Expression and functional analysis of AtMUS81 in Arabidopsis meiosis reveals a role in the second pathway of crossing-over

Plant Journal

Volumn 54, Issue 1, 2008, Pages 152-162

  Higgins, James D ^a   Buckling, Ewen F ^a   Franklin, F Chris H ^a   Jones, Gareth H ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

Arabidopsis; Chiasmata; Expression; Meiosis; MUS81; Recombination

Indexed keywords

ARABIDOPSIS; CHIASMATA; MEIOSIS; MEIOTIC CROSSOVERS;

CHROMOSOMES; CYTOLOGY; DNA; PLANTS (BOTANY); PROTEINS;

GENE EXPRESSION;

ARABIDOPSIS PROTEIN; ENDONUCLEASE; MSH4 PROTEIN, ARABIDOPSIS; MUS81 PROTEIN, ARABIDOPSIS; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; CROSSING OVER; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MEIOSIS; METABOLISM; MUTATION; PHYSIOLOGY; PLANT CHROMOSOME; PROTEIN TRANSPORT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHROMOSOMES, PLANT; CROSSING OVER, GENETIC; ENDONUCLEASES; GENE EXPRESSION REGULATION, PLANT; MEIOSIS; MUTATION; PROTEIN TRANSPORT;

ARABIDOPSIS; SCHIZOSACCHAROMYCETACEAE;

EID: 40949119007     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2008.03403.x     Document Type: Article

References (43)

1. Allers, T. Lichten, M. (2001) Differential timing and control of noncrossover and crossover recombination during meiosis. Cell, 106, 47 57.
2. Argueso, J.L., Wanat, J., Gemici, Z. Alani, E. (2004) Competing crossover pathways act during meiosis in Saccharomyces cerevisiae. Genetics, 168, 1805 1816.
3. Armstrong, S.J., Franklin, F.C.H. Jones, G.H. (2001) Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana. J. Cell Sci. 114, 4207 4217.
4. Armstrong, S.J., Caryl, A.P., Jones, G.H. Franklin, F.C.H. (2002) Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J. Cell Sci. 115, 3645 3655.
5. Armstrong, S.J., Franklin, F.C.H. Jones, G.H. (2003) A meiotic time-course for Arabidopsis. Sex. Plant Reprod. 16, 141 149.
6. Berchowitz, L.E., Francis, K.E., Bey, A.L. Copenhaver, G.P. (2007) The role of AtMUS81 in interference-insensitive crossovers in A. thaliana. PLOS Genet. 3, 1355 1364.
7. Boddy, M.N., Lopez-Girona, A., Shanahan, P., Interthal, H., Heyer, W.D. Russel, P. (2000) Damage tolerance protein Mus81 associates with the FHA1 domain of checkpoint kinase Cds1. Mol. Cell. Biol. 20, 8758 8766.
8. Borner, G.V., Kleckner, N. Hunter, N. (2004) Crossover/noncrossover differentiation, synaptonemal complex formation and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell, 117, 29 45.
9. Church, G.M. Gilbert, W. (1984) Genomic sequencing. Proc. Natl Acad. Sci. USA, 81, 1991 1995.
10. Crombie, G.A., Hyppa, R.W., Taylor, A.F., Zakharyevich, K., Hunter, N. Smith, G.R. (2006) Single Holliday junctions are intermediates of meiotic recombination. Cell, 127, 1167 1178.
11. Darlington, C.D. (1939) The Evolution of Genetic Systems. Edinburgh and London : Oliver and Boyd.
12. Dubest, S., Gallego, M.E. White, C.I. (2002) Role of the AtRad1p endonuclease in homologous recombination in plants. EMBO Rep. 3, 1049 1054.
13. Feinberg, A.P. Vogelstein, B. (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132, 6 13.
14. Feinberg, A.P. Vogelstein, B. (1984) Addendum: a technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 137, 266 267.
15. Gao, H., Chen, X.-B. McGowan, C.H. (2003) Mus81 endonuclease localizes to nucleoli and to regions of DNA damage in human S-phase cells. Mol. Biol. Cell, 14, 4826 4834.
16. Guillon, H., Baudat, F., Grey, C., Liskay, R.M. de Massy, B. (2005) Crossover and noncrossover pathways in mouse meiosis. Mol. Cell, 20, 563 573.
17. Haber, J.E. Heyer, W.D. (2001) The fuss about Mus81. Cell, 107, 551 554.
18. Hartung, F., Suer, S., Bergmann, T. Puchta, H. (2006) The role of AtMUS81 in DNA repair and its genetic interaction with the helicase AtRECQl4A. Nucleic Acids Res. 34, 4438 4448.
19. Hartung, F., Suer, S. Puchta, H. (2007) Two closely related RecQ helicases have antagonistic roles in homologous recombination and DNA repair in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 104, 18836 18841.
20. Hawley, R.S. (1988) Exchange and chromosome segregation in eukaryotes. In Genetic Recombination (Kucherlapati, R. Smith, G.R., eds). Washington DC : American Society for Microbiology, pp. 497 528.
21. Higgins, J.D., Armstrong, S.J., Franklin, F.C.H. Jones, G.H. (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.
22. Higgins, J.D., Sanchez-Moran, E., Armstrong, S.J., Jones, G.H. Franklin, F.C.H. (2005) The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev. 19, 2488 2500.
23. Hillers, K.J. Villeneuve, A.M. (2003) Chromosome-wide control of meiotic crossing over in C. elegans. Curr. Biol. 13, 1641 1647.
24. Hollingsworth, N.M. Brill, S.J. (2004) The Mus81 solution to resolution: generating meiotic crossovers without Holliday junctions. Genes Dev. 18, 117 125.
25. Interthal, H. Heyer, W.D. (2000) MUS81 encodes a novel helix-hairpin-helix protein involved in the response to UV- and methylation-induced DNA damage in Saccharomyces cerevisiae. Mol. Gen. Genet. 263, 812 827.
26. Jessop, L., Rockmill, B., Roeder, G.S. Lichten, M. (2006) Meiotic chromosome synapsis-promoting proteins antagonize the anti-crossover activity of Sgs1. PLoS Genet. 2, 1402 1412.
27. Kakeda, K., Jordan, N.D., Conner, A., Ride, J.P., Franklin-Tong, V.E. Franklin, F.C.H. (1998) Identification of residues in a hydrophilic loop of the Papaver rhoeas S protein that play a crucial role in recognition of incompatible pollen. Plant Cell, 10, 1723 1731.
28. Lancaster, H.O. (1966) The Chi-Squared Distribution. New York, NY : John Wiley and Sons.
29. Lhuissier, F.G.P., Offenberg, H.H., Wittich, P.E., Vischer, N.O.E. Heyting, C. (2007) The mismatch repair protein MLH1 marks a subset of strongly interfering crossovers in tomato. Plant Cell, 19, 862 876.
30. McPherson, J.P., Lemmers, B., Chahwan, R. et al. (2004) Involvement of mammalian Mus81 in genome integrity and tumor suppression. Science, 304, 1822 1826.
31. Mercier, R., Armstrong, S.J., Horlow, C., Jackson, N.P., Makaroff, C.A., Vezon, D., Pelletier, G., Jones, G.H. Franklin, F.C.H. (2003) The meiotic protein Swi1 is required for axial element formation and recombination initiation in Arabidopsis thaliana. Development, 130, 3309 3318.
32. Mercier, R., Jolivet, S., Vezon, D. et al. (2005) Two meiotic crossover classes cohabit in Arabidopsis: one is dependent on MER3, whereas the other one is not. Curr. Biol. 15, 692 701.
33. Mullen, J.R., Kaliraman, V., Ibrahim, S.S. Brill, S.J. (2001) Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. Genetics, 157, 103 118.
34. Osman, F., Dixon, J., Doe, C.L. Whitby, M.C. (2003) Generating crossovers by resolution of nicked Holliday junctions: a role for Mus81-Eme1 in meiosis. Mol. Cell, 12, 761 774.
35. Ross, K.J., Fransz, P. Jones, G.H. (1996) A light microscope atlas of meiosis in Arabidopsis thaliana. Chromosome Res. 4, 507 516.
36. de los Santos, T., Hunter, N., Lee, C., Larkin, B., Loidl, J. Hollingsworth, N.M. (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.
37. Smith, K.N. Nicholas, A. (1998) Recombination at work for meiosis. Curr. Opin. Genet. Dev. 8, 200 211.
38. Stacey, N.J., Kuromori, Y., Azumi, G., Roberts, C., Breuer, C., Wada, T., Maxwell, A., Roberts, K. Sugimoto-Shirasu, K. (2006) Arabidopsis SPO11-2 functions with SPO11-1 in meiotic recombination. Plant J. 48, 206 216.
39. Szostak, J.W., Orr-Weaver, T.L., Rothstein, R.J. Stahl, F.W. (1983) The double-strand-break repair model for recombination. Cell, 33, 25 35.
40. Terasawa, M., Ogawa, H., Tsukamoto, Y., Shinohara, M., Shirahige, K., Kleckner, N. Ogawa, T. (2007) Meiotic recombination-related DNA synthesis and its implications for cross-over and non-cross-over recombinant formation. Proc. Natl Acad. Sci. USA, 104, 5965 5970.
41. Visintin, R. Amon, A. (2000) The nucleolus: the magician's hat for cell cycle tricks. Curr. Opin. Cell Biol. 12, 372 377.
42. Whitby, M.C. (2005) Making crossovers during meiosis. Bioch. Soc. Trans. 33, 1451 1455.
43. Zimmerman, P., Hirsch-Hoffmann, M., Hennig, L. Gruissen, W. (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621 2632.