DOI QR코드

DOI QR Code

Current status and prospects of the meiosis-specific function of recombinase in plants

식물의 감수분열에서 상동 재조합 효소 특이 기능의 연구현황 및 전망

  • Jung, Yu Jin (Department of Horticultural Life Science, Hankyong National University) ;
  • Nam, Ki Hong (Department of Horticultural Life Science, Hankyong National University) ;
  • Kim, Tae Sung (Department of Agricultural Sciences, Korea National Open University) ;
  • Lee, In Hae (Biological Resources Division, National Institute of Biological Resources) ;
  • Cho, Yong-Gu (Department of Crop Science, Chungbuk National University) ;
  • Kang, Kwon Kyoo (Department of Horticultural Life Science, Hankyong National University)
  • 정유진 (국립한경대학교 원예생명과학과) ;
  • 남기홍 (국립한경대학교 원예생명과학과) ;
  • 김태성 (한국방송통신대학교 농학과) ;
  • 이인혜 (국립생물자원관 생물소재연구단 연구팀) ;
  • 조용구 (충북대학교 식물자원학과) ;
  • 강권규 (국립한경대학교 원예생명과학과)
  • Received : 2018.03.26
  • Accepted : 2018.03.26
  • Published : 2018.03.31

Abstract

Meiosis is a specialized cell division, essential in most reproducing organisms to halve the number of chromosomes, thereby enabling the restoration of ploidy levels during fertilization. A key step in meiosis is homologous recombination, which promotes homologous pairing and generates crossovers (COs) to connect homologous chromosomes until their separation at anaphase I. These CO sites, seen cytologically as chiasmata, represent a reciprocal exchange of genetic information between two homologous non-sister chromatids. RAD51, the eukaryotic homolog of the bacterial RecA recombinase, plays a central role in homologous recombination (HR) in yeast and animals. Loss of RAD51 function causes lethality in the flowering plant, Arabidopsis thaliana, suggesting that RAD51 has a meiotic stage-specific function that is different from homologous pairing activity.

Keywords

References

  1. Aboussekhra A, Chanet R, Adjiri A, Fabre F (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. Mol Cell Biol 12:3224-3234 https://doi.org/10.1128/MCB.12.7.3224
  2. Aihara H, Ito Y, Kurumizaka H, Yokoyama S, Shibata T (1999) The N-terminal domain of the human Rad51 protein binds DNA: structure and a DNA binding surface as revealed by NMR. J Mol Biol 290:495-504 https://doi.org/10.1006/jmbi.1999.2904
  3. Allers T, Lichten M (2001) Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106:47-57 https://doi.org/10.1016/S0092-8674(01)00416-0
  4. Basile G, Aker M, Mortimer RK (1992) Nucleotide sequence and transcriptional regulation of the yeast recombinational repair gene RAD51. Mol Cell Biol 12:3235-3246 https://doi.org/10.1128/MCB.12.7.3235
  5. Baumann P, Benson FE, West SC (1996) Human Rad51 protein promotes ATP-dependent homologous pairing and strand transfer reactions in vitro. Cell 87:757-766 https://doi.org/10.1016/S0092-8674(00)81394-X
  6. Benson FE, Stasiak A, West SC (1994) Purification and characterization of the human Rad51 protein, an analogue of E. coli RecA. EMBO J 13:5764-5771
  7. Bishop DK, Park D, Xu L, Kleckner N (1992) DMC1: a meiosisspecific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69:439-456 https://doi.org/10.1016/0092-8674(92)90446-J
  8. Bugreev DV, Golub EI, Stasiak AZ, Stasiak A, Mazin AV (2005) Activation of human meiosis-specific recombinase Dmc1 by Ca2+. J Biol Chem 280:26886-22695 https://doi.org/10.1074/jbc.M502248200
  9. Bugreev DV, Pezza RJ, Mazina OM, Voloshin ON, Camerini-Otero RD, Mazin AV (2011) The resistance of DMC1 D-loops to dissociation may account for the DMC1 requirement in meiosis. Nat Struct Mol Biol 18:56-60 https://doi.org/10.1038/nsmb.1946
  10. Busygina V, Sehorn MG, Shi IY, Tsubouchi H, Roeder GS, Sung P (2008) Hed1 regulates Rad51-mediated recombination via a novel mechanism. Genes Dev 22:786-795 https://doi.org/10.1101/gad.1638708
  11. Chen J, Villanueva N, Rould MA, Morrical SW (2010) Insights into the mechanism of Rad51 recombinase from the structure and properties of a filament interface mutant. Nucleic Acids Res. 38:4889-4906 https://doi.org/10.1093/nar/gkq209
  12. Chen Z, Yang H, Pavletich NP (2008) Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature 453:489-494 https://doi.org/10.1038/nature06971
  13. Cloud V, Chan YL, Grubb J, Budke B, Bishop DK (2012) Rad51 is an accessory factor for Dmc1-mediated joint molecule formation during meiosis. Science 337:1222-1225 https://doi.org/10.1126/science.1219379
  14. Cole F, Kauppi L, Lange J, Roig I, Wang R, Keeney S, Jasin M (2012) Homeostatic control of recombination is implemented progressively in mouse meiosis. Nat Cell Biol 4:424-430
  15. Conway AB, Lynch TW, Zhang Y, Fortin GS, Fung CW, Symington LS, Rice PA (2004) Crystal structure of a Rad51 filament. Nat Struct Mol Biol 11:791-796 https://doi.org/10.1038/nsmb795
  16. Da Ines O, Degroote F, Goubely C, Amiard S, Gallego ME, White CI (2013) Meiotic recombination in Arabidopsis is catalysed by DMC1, with RAD51 playing a supporting role. PLoS Genet 9, e1003787
  17. Fraune J, Schramm S, Alsheimer M, Benavente R (2012) The mammalian synaptonemal complex: protein components, assembly and role in meiotic recombination. Exp Cell Res 318:1340-1346 https://doi.org/10.1016/j.yexcr.2012.02.018
  18. Gupta RC, Bazemore LR, Golub EI, Radding CM (1997) Activities of human recombination protein Rad51. Proc Natl Acad Sci USA 94:463-468 https://doi.org/10.1073/pnas.94.2.463
  19. Habu T, Taki T, West A, Nishimune Y, Morita T (1996) The mouse and human homologs of DMC1, the yeast meiosis-specific homologous recombination gene, have a common unique form of exon-skipped transcript in meiosis. Nucleic Acids Res 24:470-477 https://doi.org/10.1093/nar/24.3.470
  20. Hikiba J, Hirota K, Kagawa W, Ikawa S, Kinebuchi T, Sakane I, Takizawa Y, Yokoyama S, Mandon-Pepin B, Nicolas A, Shibata T, Ohta K, Kurumizaka H (2008) Structural and functional analyses of the DMC1-M200V polymorphism found in the human population. Nucleic Acids Res 36:4181-4190 https://doi.org/10.1093/nar/gkn362
  21. Kagawa W, Kurumizaka H (2010). From meiosis to postmeiotic events: uncovering the molecular roles of the meiosis-specific recombinase Dmc1. FEBS J 277:590-598
  22. Keeney S (2008) Spo11 and the Formation of DNA Double-Strand Breaks in Meiosis. Genome Dyn Stab 2:81-123
  23. Keeney S, Giroux CN, Kleckner N (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88:375-384 https://doi.org/10.1016/S0092-8674(00)81876-0
  24. Kurumizaka H, Aihara H, Ikawa S, Kashima T, Bazemore L R, Kawasaki K, Sarai A, Radding C M, Shibata T (1996) A possible role of the C-terminal domain of the RecA protein. J Biol Chem 271:33515-33524
  25. Kurumizaka H, Ikawa S, Sarai A, Shibata T (1999) The mutant RecA proteins, RecAR243Q and RecAK245N, exhibit defective DNA binding in homologous pairing. Arch Biochem Biophys 365:83-91 https://doi.org/10.1006/abbi.1999.1166
  26. Lim DS, Hasty PA (1996) Mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53. Mol Cell Biol 16:7133-7143 https://doi.org/10.1128/MCB.16.12.7133
  27. Liu Y, Gaines WA, Callender T, Busygina V, Oke A, Sung P, Fung JC, Hollingsworth NM (2014) Down-regulation of Rad51 activity during meiosis in yeast prevents competition with Dmc1 for repair of double-strand breaks. PLoS Genet 10:e1004005 https://doi.org/10.1371/journal.pgen.1004005
  28. Maeshima K, Morimatsu K, Horii T (1996) Purification and characterization of XRad51.1 protein, Xenopus RAD51 homologue: recombinant XRad51.1 promotes strand exchange reaction. Genes Cells 1:1057-1068 https://doi.org/10.1046/j.1365-2443.1996.d01-224.x
  29. Mandon-Pepin B, Derbois C, Matsuda F, Cotinot C, Wolgemuth DJ, Smith K, McElreavey K, Nicolas A, Fellous M (2002) Human infertility: meiotic genes as potential candidates. Gynecol. Obstet Fertil. 30:817-821 https://doi.org/10.1016/S1297-9589(02)00444-7
  30. Mandon-Pepin B, Touraine P, Kuttenn F, Derbois C, Rouxel A, Matsuda F, Nicolas A, Cotinot C, Fellous M (2008) Genetic investigation of four meiotic genes in women with premature ovarian failure. European J Endocrinol 158:07-115
  31. Masson JY, Davies AA, Hajibagheri N, Van Dyck, E, Benson FE, Stasiak AZ, Stasiak A, West SC (1999) The meiosis-specific recombinase hDmc1 forms ring structures and interacts with hRad51. EMBO J 8:6552-6560
  32. Matsuo Y, Sakane I, Takizawa Y, Takahashi M, Kurumizaka H (2006) Roles of the human Rad51 L1 and L2 loops in DNA binding. FEBS J 273:3148-3159 https://doi.org/10.1111/j.1742-4658.2006.05323.x
  33. Mimitou EP, Symington LS (2008). Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455:770-774 https://doi.org/10.1038/nature07312
  34. Nassif N, Penney J, Pal S, Engels WR, Gloor GB (1994) Efficient copying of nonhomologous sequences from ectopic sites via P-element-induced gap repair. Mol Cell Biol 14:1613-1625 https://doi.org/10.1128/MCB.14.3.1613
  35. Neale MJ, Keeney S (2006). Clarifying the mechanics of DNA strand exchange in meiotic recombination. Nature 442:, 153-158
  36. Niu H, Wan L, Busygina V, Kwon Y, Allen JA, Li X, Kunz RC, Kubota K, Wang B, Sung P, Shokat KM, Gygi SP, Hollingsworth NM (2009) Regulation of meiotic recombination via Mek1-mediated Rad54 phosphorylation. Mol Cell 36:393-404 https://doi.org/10.1016/j.molcel.2009.09.029
  37. Ogawa T, Yu X, Shinohara A, Egelman EH (1993) Similarity of the yeast RAD51 filament to the bacterial RecA filament. Science 259:1896-1899 https://doi.org/10.1126/science.8456314
  38. Passy SI, Yu X, Li Z, Radding CM, Masson JY, West SC, Egelman EH (1999) Human Dmc1 protein binds DNA as an octameric ring. Proc Natl Acad Sci USA 96:10684-10688 https://doi.org/10.1073/pnas.96.19.10684
  39. Petronczki M, Siomos MF, Nasmyth K (2003) Un menage a quatre: the molecular biology of chromosome segregation in meiosis. Cell 112:423-40 https://doi.org/10.1016/S0092-8674(03)00083-7
  40. Pittman DL, Cobb J, Schimenti KJ, Wilson LA, Cooper DM, Brignull E, Handel MA, Schimenti JC (1998) Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. Mol Cell 1:697-705 https://doi.org/10.1016/S1097-2765(00)80069-6
  41. Renkawitz J, Lademann C A, Jentsch S (2014) Mechanisms and principles of homology search during recombination. Nat Rev. Mol Cell Biol 15:369-383
  42. Reymer A, Frykholm K, Morimatsu K, Takahashi M, Norden B (2009) Structure of human Rad51 protein filament from molecular modeling and site-specific linear dichroism spectroscopy. Proc Natl Acad Sci USA 106:13248-53
  43. Roeder GS (1997) Meiotic chromosomes: it takes two to tango. Genes Dev 15:2600-2621
  44. Sakane I, Kamataki C, Takizawa Y, Nakashima M, Toki S, Ichikawa H, Ikawa S, Shibata T, Kurumizaka H (2008) Filament formation and robust strand exchange activities of the rice DMC1A and DMC1B proteins. Nucleic Acids Res 6:4266-4276
  45. San Filippo J, Sung P, Klein H (2008) Mechanism of eukaryotic homologous recombination. Annu Rev Biochem 77: 229-257 https://doi.org/10.1146/annurev.biochem.77.061306.125255
  46. Schwacha A, Kleckner N (1997) Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomolog-only pathway. Cell 190:1123-1135
  47. Sehorn MG, Sigurdsson S, Bussen W, Unger VM, Sung P (2004) Human meiotic recombinase Dmc1 promotes ATP-dependent homologous DNA strand exchange. Nature 429:433-437 https://doi.org/10.1038/nature02563
  48. Shinohara A, Ogawa H, Ogawa T (1992) Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69:457-470 https://doi.org/10.1016/0092-8674(92)90447-K
  49. Shinohara A, Ogawa H, Matsuda Y, Ushio N, Ikeo K, Ogawa T (1993) Cloning of human, mouse and fission yeast recombination genes homologous to RAD51 and recA. Nat Genet 4:239-243 https://doi.org/10.1038/ng0793-239
  50. Shinohara M, Oh SD, Hunter N, Shinohara A (2008) Crossover assurance and crossover interference are distinctly regulated by the ZMM proteins during yeast meiosis. Nat Genet 40:299-309 https://doi.org/10.1038/ng.83
  51. Sonoda E, Sasaki MS, Buerstedde JM, Bezzubova O, Shinohara A, Ogawa H, Takata M, Yamaguchi-Iwai Y, Takeda S (1998) Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J 17:598-608 https://doi.org/10.1093/emboj/17.2.598
  52. Sung P (1994) Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science 265:1241-1243 https://doi.org/10.1126/science.8066464
  53. Symington L S (2002) Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol Mol Biol Rev 66:630-670 https://doi.org/10.1128/MMBR.66.4.630-670.2002
  54. Szostak JW, Orr-Weaver TL, Rothstein RJ, Stahl FW (1983) The double-strand-break repair model for recombination Cell 33: 25-35 https://doi.org/10.1016/0092-8674(83)90331-8
  55. Tsuzuki T, Fujii Y, Sakumi K, Tominaga Y, Nakao K, Sekiguchi M, Matsushiro A, Yoshimura Y, Morita T (1996) Targeted disruption of the Rad51 gene leads to lethality in embryonic mice. Proc Natl Acad Sci USA 93:6236-6240 https://doi.org/10.1073/pnas.93.13.6236
  56. West SC (2003) Molecular views of recombination proteins and their control. Nat Rev Mol Cell Biol 4:435-445
  57. Yoshida K, Kondoh G, Matsuda Y, Habu T, Nishimune Y, Morita T (1998) The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis. Mol Cell 1:707-718 https://doi.org/10.1016/S1097-2765(00)80070-2
  58. Yu X, Jacobs SA, West SC, Ogawa T, Egelman EH (2001) Domain structure and dynamics in the helical filaments formed by RecA and Rad51 on DNA. Proc Natl Acad Sci USA 98:8419-8424 https://doi.org/10.1073/pnas.111005398
  59. Zhou Y, Caron P, Legube G, Paull TT (2014) Quantitation of DNA double-strand break resection intermediates in human cells. Nucleic Acids Res 42:e19 https://doi.org/10.1093/nar/gkt1309