PHS1 regulates meiotic recombination and homologous chromosome pairing by controlling the transport of RAD50 to the nucleus

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 47, 2009, Pages 20121-20126

  Ronceret, Arnaud ^a   Doutriaux, Marie Pascale ^b   Golubovskaya, Inna N ^c,d   Pawlowski, Wojciech P ^a  

^a Department of Obstetrics Gynecology   (United States)

^b INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d N I VAVILOV ALL RUSSIAN INSTITUTE OF PLANT GENETIC RESOURCES   (Russian Federation)

Author keywords

Chromosome pairing; Maize; Meiosis; Recombination

Indexed keywords

CYTOPLASM PROTEIN; GENE PRODUCT; PLANT DNA; POOR HOMOLOGOUS SYNAPSIS 1 PROTEIN; RAD50 PROTEIN; REPETITIVE DNA; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; CELL NUCLEUS; CENTROMERE; CHROMOSOME ARM; CHROMOSOME PAIRING; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; HOMOLOGOUS RECOMBINATION; MAIZE; MEIOSIS; MITOTIC RECOMBINATION; MOLECULAR INTERACTION; MOLECULAR SIZE; MUTANT; NONHUMAN; PLANT CHROMOSOME; PLANT GENOME; PRIORITY JOURNAL; PROPHASE; PROTEIN FUNCTION; PROTEIN TRANSPORT; WHEAT; YEAST;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL NUCLEUS; CENTROMERE; CHROMOSOME PAIRING; IN SITU HYBRIDIZATION, FLUORESCENCE; MEIOSIS; POINT MUTATION; PROTEIN TYROSINE PHOSPHATASES; RECOMBINATION, GENETIC; RNA INTERFERENCE; ZEA MAYS;

ARABIDOPSIS; MAMMALIA; TRITICUM AESTIVUM; ZEA MAYS;

EID: 73949130741     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0906273106     Document Type: Article

References (44)

1. Pawlowski WP, Cande WZ (2005) Coordinating the events of the meiotic prophase. Trends Cell Biol 15:674-681.
2. Pawlowski WP, et al. (2004) Coordination of meiotic recombination, pairing, and synapsis by PHS1. Science 303:89-92.
3. Zickler D, Kleckner N (1999) Meiotic chromosomes: Integrating structure and function. Annu Rev Genet 33:603-754.
4. Sanchez-Moran E, Santos JL, Jones GH, Franklin FC (2007) ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Genes Dev 21:2220-2233.
5. Waterworth WM, et al. (2007) NBS1 is involved in DNA repair and plays a synergistic role with ATM in mediating meiotic homologous recombination in plants. Plant J 52:41-52.
6. Borde V (2007) The multiple roles of the Mre11 complex for meiotic recombination. Chromosome Res 15:551-563.
7. Buis J, et al. (2008) Mre11 nuclease activity has essential roles in DNA repair and genomic stability distinct from ATM activation. Cell 135:85-96.
8. Hopfner KP, et al. (2002) The Rad50 zinc-hook is a structure joining Mre11 complexes in DNA recombination and repair. Nature 418:562-566.
9. Neale MJ, Keeney S (2006) Clarifying the mechanics of DNA strand exchange in meiotic recombination. Nature 442:153-158.
10. Bhalla N, Dernburg AF (2008) Prelude to a division. Annu Rev Cell Dev Biol 24:397-424.
11. Grelon M, Vezon D, Gendrot G, Pelletier G (2001) AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO J 20:589-600.
12. Stacey NJ, et al. (2006) Arabidopsis SPO11-2 functions with SPO11-1 in meiotic recombination. Plant J 48:206-216.
13. Bleuyard JY, Gallego ME, White CI (2004) Meiotic defects in the Arabidopsis rad50 mutant point to conservation of the MRX complex function in early stages of meiotic recombination. Chromosoma 113:197-203.
14. Puizina J, Siroky J, Mokros P, Schweizer D, Riha K (2004) Mre11 deficiency in Arabidopsis is associated with chromosomal instability in somatic cells and Spo11-dependent genome fragmentation during meiosis. Plant Cell 16:1968-1978.
15. Eggler AL, Inman RB, Cox MM (2002) The Rad51-dependent pairing of long DNA substrates is stabilized by replication protein A. J Biol Chem 277:39280-39288.
16. Rockmill B, Sym M, Scherthan H, Roeder GS (1995) Roles for two RecA homologs in promoting meiotic chromosome synapsis. Genes Dev 9:2684-2695.
17. Weiner BM, Kleckner N (1994) Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast. Cell 77:977-991.
18. Yoshida K, et al. (1998) The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis. Mol Cell 1:707-718.
19. Li W, et al. (2004) The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis. Proc Natl Acad Sci USA 101:10596-10601.
20. Li J, et al. (2007) Functional analysis of maizeRAD51in meiosis and double-strand break repair. Genetics 176:1469-1482.
21. Haberer G, et al. (2005) Structure and architecture of the maize genome. Plant Physiol 139:1612-1624.
22. Gaut BS, Doebley JF (1997) DNA sequence evidence for the segmental allotetraploid origin of maize. Proc Natl Acad Sci USA 94:6809-6814.
23. Simillion C, Vandepoele K, Van Montagu MC, Zabeau M, Van de Peer Y (2002) The hidden duplication past of Arabidopsis thaliana. Proc Natl Acad Sci USA 99:13627-13632.
24. Siaud N, et al. (2004) Brca2 is involved in meiosis in Arabidopsis thaliana as suggested by its interaction with Dmc1. EMBO J 23:1392-1401.
25. Kuromori T, et al. (2004)Acollection of 11 800 single-copy Ds transposon insertion lines in Arabidopsis. Plant J 37:897-905.
26. Armstrong SJ, Franklin FC, Jones GH (2001) Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana. J Cell Sci 114:4207-4217.
27. Armstrong SJ, Caryl AP, Jones GH, Franklin FC (2002) Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J Cell Sci 115:3645-3655.
28. Golubovskaya IN, et al. (2006) Alleles of afd1 dissect REC8 functions during meiotic prophase I. J Cell Sci 119:3306-3315.
29. Higgins JD, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FC (2005) The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev 19:2488-2500.
30. Xue Y, Zhou F, Fu C, Xu Y, Yao X (2006) SUMOsp: A web server for sumoylation site prediction. Nucleic Acids Res 34:W254-257.
31. de Carvalho CE, Colaiacovo MP (2006) SUMO-mediated regulation of synaptonemal complex formation during meiosis. Genes Dev 20:1986-1992.
32. Weil CF, Monde RA (2007) Induced mutations in maize. Israel J Plant Sci 55:183-190.
33. Lohmiller LD, et al. (2008) Cytological analysis of MRE11 protein during early meiotic prophase I in Arabidopsis and tomato. Chromosoma 117:277-288.
34. Desai-Mehta A, Cerosaletti KM, Concannon P (2001) Distinct functional domains of nibrin mediate Mre11 binding, focus formation, and nuclear localization. Mol Cell Biol 21:2184-2191.
35. 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.
36. Tsubouchi T, Roeder GS (2005) A synaptonemal complex protein promotes homologyindependent centromere coupling. Science 308:870-873.
37. Martinez-Perez E, Shaw P, Moore G (2001) The Ph1 locus is needed to ensure specific somatic and meiotic centromere association. Nature 411:204-207.
38. Tsubouchi T, Macqueen AJ, Roeder GS (2008) Initiation of meiotic chromosome synapsis at centromeres in budding yeast. Genes Dev 22:3217-3226.
39. Sanchez-Moran E, Jones GH, Franklin FC, Santos JL (2004) A puromycin-sensitive aminopeptidase is essential for meiosis in Arabidopsis thaliana. Plant Cell 16:2895-2909.
40. Schommer C, Beven A, Lawrenson T, Shaw P, Sablowski R (2003) AHP2 is required for bivalent formation and for segregation of homologous chromosomes in Arabidopsis meiosis. Plant J 36:1-11.
41. Maluszynska J, Heslop-Harrison JS (1991) Localization of tandemly repeated DNA sequences in Arabidopsis thaliana. Plant J 1:159-166.
42. Golubovskaya IN, Harper LC, Pawlowski WP, Schichnes D, Cande WZ (2002) The pam1 gene is required for meiotic bouquet formation and efficient homologous synapsis in maize (Zea mays, L.). Genetics 162:1979-1993.
43. Pawlowski WP, Golubovskaya IN, Cande WZ (2003) Altered nuclear distribution of recombination protein RAD51 in maize mutants suggests involvement of RAD51 in the meiotic homology recognition. Plant Cell 8:1807-1816.
44. Daoudal-Cotterell S, Gallego ME, White CI (2002) The plant Rad50-Mre11 protein complex. FEBS Lett 516:164-166.