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Journal of Nucleic Acids
Volume 2010 (2010), Article ID 646109, 10 pages
http://dx.doi.org/10.4061/2010/646109
Review Article

Plant DNA Recombinases: A Long Way to Go

Plant Biochemistry Section, Molecular Biology Division, Bhabha Atomic Research Center, Trombay, Mumbai 400 085, India

Received 8 July 2009; Accepted 8 September 2009

Academic Editor: Aidan Doherty

Copyright © 2010 Rajani Kant Chittela and Jayashree K. Sainis. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. M. Cox, “Recombinational DNA repair of damaged repliction forks in Escherichia coli: questions,” Annual Review of Genetics, vol. 35, pp. 53–82, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  2. L. S. Symington, “Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair,” Microbiology and Molecular Biology Reviews, vol. 66, no. 4, pp. 630–670, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. A. J. Clark and A. D. Margulies, “Isolation and characterization of recombination-deficient mutants of E. coli K-12,” Proceedings of the National Academy of Sciences of the United States of America, vol. 53, pp. 451–459, 1965.
  4. P. Howard-Flanders and L. Theriot, “Mutants of Escherichia coli K-12 defective in DNA repair and in genetic recombination,” Genetics, vol. 53, no. 6, pp. 1137–1150, 1966. View at Scopus
  5. A. Shinohara, H. Ogawa, and T. Ogawa, “Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein,” Cell, vol. 69, no. 3, pp. 457–470, 1992. View at Publisher · View at Google Scholar · View at Scopus
  6. F.-X. Barre, B. Soballe, B. Michel, M. Aroyo, M. Robertson, and D. Sherratt, “Circles: the replication-recombination-chromosome segregation connection,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 15, pp. 8189–8195, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  7. E. C. Kowalczykowski, D. A. Dixon, A. K. Eggleston, S. D. Lauder, and W. M. Rehrauer, “Biochemistry of homologous recombination in Escherichia coli,” Microbiological Reviews, vol. 58, no. 3, pp. 401–465, 1994. View at Scopus
  8. G. M. Weinstock, K. McEntee, and I. R. Lehman, “ATP-dependent renaturation of DNA catalyzed by the recA protein of Escherichia coli,” Proceedings of the National Academy of Sciences of the United States of America, vol. 76, no. 1, pp. 126–130, 1979. View at Scopus
  9. F. R. Bryant and I. R. Lehman, “On the mechanism of renaturation of complementary DNA strands by the recA protein of Escherichia coli,” Proceedings of the National Academy of Sciences of the United States of America, vol. 82, no. 2, pp. 297–301, 1985. View at Scopus
  10. S. S. Tsang, K. Muniyappa, E. Azhderian, et al., “Intermediates in homologous pairing promoted by recA protein: isolation and characterization of coli protein omega,” Journal of Molecular Biology, vol. 55, pp. 523–533, 1985.
  11. F. R. Bryant, K. L. Menge, and T. T. Nguyen, “Kinetic modeling of the RecA protein promoted renaturation of complementary DNA strands,” Biochemistry, vol. 28, no. 3, pp. 1062–1069, 1989. View at Scopus
  12. K. McEntee, G. M. Weinstock, and I. R. Lehman, “DNA and nucleoside triphosphate binding properties of recA protein from Escherichia coli,” Progress in Nucleic Acid Research and Molecular Biology, vol. 26, pp. 265–279, 1981. View at Scopus
  13. J. P. Menetski and S. C. Kowalczykowski, “Interaction of recA protein with single-stranded DNA. Quantitative aspects of binding affinity modulation by nucleotide cofactors,” Journal of Molecular Biology, vol. 181, no. 2, pp. 281–295, 1985. View at Scopus
  14. W. Rosselli and A. Stasiak, “Energetics of RecA-mediated recombination reactions: without ATP hydrolysis RecA can mediate polar strand exchange but is unable to recycle,” Journal of Molecular Biology, vol. 216, no. 2, pp. 335–352, 1990. View at Publisher · View at Google Scholar · View at Scopus
  15. W. M. Rehrauer and S. C. Kowalczykowski, “Alteration of the nucleoside triphosphate (NTP) catalytic domain within Escherichia coli recA protein attenuates NTP hydrolysis but not joint molecule formation,” The Journal of Biological Chemistry, vol. 268, no. 2, pp. 1292–1297, 1993. View at Scopus
  16. K. J. MacFarland, Q. Shan, R. B. Inman, and M. M. Cox, “RecA as motor protein,” The Journal of Biological Chemistry, vol. 272, pp. 17675–17685, 1997.
  17. J.-Y. Masson and S. C. West, “The Rad51 and Dmc1 recombinases: a non-identical twin relationship,” Trends in Biochemical Sciences, vol. 26, no. 2, pp. 131–136, 2001. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Dudas and M. Chovanec, “DNA double-strand break repair by homologous recombination,” Mutation Research, vol. 566, no. 2, pp. 131–167, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  19. G. Basile, M. Aker, and R. K. Mortimer, “Nucleotide sequence and transcriptional regulation of the yeast recombinational repair gene RAD51,” Molecular and Cellular Biology, vol. 12, no. 7, pp. 3235–3246, 1992. View at Scopus
  20. P. Sung, “Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein,” Science, vol. 265, no. 5176, pp. 1241–1243, 1994. View at Scopus
  21. D. K. Bishop, D. Park, L. Xu, and N. Kleckner, “DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression,” Cell, vol. 69, no. 3, pp. 439–456, 1992. View at Publisher · View at Google Scholar · View at Scopus
  22. E. L. Hong, A. Shinohara, and D. K. Bishop, “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, vol. 276, no. 45, pp. 41906–41912, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  23. Y.-C. Chang, Y.-H. Lo, M.-H. Lee, et al., “Molecular visualization of the yeast Dmc1 protein ring and Dmc1-ssDNA nucleoprotein complex,” Biochemistry, vol. 44, no. 16, pp. 6052–6058, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  24. T. Habu, T. Taki, A. West, Y. Nishimune, and T. Morita, “The mouse and human homologs of DMC 1, the yeast meiosis-specific homologous recombination gene, have a common unique form of exon-skipped transcript in meiosis,” Nucleic Acids Research, vol. 24, no. 3, pp. 470–477, 1996. View at Scopus
  25. D. L. Pittman, J. Cobb, K. J. Schimenti, et al., “Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog,” Molecular Cell, vol. 1, no. 5, pp. 697–705, 1998. View at Scopus
  26. K. Yoshida, G. Kondoh, Y. Matsuda, T. Habu, Y. Nishimune, and T. Morita, “The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis,” Molecular Cell, vol. 1, no. 5, pp. 707–718, 1998. View at Scopus
  27. A. Shinohara, H. Ogawa, Y. Matsuda, N. Ushio, K. Ikeo, and T. Ogawa, “Cloning of human, mouse and fission yeast recombination genes homologous to RAD51 and recA,” Nature Genetics, vol. 4, no. 3, pp. 239–243, 1993. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  28. T. Morita, Y. Yoshimura, A. Yamamoto, et al., “A mouse homolog of the Escherichia coli recA and Saccharomyces cerevisiae RAD51 genes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 14, pp. 6577–6580, 1993. View at Scopus
  29. Y. Yoshimura, T. Morita, A. Yamamoto, and A. Matsushiro, “Cloning and sequence of the human RecA-like gene cDNA,” Nucleic Acids Research, vol. 21, no. 7, p. 1665, 1993. View at Scopus
  30. D.-S. Lim and P. Hasty, “A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53,” Molecular and Cellular Biology, vol. 16, no. 12, pp. 7133–7143, 1996. View at Scopus
  31. S. Tashiro, N. Kotomura, A. Shinohara, K. Tanaka, K. Ueda, and N. Kamada, “S phase specific formation of the human Rad51 protein nuclear foci in lymphocytes,” Oncogene, vol. 12, no. 10, pp. 2165–2170, 1996. View at Scopus
  32. J. Flygare, F. Benson, and D. Hellgren, “Expression of the human RAD51 gene during the cell cycle in primary human peripheral blood lymphocytes,” Biochimica et Biophysica Acta, vol. 1312, no. 3, pp. 231–236, 1996. View at Publisher · View at Google Scholar · View at Scopus
  33. S. J. Xia, M. A. Shammas, and R. J. Shmookler Reis, “Elevated recombination in immortal human cells is mediated by HsRAD51 recombinase,” Molecular and Cellular Biology, vol. 17, no. 12, pp. 7151–7158, 1997. View at Scopus
  34. E. A. Namsaraev and P. Berg, “Rad51 uses one mechanism to drive DNA strand exchange in both directions,” The Journal of Biological Chemistry, vol. 275, no. 6, pp. 3970–3976, 2000. View at Publisher · View at Google Scholar · View at Scopus
  35. E. A. Namsaraev and P. Berg, “Branch migration during Rad51-promoted strand exchange proceeds in either direction,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 18, pp. 10477–10481, 1998. View at Publisher · View at Google Scholar · View at Scopus
  36. P. Baumann, F. E. Benson, and S. C. West, “Human Rad51 protein promotes ATP-dependent homologous pairing and strand transfer reactions in vitro,” Cell, vol. 87, no. 4, pp. 757–766, 1996. View at Publisher · View at Google Scholar · View at Scopus
  37. R. C. Gupta, L. R. Bazemore, E. I. Golub, and C. M. Radding, “Activities of human recombination protein Rad51,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 2, pp. 463–468, 1997. View at Publisher · View at Google Scholar · View at Scopus
  38. J. K. Zutter and K. L. Knight, “The hRad51 and RecA proteins show significant differences in cooperative binding to single-stranded DNA,” Journal of Molecular Biology, vol. 293, no. 4, pp. 769–780, 1999. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  39. A. V. Mazin, E. Zaitseva, P. Sung, and S. C. Kowalczykowski, “Tailed duplex DNA is the preferred substrate for Rad51 protein-mediated homologous pairing,” The EMBO Journal, vol. 19, no. 5, pp. 1148–1156, 2000. View at Scopus
  40. R. C. Gupta, E. Golub, B. Bi, and C. M. Radding, “The synaptic activity of HsDmc1, a human recombination protein specific to meiosis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 15, pp. 8433–8439, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  41. Z. Li, E. I. Golub, R. Gupta, and C. M. Radding, “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, vol. 94, no. 21, pp. 11221–11226, 1997. View at Publisher · View at Google Scholar · View at Scopus
  42. M. G. Sehorn, S. Sigurdsson, W. Bussen, V. M. Unger, and P. Sung, “Human meiotic recombinase Dmc1 promotes ATP-dependent homologous DNA strand exchange,” Nature, vol. 429, no. 6990, pp. 433–437, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  43. S. I. Passy, X. Yu, Z. Li, et al., “Human Dmc1 protein binds DNA as an octameric ring,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 19, pp. 10684–10688, 1999. View at Publisher · View at Google Scholar · View at Scopus
  44. J.-Y. Masson, A. A. Davies, N. Hajibagheri, et al., “The meiosis-specific recombinase hDmc1 forms ring structures and interacts with hRad51,” The EMBO Journal, vol. 18, no. 22, pp. 6552–6560, 1999. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  45. M. C. Rice, S. T. Smith, F. Bullrich, P. Havre, and E. B. Kmiec, “Isolation of human and mouse genes based on homology to rec2, a recombinational repair gene from the fungus ustilago maydis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 14, pp. 7417–7422, 1997. View at Publisher · View at Google Scholar · View at Scopus
  46. J. S. Albala, M. P. Thelen, C. Prange, et al., “Identification of a novel human RAD51 homolog, RAD51B,” Genomics, vol. 46, no. 3, pp. 476–479, 1997. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  47. N. Liu, J. E. Lamerdin, R. S. Tebbs, et al., “XRCC2 and XRCC3, new human Rad51-family members, promote chromosome stability and protect against DNA cross-links and other damages,” Molecular Cell, vol. 1, no. 6, pp. 783–793, 1998. View at Scopus
  48. M. Kawabata and K. Saeki, “Sequence analysis and expression of a novel mouse homolog of Escherichia coli recA gene,” Biochimica et Biophysica Acta, vol. 1398, no. 3, pp. 353–358, 1998. View at Publisher · View at Google Scholar · View at Scopus
  49. M. K. Dosanjh, D. W. Collins, W. Fan, et al., “Isolation and characterization of RAD51C, a new human member of the RAD51 family of related genes,” Nucleic Acids Research, vol. 26, no. 5, pp. 1179–1184, 1998. View at Publisher · View at Google Scholar · View at Scopus
  50. R. Cartwright, A. M. Dunn, P. J. Simpson, C. E. Tambini, and J. Thacker, “Isolation of novel human and mouse genes of the recA/RAD51 recombination-repair gene family,” Nucleic Acids Research, vol. 26, no. 7, pp. 1653–1659, 1998. View at Publisher · View at Google Scholar · View at Scopus
  51. L. H. Thompson and D. Schild, “Recombinational DNA repair and human disease,” Mutation Research, vol. 509, no. 1-2, pp. 49–78, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. Z. Shu, S. Smith, L. Wang, M. C. Rice, and E. B. Kmiec, “Disruption of muREC2/RAD51L1 in mice results in early embryonic lethality which can be partially rescued in a p532/2 background,” Molecular and Cellular Biology, vol. 19, no. 12, pp. 8686–8693, 1999. View at Scopus
  53. D. L. Pittman and J. C. Schimenti, “Midgestation lethality in mice deficient for the RecA-related gene, Rad51d/Rad51l3,” Genesis, vol. 26, no. 3, pp. 167–173, 2000.
  54. B. Deans, C. S. Griffin, M. Maconochie, and J. Thacker, “Xrcc2 is required for genetic stability, embryonic neurogenesis and viability in mice,” The EMBO Journal, vol. 19, no. 24, pp. 6675–6685, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  55. S. Sigurdsson, K. Trujillo, B. Song, S. Stratton, and P. Sung, “Basis for Avid Homologous DNA strand exchange by human Rad51 and RPA,” The Journal of Biological Chemistry, vol. 276, no. 12, pp. 8798–8806, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  56. Y.-C. Lio, A. V. Mazin, S. C. Kowalczykowski, and D. J. Chen, “Complex formation by the human Rad51B and Rad51C DNA repair proteins and their activities in vitro,” The Journal of Biological Chemistry, vol. 278, no. 4, pp. 2469–2478, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  57. R. M. Story and T. A. Steitz, “Structure of the recA protein-ADP complex,” Nature, vol. 355, no. 6358, pp. 374–376, 1992. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  58. R. M. Story, I. T. Weber, and T. A. Steitz, “The structure of the E. coli recA protein monomer and polymer,” Nature, vol. 355, no. 6358, pp. 318–325, 1992. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  59. E. H. Egelman and A. Stasiak, “Structure of helical RecA-DNA complexes: complexes formed in the presence of ATP-gamma-S or ATP,” Journal of Molecular Biology, vol. 191, no. 4, pp. 677–697, 1986. View at Scopus
  60. E. H. Egelman and A. Stasiak, “Structure of helical RecA-DNA complexes—II: local conformational changes visualized in bundles of recA-ATP-γ-S filaments,” Journal of Molecular Biology, vol. 200, no. 2, pp. 329–349, 1988. View at Scopus
  61. M.-H. Lee, Y.-C. Chang, E. L. Hong, et al., “Calcium ion promotes yeast Dmc1 activity via formation of long and fine helical filaments with single-stranded DNA,” The Journal of Biological Chemistry, vol. 280, no. 49, pp. 40980–40984, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  62. T. Kinebuchi, W. Kagawa, R. Enomoto, et al., “Structural basis for octameric ring formation and DNA interaction of the human homologous-pairing protein Dmc1,” Molecular Cell, vol. 14, no. 3, pp. 363–374, 2004. View at Publisher · View at Google Scholar · View at Scopus
  63. F. E. Benson, A. Stasiak, and S. C. West, “Purification and characterization of the human Rad51 protein, an analogue of E. coli RecA,” The EMBO Journal, vol. 13, no. 23, pp. 5764–5771, 1994. View at Scopus
  64. P. Baumann and S. C. West, “Role of the human RAD51 protein in homologous recombination and double-stranded-break repair,” Trends in Biochemical Sciences, vol. 23, no. 7, pp. 247–251, 1998. View at Publisher · View at Google Scholar · View at Scopus
  65. P. Chi, S. Van-Komen, M. G. Sehorn, S. Sigurdsson, and P. Sung, “Roles of ATP binding and ATP hydrolysis in human Rad51 recombinase function,” DNA Repair, vol. 5, no. 3, pp. 381–391, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  66. V. E. Galkin, F. Esashi, X. Yu, S. Yang, S. C. West, and E. H. Egelman, “BRCA2 BRC motifs bind RAD51-DNA filaments,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 24, pp. 8537–8542, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  67. P. Sung and D. L. Robberson, “DNA strand exchange mediated by a RAD51-ssDNA nucleoprotein filament with polarity opposite to that of RecA,” Cell, vol. 82, no. 3, pp. 453–461, 1995. View at Scopus
  68. T. Ogawa, X. Yu, A. Shinohara, and E. H. Egelman, “Similarity of the yeast RAD51 filament to the bacterial RecA filament,” Science, vol. 259, no. 5103, pp. 1896–1899, 1993. View at Scopus
  69. A. B. Conway, T. W. Lynch, Y. Zhang, et al., “Crystal structure of a Rad51 filament,” Nature Structural and Molecular Biology, vol. 11, no. 8, pp. 791–796, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  70. A. A. Davies, J.-Y. Masson, M. J. McIlwraith, et al., “Role of BRCA2 in control of the RAD51 recombination and DNA repair protein,” Molecular Cell, vol. 7, no. 2, pp. 273–282, 2001. View at Publisher · View at Google Scholar · View at Scopus
  71. L. Pellegrini, D. S. Yu, T. Lo, et al., “Insights into DNA recombination from the structure of a RAD51-BRCA2 complex,” Nature, vol. 420, no. 6913, pp. 287–293, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  72. X. Xu, A. P. Hsia, L. Zhang, B. J. Nikolau, and P. S. Schnable, “Meiotic recombination break points resolve at high rates at the 5 end of a maize coding sequence,” The Plant Cell, vol. 7, pp. 2151–2161, 1995.
  73. G. I. Patterson, K. M. Kubo, T. Shroyer, and V. L. Chandler, “Sequences required for paramutation of the maize b gene map to a region containing the promoter and upstream sequences,” Genetics, vol. 140, no. 4, pp. 1389–1406, 1995. View at Scopus
  74. A. Peterhans, H. Schlupmann, C. Basse, and J. Paszkowski, “Intrachromosomal recombination in plants,” The EMBO Journal, vol. 9, no. 11, pp. 3437–3445, 1990. View at Scopus
  75. S. Gal, B. Pisan, T. Hohn, N. Grimsley, and B. Hohn, “Genomic homologous recombination in planta,” The EMBO Journal, vol. 10, no. 6, pp. 1571–1578, 1991. View at Scopus
  76. P. Swoboda, S. Gal, B. Hohn, and H. Puchta, “Intrachromosomal homologous recombination in whole plants,” The EMBO Journal, vol. 13, no. 2, pp. 484–489, 1994. View at Scopus
  77. H. Puchta, P. Swoboda, S. Gal, M. Blot, and B. Hohn, “Somatic intrachromosomal homologous recombination events in populations of plant siblings,” Plant Molecular Biology, vol. 28, no. 2, pp. 281–292, 1995. View at Scopus
  78. H. Puchta and B. Hohn, “From centiMorgans to base pairs: homologous recombination in plants,” Trends in Plant Science, vol. 1, no. 10, pp. 340–348, 1996. View at Publisher · View at Google Scholar · View at Scopus
  79. R. Offringa, M. J. A. de Groot, H. J. Haagsman, M. P. Does, P. J. M. Van den Elzen, and P. J. J. Hooykaas, “Extrachromosomal homologous recombination and gene targeting in plant cells after Agrobacterium mediated transformation,” The EMBO Journal, vol. 9, no. 10, pp. 3077–3084, 1990. View at Scopus
  80. B. Tinland, B. Hohn, and H. Puchta, “Agrobacterium tumefaciens transfers single-stranded transferred DNA (T-DNA) into the plant cell nucleus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 17, pp. 8000–8004, 1994. View at Publisher · View at Google Scholar · View at Scopus
  81. P. Athma and T. Peterson, “Ac induces homologous recombination at the maize P locus,” Genetics, vol. 128, no. 1, pp. 163–173, 1991. View at Scopus
  82. J. Tovar and C. Lichtenstein, “Somatic and meiotic chromosomal recombination between inverted duplications in transgenic tobacco plants,” The Plant Cell, vol. 4, no. 3, pp. 319–332, 1992. View at Scopus
  83. F. F. Assaad and E. R. Signer, “Somatic and germinal recombination of a direct repeat in Arabidopsis,” Genetics, vol. 132, no. 2, pp. 553–566, 1992. View at Scopus
  84. D. Schuermann, J. Molinier, O. Fritsch, and B. Hohn, “The dual nature of homologous recombination in plants,” Trends in Genetics, vol. 21, no. 3, pp. 172–181, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  85. J. E. Masson, P. J. King, and J. Paszkowski, “Mutants of Arabidopsis thaliana hypersensitive to DNA-damaging treatments,” Genetics, vol. 146, no. 1, pp. 401–407, 1997. View at Scopus
  86. J. E. Masson and J. Paszkowski, “Arabidopsis thaliana mutants altered in homologous recombination,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 21, pp. 11731–11735, 1997. View at Publisher · View at Google Scholar · View at Scopus
  87. M. E. Gallego, M. Jeanneau, F. Granier, et al., “Disruption of the Arabidopsis RAD50 gene leads to plant sterility and MMS sensitivity,” The Plant Journal, vol. 25, no. 1, pp. 31–41, 2001. View at Publisher · View at Google Scholar · View at Scopus
  88. H. Gherbi, M. E. Gallego, N. Jalut, J. M. Lucht, B. Hohn, and C. I. White, “Homologous recombination in planta is stimulated in the absence of Rad50,” EMBO Reports, vol. 2, no. 4, pp. 287–291, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  89. M. E. Gallego and C. I. White, “RAD50 function is essential for telomere maintenance in Arabidopsis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 4, pp. 1711–1716, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  90. F. Heitzeberg, I.-P. Chen, F. Hartung, N. Orel, K. J. Angelis, and H. Puchta, “The Rad17 homologue of Arabidopsis is involved in the regulation of DNA damage repair and homologous recombination,” The Plant Journal, vol. 38, no. 6, pp. 954–968, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  91. J.-Y. Bleuyard, M. E. Gallego, and C. I. White, “Recent advances in understanding of the DNA double-strand break repair machinery of plants,” DNA Repair, vol. 5, no. 1, pp. 1–12, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  92. S. Sato, Y. Hotta, and S. Tabata, “Structural analysis of a recA-like gene in the genome of Arabidopsis thaliana,” DNA Research, vol. 2, no. 2, pp. 89–93, 1995. View at Scopus
  93. M.-P. Doutriaux, F. Couteau, C. Bergounioux, and C. White, “Isolation and characterisation of the RAD51 and DMC1 homologs from Arabidopsis thaliana,” Molecular and General Genetics, vol. 257, no. 3, pp. 283–291, 1998. View at Publisher · View at Google Scholar · View at Scopus
  94. V. I. Klimyuk and J. D. G. Jones, “AtDMC1, the Arabidopsis homologue of the yeast DMC1 gene: characterization, transposon-induced allelic variation and meiosis-associated expression,” The Plant Journal, vol. 11, no. 1, pp. 1–14, 1997. View at Publisher · View at Google Scholar · View at Scopus
  95. J. Shimazu, C. Matsukura, M. Senda, et al., “Characterization of a DMC1 homologue, RiLIM15, in meiotic panicles, mitotic cultured cells and mature leaves of rice (Oryza sativa L.),” Theoretical and Applied Genetics, vol. 102, no. 8, pp. 1159–1163, 2001. View at Publisher · View at Google Scholar · View at Scopus
  96. A. Kathiresan, G. S. Khush, and J. Bennett, “Two rice DMC1 genes are differentially expressed during meiosis and during haploid and diploid mitosis,” Sexual Plant Reproduction, vol. 14, no. 5, pp. 257–267, 2002. View at Publisher · View at Google Scholar · View at Scopus
  97. Z.-J. Ding, T. Wang, K. Chong, and S. Bai, “Isolation and characterization of OsDMC1, the rice homologue of the yeast DMC1 gene essential for meiosis,” Sexual Plant Reproduction, vol. 13, no. 5, pp. 285–288, 2000. View at Publisher · View at Google Scholar · View at Scopus
  98. S. S. Metkar, J. K. Sainis, and S. K. Mahajan, “Cloning and characterization of the DMC1 genes in Oryza sativa,” Current Science, vol. 87, no. 3, pp. 353–357, 2004. View at Scopus
  99. T. Kobayashi, E. Kobayashi, S. Sato, et al., “Characterization of cDNAs induced in meiotic prophase in lily microsporocytes,” DNA Research, vol. 1, no. 1, pp. 15–26, 1994. View at Scopus
  100. M. Terasawa, A. Shinohara, Y. Hotta, H. Ogawa, and T. Ogawa, “Localization of RecA-like recombination proteins on chromosomes of the lily at various meiotic stages,” Genes and Development, vol. 9, no. 8, pp. 925–934, 1995. View at Scopus
  101. S. George, P. Behl, R. DeGuzman, et al., “Dmc1 fluorescent foci in prophase I nuclei of diploid, triploid and hybrid lilies,” Chromosoma, vol. 111, no. 2, pp. 96–105, 2002. View at Scopus
  102. F. Couteau, F. Belzile, C. Horlow, O. Grandjean, D. Vezon, and M.-P. Doutriaux, “Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis,” The Plant Cell, vol. 11, no. 9, pp. 1623–1634, 1999. View at Publisher · View at Google Scholar · View at Scopus
  103. Z. Y. Deng and T. Wang, “OsDMC1 is required for homologous pairing in Oryza sativa,” Plant Molecular Biology, vol. 65, no. 1-2, pp. 31–42, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  104. C. R. Kant, B. J. Rao, and J. K. Sainis, “DNA binding and pairing activity of OsDmc1, a recombinase from rice,” Plant Molecular Biology, vol. 57, no. 1, pp. 1–11, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  105. C. Rajanikant, M. Kumbhakar, H. Pal, B. J. Rao, and J. K. Sainis, “DNA strand exchange activity of rice recombinase OsDmc1 monitored by fluorescence resonance energy transfer and the role of ATP hydrolysis,” FEBS Journal, vol. 273, no. 7, pp. 1497–1506, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  106. I. Sakane, C. Kamataki, Y. Takizawa, et al., “Filament formation and robust strand exchange activities of the rice DMC1A and DMC1B proteins,” Nucleic Acids Research, vol. 36, no. 13, pp. 4266–4276, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  107. N. Y. Stassen, J. M. Logsdon Jr., G. J. Vora, H. H. Offenberg, J. D. Palmer, and M. E. Zolan, “Isolation and characterization of rad51 orthologs from Coprinus cinereus and Lycopersicon esculentum, and phylogenetic analysis of eukaryotic recA homologs,” Current Genetics, vol. 31, no. 2, pp. 144–157, 1997. View at Publisher · View at Google Scholar · View at Scopus
  108. A. E. Franklin, J. McElver, I. Sunjevaric, R. Rothstein, B. Bowen, and W. Z. Cande, “Three-dimensional microscopy of the Rad51 recombination protein during meiotic prophase,” The Plant Cell, vol. 11, no. 5, pp. 809–824, 1999. View at Publisher · View at Google Scholar · View at Scopus
  109. S. Ayora, J. I. Piruat, R. Luna, et al., “Characterization of two highly similar Rad51 homologs of Physcomitrella patens,” Journal of Molecular Biology, vol. 316, no. 1, pp. 35–49, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  110. U. Markmann-Mulisch, M. Z. Hadi, K. Koepchen, et al., “The organization of Physcomitrella patens RAD51 genes is unique among eukaryotic organisms,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 5, pp. 2959–2964, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  111. W. Li, C. Chen, U. Markmann-Mulisch, et al., “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, vol. 101, no. 29, pp. 10596–10601, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  112. K. Abe, K. Osakabe, S. Nakayama, et al., “Arabidopsis RAD51C gene is important for homologous recombination in meiosis and mitosis,” Plant Physiology, vol. 139, no. 2, pp. 896–908, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  113. J.-Y. Bleuyard, M. E. Gallego, F. Savigny, and C. I. White, “Differing requirements for the Arabidopsis Rad51 paralogs in meiosis and DNA repair,” The Plant Journal, vol. 41, no. 4, pp. 533–545, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  114. W. Li, X. Yang, Z. Lin, et al., “The AtRAD51C gene is required for normal meiotic chromosome synapsis and double-stranded break repair in Arabidopsis,” Plant Physiology, vol. 138, no. 2, pp. 965–976, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  115. K. Osakabe, K. Abe, H. Yamanouchi, et al., “Arabidopsis Rad51B is important for double-strand DNA breaks repair in somatic cells,” Plant Molecular Biology, vol. 57, no. 6, pp. 819–833, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  116. E. Dray, N. Siaud, E. Dubois, and M.-P. Doutriaux, “Interaction between Arabidopsis Brca2 and its partners Rad51, Dmc1, and Dss1,” Plant Physiology, vol. 140, no. 3, pp. 1059–1069, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  117. A. E. Franklin, I. N. Golubovskaya, H. W. Bass, and W. Z. Cande, “Improper chromosome synapsis is associated with elongated RAD51 structures in the maize desynaptic2 mutant,” Chromosoma, vol. 112, no. 1, pp. 17–25, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  118. W. P. Pawlowski, I. N. Golubovskaya, and W. Z. Cande, “Altered nuclear distribution of recombination protein RAD51 in maize mutants suggests the involvement of RAD51 in meiotic homology recognition,” The Plant Cell, vol. 15, no. 8, pp. 1807–1816, 2003. View at Publisher · View at Google Scholar · View at Scopus
  119. D. G. Schaefer and J.-P. Zryd, “Efficient gene targeting in the moss Physcomitrella patens,” The Plant Journal, vol. 11, no. 6, pp. 1195–1206, 1997. View at Publisher · View at Google Scholar · View at Scopus
  120. C. Rajanikant, M. Melzer, B. J. Rao, and J. K. Sainis, “Homologous recombination properties of OsRad51, a recombinase from rice,” Plant Molecular Biology, vol. 68, no. 4-5, pp. 479–491, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  121. A. Barzel and M. Kupiec, “Finding a match: how do homologous sequences get together for recombination?” Nature Reviews Genetics, vol. 9, no. 1, pp. 27–37, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus