores-RozasHKolodnerRD 2001 The MER3 helicase involved in meiotic crossing over is stimulated by single-stranded DNA-binding proteins and unwinds DNA in the 3′ to 5′ direction. J Biol Chem 276 31487 31493

10. SnowdenTAcharyaSButzCBerardiniMFishelR 2004 hMSH4-hMSH5 recognizes Holliday Junctions and forms a meiosis-specific sliding clamp that embraces homologous chromosomes. Mol Cell 15 437 451

11. BockerTBaruseviciusASnowdenTRasioDGuerretteS 1999 hMSH5: a human MutS homologue that forms a novel heterodimer with hMSH4 and is expressed during spermatogenesis. Cancer Res 59 816 822

12. ChuaPRRoederGS 1998 Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93 349 359

13. PerryJKlecknerNBornerGV 2005 Bioinformatic analyses implicate the collaborating meiotic crossover/chiasma proteins Zip2, Zip3, and Spo22/Zip4 in ubiquitin labeling. Proc Natl Acad Sci U S A 102 17594 17599

14. ChengCHLoYHLiangSSTiSCLinFM 2006 SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae. Genes & Dev 20 2067 2081

15. AgarwalSRoederGS 2000 Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102 245 255

16. LynnASoucekRBornerGV 2007 ZMM proteins during meiosis: crossover artists at work. Chromosome Res 15 591 605

17. TsubouchiTZhaoHRoederGS 2006 The meiosis-specific zip4 protein regulates crossover distribution by promoting synaptonemal complex formation together with zip2. Dev Cell 10 809 819

18. MacqueenAJRoederGS 2009 Fpr3 and Zip3 ensure that initiation of meiotic recombination precedes chromosome synapsis in budding yeast. Curr Biol 19 1519 1526

19. TsubouchiTMacqueenAJRoederGS 2008 Initiation of meiotic chromosome synapsis at centromeres in budding yeast. Genes Dev 22 3217 3226

20. WangKTangDWangMLuJYuH 2009 MER3 is required for normal meiotic crossover formation, but not for presynaptic alignment in rice. J Cell Sci 122 2055 2063

21. HigginsJDVignardJMercierRPughAGFranklinFC 2008 AtMSH5 partners AtMSH4 in the class I meiotic crossover pathway in Arabidopsis thaliana, but is not required for synapsis. Plant J 55 28 39

22. MercierRJolivetSVezonDHuppeEChelyshevaL 2005 Two meiotic crossover classes cohabit in Arabidopsis: one is dependent on MER3, whereas the other one is not. Curr Biol 15 692 701

23. ChenCZhangWTimofejevaLGerardinYMaH 2005 The Arabidopsis ROCK-N-ROLLERS gene encodes a homolog of the yeast ATP-dependent DNA helicase MER3 and is required for normal meiotic crossover formation. Plant J 43 321 334

24. HigginsJDArmstrongSJFranklinFCJonesGH 2004 The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis. Genes & Dev 18 2557 2570

25. WangMWangKTangDWeiCLiM 2010 The central element protein ZEP1 of synaptonemal complex regulates the number of crossovers during meiosis in rice. Plant Cell 22 417 430

26. HigginsJDSanchez-MoranEArmstrongSJJonesGHFranklinFC 2005 The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes & Dev 19 2488 2500

27. ChelyshevaLGendrotGVezonDDoutriauxMPMercierR 2007 Zip4/Spo22 is required for class I CO formation but not for synapsis completion in Arabidopsis thaliana. PLoS Genet 3 e83 doi:10.1371/journal.pgen.0030083

28. ShenYTangDWangKWangMHuangJ 2012 The Role of ZIP4 in Homologous Chromosome Synapsis and Crossover Formation in Rice Meiosis. Journal of Cell Science: In press

29. MacaisneNVignardJMercierR 2011 SHOC1 and PTD form an XPF-ERCC1-like complex that is required for formation of class I crossovers. J Cell Sci 124 2687 2691

30. MacaisneNNovatchkovaMPeireraLVezonDJolivetS 2008 SHOC1, an XPF endonuclease-related protein, is essential for the formation of class I meiotic crossovers. Curr Biol 18 1432 1437

31. WijeratneAJChenCZhangWTimofejevaLMaH 2006 The Arabidopsis thaliana PARTING DANCERS gene encoding a novel protein is required for normal meiotic homologous recombination. Mol Biol Cell 17 1331 1343

32. JantschVPasierbekPMuellerMMSchweizerDJantschM 2004 Targeted gene knockout reveals a role in meiotic recombination for ZHP-3, a Zip3-related protein in Caenorhabditis elegans. Mol Cell Biol 24 7998 8006

33. BhallaNWynneDJJantschVDernburgAF 2008 ZHP-3 acts at crossovers to couple meiotic recombination with synaptonemal complex disassembly and bivalent formation in C. elegans. PLoS Genet 4 e1000235 doi:10.1371/journal.pgen.1000235

34. TobyGGGherrabyWColemanTRGolemisEA 2003 A novel RING finger protein, human enhancer of invasion 10, alters mitotic progression through regulation of cyclin B levels. Mol Cell Biol 23 2109 2122

35. SinghMKNicolasEGherrabyWDadkeDLessinS 2007 HEI10 negatively regulates cell invasion by inhibiting cyclin B/Cdk1 and other promotility proteins. Oncogene 26 4825 4832

36. Sanchez MoranEArmstrongSJSantosJLFranklinFCJonesGH 2001 Chiasma formation in Arabidopsis thaliana accession Wassileskija and in two meiotic mutants. Chromosome Res 9 121 128

37. ShaoTTangDWangKWangMCheL 2011 OsREC8 is essential for chromatid cohesion and metaphase I monopolar orientation in rice meiosis. Plant Physiol 156 1386 1396

38. de BoerEStamPDietrichAJPastinkAHeytingC 2006 Two levels of interference in mouse meiotic recombination. Proc Natl Acad Sci U S A 103 9607 9612

39. LhuissierFGOffenbergHHWittichPEVischerNOHeytingC 2007 The mismatch repair protein MLH1 marks a subset of strongly interfering crossovers in tomato. Plant Cell 19 862 876

40. WangKWangMTangDShenYQinB 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

41. StrongERSchimentiJC 2010 Evidence Implicating CCNB1IP1, a RING Domain-Containing Protein Required for Meiotic Crossing Over in Mice, as an E3 SUMO Ligase. Genes (Basel) 1 440 451

42. KlecknerN 2006 Chiasma formation: chromatin/axis interplay and the role(s) of the synaptonemal complex. Chromosoma 115 175 194

43. PageSLHawleyRS 2004 The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol 20 525 558

44. ZicklerDKlecknerN 1999 Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33 603 754

45. DaweRK 1998 Meiotic Chromosome Organization and Segregation in Plants. Annu Rev Plant Physiol Plant Mol Biol 49 371 395

46. HamantOMaHCandeWZ 2006 Genetics of meiotic prophase I in plants. Annu Rev Plant Biol 57 267 302

47. LipkinSMMoensPBWangVLenziMShanmugarajahD 2002 Meiotic arrest and aneuploidy in MLH3-deficient mice. Nat Genet 31 385 390

48. MarconEMoensP 2003 MLH1p and MLH3p localize to precociously induced chiasmata of okadaic-acid-treated mouse spermatocytes. Genetics 165 2283 2287

49. JacksonNSanchez-MoranEBucklingEArmstrongSJJonesGH 2006 Reduced meiotic crossovers and delayed prophase I progression in AtMLH3-deficient Arabidopsis. Embo J 25 1315 1323

50. ChenJLuoWXLiMLuoQ 2011 Chromosome recombination in rice meiosis. Yi Chuan 33 648 653

51. OsmanKHigginsJDSanchez-MoranEArmstrongSJFranklinFC 2011 Pathways to meiotic recombination in Arabidopsis thaliana. New Phytol 190 523 544

52. HookerGWRoederGS 2006 A Role for SUMO in meiotic chromosome synapsis. Curr Biol 16 1238 1243

53. DeshaiesRJJoazeiroCA 2009 RING domain E3 ubiquitin ligases. Annu Rev Biochem 78 399 434

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2012 Číslo 7
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Eozinofilní granulomatóza s polyangiitidou
nový kurz
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#