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Caenorhabditis elegans Ce-rdh-1/rad-51 functions after double-strand break formation of meiotic recombination

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Abstract

During meiotic prophase 1, homologous recombination is accompanied by dynamic chromosomal changes. The Ce-rdh-1/rad-51 gene is the only bacterial recA-like gene in the nematode C. elegans genome. Upon depletion of Ce-rdh-1/rad-51 using the RNA interference method, abnormal ‘kinked’ chromosomes can be observed in mature oocytes at diakinesis, whereas synapsis between homologous chromosomes during the pachytene stage is normal. Following fertilization, Ce-rdh-1/rad-51-depleted embryos die early in embryogenesis, and their nuclei exhibit abnormal chromosome fragments and bridges. From epistasis analyses with Ce-spo-11 defective mutant and ionizing radiation, it is indicated that Ce-rdh-1/rad-51 functions after double-strand break (DSB) formation of meiotic recombination. Under the Ce-chk-2 defective condition, whose meiotic synapsis and meiotic recombination between homologous chromosomes are completely inhibited, the Ce-rdh-1/rad51 is normally expressed in the gonadal cells. Moreover, it seems that exogenous DSBs in the Ce-chk-2 defective nuclei at the pachytene stage can be repaired between sister chromatids in a Ce-rdh-1/rad-51-dependent manner. These results indicate that Ce-rdh-1/rad51 functions after both endogenous and exogenous DSB formation during meiosis, but not as ‘pairing centers’ for meiotic synapsis.

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References

  • Bailis JM, Roeder GS (1998) Synaptonemal complex morphogenesis and sister-chromatid cohesion require Mek1-dependent phosphorylation of a meiotic chromosomal protein. Genes Dev 12: 3551-3563.

    Google Scholar 

  • Bascom-Slack CA, Ross LO, Dawson DS (1997) Chiasmata, crossovers, and meiotic chromosome segregation. Adv Genet 35: 253-284.

    Google Scholar 

  • Baudat F, Manova K, Yuen JP, Jasin M, Keeney S (2000) Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Mol Cell 6: 989-998.

    Google Scholar 

  • Bullard SA, Kim S, Galbraith AM, Malone RE (1996) Double strand breaks at the HIS2 recombination hot spot in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 93: 13054-13059.

    Google Scholar 

  • Cao L, Alani E, Kleckner N (1990) A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell 61: 1089-1101.

    Google Scholar 

  • Chin GM, Villeneuve AM (2001) C. elegans mre-11 is required for meioticrecombination and DNA repair but is dispensable for the meiotic G(2) DNA damage checkpoint. Genes Dev 15: 522-534.

    Google Scholar 

  • Cummings WJ, Zolan ME (1998) Functions of DNA repair genes during meiosis. Curr Top Dev Biol 37: 117-140.

    Google Scholar 

  • de Massy B, Rocco V, Nicolas A (1995) The nucleotide mapping of DNA double-strand breaks at the CYS3 initiation site of meiotic recombination in Saccharomyces cerevisiae. EMBO J 14: 4589-4598.

    Google Scholar 

  • Dernburg AF, McDonald K, Moulder G, Barstead R, Dresser M, Villeneuve AM (1998) Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94: 387-398.

    Google Scholar 

  • Diaz RL, Alcid AD, Berger JM, Keeney S (2002) Identification of residues in yeast Spo11p critical for meiotic DNA double-strand break formation. Mol Cell Biol 22: 1106-1115.

    Google Scholar 

  • Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-strandedRNAin Caenorhabditis elegans. Nature 391: 806-811.

    Google Scholar 

  • Gupta RC, Golub E, Bi B, Radding CM (2001) The synaptic activity of HsDmc1, a human recombination protein specific to meiosis. Proc Natl Acad Sci USA 98: 8433-8439.

    Google Scholar 

  • Higashitani A, Aoki H, Mori A, Sasagawa Y, Takanami T, Takahashi H (2000) Caenorhabditis elegans Chk2-like gene is essential for meiosis but dispensable for DNA repair. FEBS Lett 485: 35-39.

    Google Scholar 

  • Hong EL, Shinohara A, Bishop DK (2001) Saccharomyces cerevisiae Dmc1 protein promotes renaturation of single-strand DNA (ssDNA) and assimilation of ssDNA into homologous super-coiled duplex DNA. J Biol Chem 276: 41906-41912.

    Google Scholar 

  • Hubbard EJ, Greenstein D (2000) The Caenorhabditis elegans gonad: a test tube for cell and developmental biology. Dev Dyn 218: 2-22.

    Google Scholar 

  • Keeney S (2001) Mechanism and control of meiotic recombination initiation. Curr Top Dev Biol 52: 1-53.

    Google Scholar 

  • 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.

    Google Scholar 

  • Kleckner N (1996) Meiosis: how could it work? Proc Natl Acad Sci USA 93: 8167-8174.

    Google Scholar 

  • Lewis JA, Fleming JT (1995) Basic culture methods. Meth Cell Biol 48: 3-29.

    Google Scholar 

  • Li Z, Golub EI, Gupta R, Radding CM (1997) Recombination activities of HsDmc1 protein, the meiotic human homolog of RecA protein. Proc Natl Acad Sci USA 94: 11221-11226.

    Google Scholar 

  • Loidl J, Klein F, Scherthan H (1994) Homologous pairing is reduced but not abolished in asynaptic mutants of yeast. J Cell Biol 125: 1191-1200.

    Google Scholar 

  • MacQueen AJ, Villeneuve AM (2001) Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2. Genes Dev 15: 1674-1687.

    Google Scholar 

  • Masson JY, West SC (2001) The Rad51 and Dmc1 recombinases: a non-identical twin relationship. Trends Biochem Sci 26: 131-136.

    Google Scholar 

  • McKim KS, Hayashi-Hagihara A (1998) mei-W68 in Drosophila melanogaster encodes a Spo11 homolog: evidence that the mechanism for initiating meiotic recombination is conserved. Genes Dev 12: 2932-2942.

    Google Scholar 

  • Mitchell A (2001) Meiosis: Synapsis spoilt. Nat Rev Mol Cell Biol 2: 5.

    Google Scholar 

  • Moens RB (ed.) (1987) In: Meiosis.Orlando, Florida: Academic Press, 1-391.

    Google Scholar 

  • Molnar M, Bahler J, Kohli J, Hiraoka Y (2001) Live observation of fission yeast meiosis in recombination-deficient mutants: a study on achiasmate chromosome segregation. J Cell Sci 114: 2843-2853.

    Google Scholar 

  • Nairz K, Klein F (1997) mre11S —a yeast mutation that blocks double-strand-break processing and permits nonhomologous synapsis in meiosis. Genes Dev 11: 2272-2290.

    Google Scholar 

  • Oishi I, Iwai K, Kagohashi Y et al.(2001) Critical role of Caenorhabditis elegans homologs of Cds1 (Chk2)-related kinases in meiotic recombination. Mol Cell Biol 21: 1329-1335.

    Google Scholar 

  • Pasierbek P, Jantsch M, Melcher M, Schleiffer A, Schweizer D, Loidl J (2001) A Caenorhabditis elegans cohesion protein with functions in meiotic chromosome pairing and disjunction. Genes Dev 15: 1349-1360.

    Google Scholar 

  • Pittman DL, Cobb J, Schimenti KJ et al.(1998) Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. Mol Cell 1: 697-705. 134 Takako Takanami et al.

    Google Scholar 

  • Rinaldo C, Ederle S, Rocco V, La Volpe A (1998) The Caenorhabditis elegans RAD51 homolog is transcribed into two alternative mRNAs potentially encoding proteins of different sizes. Mol Gen Genet 260: 289-294.

    Google Scholar 

  • Rinaldo C, Bazzicalupo P, Ederle S, Hilliard M, La Volpe A (2002) Roles for Caenorhabditis elegans rad-51 in meiosis and in resistance to ionizing radiation during development. Genetics 160: 471-479.

    Google Scholar 

  • Roeder GS (1997) Meiotic chromosomes: it takes two to tango. Genes Dev 11: 2600-2621.

    Google Scholar 

  • Romanienko PJ, Camerini-Otero RD (2000) The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol Cell 6: 975-987.

    Google Scholar 

  • Schedl T (1997) Developmental genetics of the germ line.In: Riddle DL, Blumenthal T, Meyer BJ, Priess JR, eds. C. ELEGANS II.Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press, pp 241-270.

    Google Scholar 

  • Shinohara A, Ogawa T (1995) Homologous recombination and the roles of double-strand breaks. Trends Biochem Sci 20: 387-391.

    Google Scholar 

  • Shinohara A, Ogawa T (1998) Stimulation by Rad52 of yeast Rad51-mediated recombination. Nature 391: 404-407.

    Google Scholar 

  • Shinohara A, Gasior S, Ogawa T, Kleckner N, Bishop DK (1997) Saccharomyces cerevisiae recA homologues RAD51 and DMC1 have both distinct and overlapping roles in meiotic recombination. Genes Cells 2: 615-629.

    Google Scholar 

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

    Google Scholar 

  • Takanami T, Sato S, Ishihara T, Katsura I, Takahashi H, Higashitani A (1998) Characterization of a Caenorhabditis elegans recA-like gene Ce-rdh-1 involved in meiotic recombination. DNA Res 5: 373-377.

    Google Scholar 

  • Takanami T, Mori A, Takahashi H, Higashitani A (2000) Hyper-resistance of meiotic cells to radiation due to a strong expression of a single recA-like gene in Caenorhabditis elegans. Nucleic Acids Res 28: 4232-4236.

    Google Scholar 

  • Tsubouchi H, Ogawa H (2000) Exo1 roles for repair of DNA double-strand breaks and meiotic crossing over in Saccharomyces cerevisiae. Mol Biol Cell 11: 2221-2233.

    Google Scholar 

  • 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.

    Google Scholar 

  • Zetka MC, Kawasaki I, Strome S, Muller F (1999) Synapsis and chiasma formation in Caenorhabditis elegans require HIM-3, a meiotic chromosome core component that functions in chromosome segregation. Genes Dev 13: 2258-2270.

    Google Scholar 

  • Zickler D, Kleckner N (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33: 603-754.

    Google Scholar 

Download references

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Correspondence to Atsushi Higashitani.

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Takanami, T., Mori, A., Takahashi, H. et al. Caenorhabditis elegans Ce-rdh-1/rad-51 functions after double-strand break formation of meiotic recombination. Chromosome Res 11, 125–135 (2003). https://doi.org/10.1023/A:1022863814686

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