The Kinesin AtPSS1 Promotes Synapsis and is Required for Proper Crossover Distribution in Meiosis

PLoS Genetics

Volumn 10, Issue 10, 2014, Pages

  Duroc, Yann ^a,b   Lemhemdi, Afef ^a,b   Larchevêque, Cécile ^a,b   Hurel, Aurélie ^a,b   Cuacos, Maria ^c   Cromer, Laurence ^a,b   Horlow, Christine ^a,b   Armstrong, Susan J ^c   Chelysheva, Liudmila ^a,b   Mercier, Raphael ^a,b  

^a INSTITUT JEAN PIERRE BOURGIN   (France)

^b AGROPARISTECH   (France)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPHASE; ARABIDOPSIS; ARTICLE; ATPSS1 GENE; CHROMOSOME PAIRING; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; GENE; GENE FREQUENCY; GENE INSERTION; GENE MUTATION; HETEROZYGOSITY; HOMEOSTASIS; HOMOZYGOSITY; IMMUNOLOCALIZATION; MEIOSIS; METAPHASE; NONHUMAN; PHENOTYPE; PROTEIN PROTEIN INTERACTION; SYNAPSE; GENETICS; METABOLISM; MICROTUBULE; MUTATION;

ARABIDOPSIS PROTEIN; ATPSS1 PROTEIN, ARABIDOPSIS; CELL CYCLE PROTEIN; ENDONUCLEASE; KINESIN; MUS81 PROTEIN, ARABIDOPSIS; REC8 PROTEIN, ARABIDOPSIS; ZYP1A PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL CYCLE PROTEINS; CHROMOSOME PAIRING; ENDONUCLEASES; KINESIN; MEIOSIS; MICROTUBULES; MUTATION;

EID: 84908341210     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004674     Document Type: Article

References (68)

1. Mézard C, Vignard J, Drouaud J, Mercier R, (2007) The road to crossovers: plants have their say. Trends Genet 23: 91–99 doi:10.1016/j.tig.2006.12.007
2. Youds JL, Boulton SJ, (2011) The choice in meiosis - defining the factors that influence crossover or non-crossover formation. J Cell Sci 124: 501–513 doi:10.1242/jcs.074427
3. Nagaoka SI, Hassold TJ, Hunt P, (2012) Human aneuploidy: mechanisms and new insights into an age-old problem. Nat Rev Genet 13: 493–504 doi:10.1038/nrg3245
4. Berchowitz LE, Copenhaver GP, (2010) Genetic interference: don't stand so close to me. Curr Genomics 11: 91–102 doi:10.2174/138920210790886835
5. Martini E, Diaz RL, Hunter N, Keeney S, (2006) Crossover homeostasis in yeast meiosis. Cell 126: 285–295 doi:10.1016/j.cell.2006.05.044
6. Yokoo R, Zawadzki KA, Nabeshima K, Drake M, Arur S, et al. (2012) COSA-1 Reveals Robust Homeostasis and Separable Licensing and Reinforcement Steps Governing Meiotic Crossovers. Cell 149: 75–87 doi:10.1016/j.cell.2012.01.052
7. Cole F, Kauppi L, Lange J, Roig I, Wang R, et al. (2012) Homeostatic control of recombination is implemented progressively in mouse meiosis. Nat Cell Biol 14: 424–430 doi:10.1038/ncb2451
8. Baudat F, Imai Y, de Massy B, (2013) Meiotic recombination in mammals: localization and regulation. Nat Rev Genet 14: 794–806 doi:10.1038/nrg3573
9. Drouaud J, Khademian H, Giraut L, Zanni V, Bellalou S, et al. (2013) Contrasted Patterns of Crossover and Non-crossover at Arabidopsis thaliana Meiotic Recombination Hotspots. PLoS Genet 9: e1003922 doi:10.1371/journal.pgen.1003922
10. De Massy B, (2013) Initiation of meiotic recombination: how and where? Conservation and specificities among eukaryotes. Annu Rev Genet 47: 563–599 doi:10.1146/annurev-genet-110711-155423
11. Gerton JL, Hawley RS, (2005) Homologous chromosome interactions in meiosis: diversity amidst conservation. Nat Rev Genet 6: 477–487 doi:10.1038/nrg1614
12. Vignard J, Siwiec T, Chelysheva L, Vrielynck N, Gonord F, et al. (2007) The interplay of RecA-related proteins and the MND1-HOP2 complex during meiosis in Arabidopsis thaliana. PLoS Genet 3: 1894–1906 doi:10.1371/journal.pgen.0030176
13. Couteau F, Belzile F, Horlow C, Grandjean O, Vezon D, et al. (1999) Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis. Plant Cell 11: 1623–1634.
14. De Muyt A, Pereira L, Vezon D, Chelysheva L, Gendrot G, et al. (2009) A high throughput genetic screen identifies new early meiotic recombination functions in Arabidopsis thaliana. PLoS Genet 5: e1000654 doi:10.1371/journal.pgen.1000654
15. Wijnker E, Velikkakam James G, Ding J, Becker F, Klasen JR, et al. (2013) The genomic landscape of meiotic crossovers and gene conversions in Arabidopsis thaliana. Elife 2: e01426 doi:10.7554/eLife.01426
16. Qi J, Wijeratne AJ, Tomsho LP, Hu Y, Schuster SC, et al. (2009) Characterization of meiotic crossovers and gene conversion by whole-genome sequencing in Saccharomyces cerevisiae. BMC Genomics 10: 475 doi:10.1186/1471-2164-10-475
17. Cifuentes M, Rivard M, Pereira L, Chelysheva L, Mercier R, (2013) Haploid meiosis in Arabidopsis: double-strand breaks are formed and repaired but without synapsis and crossovers. PLoS One 8: e72431 doi:10.1371/journal.pone.0072431
18. Osman K, Higgins JD, Sanchez-Moran E, Armstrong SJ, Franklin FCH, (2011) Pathways to meiotic recombination in Arabidopsis thaliana. New Phytol 190: 523–544 doi:10.1111/j.1469-8137.2011.03665.x
19. Harrison CJ, Alvey E, Henderson IR, (2010) Meiosis in flowering plants and other green organisms. J Exp Bot 61: 2863–2875 doi:10.1093/jxb/erq191
20. Cromie GA, Smith GR, (2007) Branching out: meiotic recombination and its regulation. Trends Cell Biol 17: 448–455 doi:10.1016/j.tcb.2007.07.007
21. Lynn A, Soucek R, Börner GV, (2007) ZMM proteins during meiosis: crossover artists at work. Chromosome Res 15: 591–605 doi:10.1007/s10577-007-1150-1
22. Crismani W, Girard C, Froger N, Pradillo M, Santos JL, et al. (2012) FANCM limits meiotic crossovers. Science (80-) 336: 1588–1590 doi:10.1126/science.1220381
23. Knoll A, Higgins JD, Seeliger K, Reha SJ, Dangel NJ, et al. (2012) The Fanconi anemia ortholog FANCM ensures ordered homologous recombination in both somatic and meiotic cells in Arabidopsis. Plant Cell 24: 1448–1464 doi:10.1105/tpc.112.096644
24. Koszul R, Kleckner NE, (2009) Dynamic chromosome movements during meiosis: a way to eliminate unwanted connections? Trends Cell Biol 19: 716–724 doi:10.1016/j.tcb.2009.09.007
25. Hiraoka Y, Dernburg AF, (2009) The SUN rises on meiotic chromosome dynamics. Dev Cell 17: 598–605 doi:10.1016/j.devcel.2009.10.014
26. Chikashige Y, Ding DQ, Funabiki H, Haraguchi T, Mashiko S, et al. (1994) Telomere-led premeiotic chromosome movement in fission yeast. Science 264: 270–273.
27. Chikashige Y, Tsutsumi C, Yamane M, Okamasa K, Haraguchi T, et al. (2006) Meiotic proteins bqt1 and bqt2 tether telomeres to form the bouquet arrangement of chromosomes. Cell 125: 59–69 doi:10.1016/j.cell.2006.01.048
28. Sato A, Isaac B, Phillips CM, Rillo R, Carlton PM, et al. (2009) Cytoskeletal forces span the nuclear envelope to coordinate meiotic chromosome pairing and synapsis. Cell 139: 907–919 doi:10.1016/j.cell.2009.10.039
29. Shibuya H, Ishiguro K-I, Watanabe Y, (2014) The TRF1-binding protein TERB1 promotes chromosome movement and telomere rigidity in meiosis. Nat Cell Biol 16: 145–156 doi:10.1038/ncb2896
30. Scherthan H, Weich S, Schwegler H, Heyting C, Härle M, et al. (1996) Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing. J Cell Biol 134: 1109–1125.
31. Sheehan MJ, Pawlowski WP, (2009) Live imaging of rapid chromosome movements in meiotic prophase I in maize. Proc Natl Acad Sci U S A 106: 20989–20994 doi:10.1073/pnas.0906498106
32. Scherthan H, (2001) A bouquet makes ends meet. Nat Rev Mol Cell Biol 2: 621–627 doi:10.1038/35085086
33. Chikashige Y, Haraguchi T, Hiraoka Y, (2007) Another way to move chromosomes. Chromosoma 116: 497–505 doi:10.1007/s00412-007-0114-8
34. Ding X, Xu R, Yu J, Xu T, Zhuang Y, et al. (2007) SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice. Dev Cell 12: 863–872 doi:10.1016/j.devcel.2007.03.018
35. Koszul R, Kim KP, Prentiss M, Kleckner NE, Kameoka S, (2008) Meiotic chromosomes move by linkage to dynamic actin cables with transduction of force through the nuclear envelope. Cell 133: 1188–1201 doi:10.1016/j.cell.2008.04.050
36. Zickler D, Kleckner NE, (1998) The leptotene-zygotene transition of meiosis. Annu Rev Genet 32: 619–697 doi:10.1146/annurev.genet.32.1.619
37. Roberts NY, Osman K, Armstrong SJ, (2009) Telomere distribution and dynamics in somatic and meiotic nuclei of Arabidopsis thaliana. Cytogenet Genome Res 124: 193–201 doi:10.1159/000218125
38. Zhou S, Wang Y, Li W, Zhao Z, Ren Y, et al. (2011) Pollen semi-sterility1 encodes a kinesin-1-like protein important for male meiosis, anther dehiscence, and fertility in rice. Plant Cell 23: 111–129 doi:10.1105/tpc.109.073692
39. Richardson DN, Simmons MP, Reddy ASN, (2006) Comprehensive comparative analysis of kinesins in photosynthetic eukaryotes. BMC Genomics 7: 18 doi:10.1186/1471-2164-7-18
40. Ross KJ, Fransz P, Jones GH, (1996) A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosom Res 4: 507–516.
41. Ferdous M, Higgins JD, Osman K, Lambing C, Roitinger E, et al. (2012) Inter-homolog crossing-over and synapsis in Arabidopsis meiosis are dependent on the chromosome axis protein AtASY3. PLoS Genet 8: e1002507 doi:10.1371/journal.pgen.1002507
42. Armstrong SJ, Caryl APP, Jones GH, Franklin FCH, (2002) Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J Cell Sci 115: 3645–3655 doi:10.1242/jcs.00048
43. Higgins JD, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FCH, (2005) The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev 19: 2488–2500 doi:10.1101/gad.354705
44. Chelysheva L, Vezon D, Belcram K, Gendrot G, Grelon M, (2008) The Arabidopsis BLAP75/Rmi1 homologue plays crucial roles in meiotic double-strand break repair. PLoS Genet 4: e1000309 doi:10.1371/journal.pgen.1000309
45. Motamayor JC, Vezon D, Bajon C, Sauvanet A, Grandjean O, et al. (2000) Switch (swi1), an Arabidopsis thaliana mutant affected in the female meiotic switch. Sex Plant Reprod 12: 209–218.
46. Berchowitz LE, Copenhaver GP, (2008) Fluorescent Arabidopsis tetrads: a visual assay for quickly developing large crossover and crossover interference data sets. Nat Protoc 3: 41–50 doi:10.1038/nprot.2007.491
47. Chelysheva L, Grandont L, Vrielynck N, le Guin S, Mercier R, et al. (2010) An easy protocol for studying chromatin and recombination protein dynamics during Arabidopsis thaliana meiosis: immunodetection of cohesins, histones and MLH1. Cytogenet Genome Res 129: 143–153 doi:10.1159/000314096
48. Chelysheva L, Vezon D, Chambon A, Gendrot G, Pereira L, et al. (2012) The Arabidopsis HEI10 is a new ZMM protein related to Zip3. PLoS Genet 8: e1002799 doi:10.1371/journal.pgen.1002799
49. Higgins JD, Buckling EF, Franklin FCH, Jones GH, (2008) Expression and functional analysis of AtMUS81 in Arabidopsis meiosis reveals a role in the second pathway of crossing-over. Plant J 54: 152–162 doi:10.1111/j.1365-313X.2008.03403.x
50. Berchowitz LE, Francis KE, Bey AL, Copenhaver GP, (2007) The role of AtMUS81 in interference-insensitive crossovers in A. thaliana. PLoS Genet 3: e132 doi:10.1371/journal.pgen.0030132
51. Endow Sa, Kull FJ, Liu H, (2010) Kinesins at a glance. J Cell Sci 123: 3420–3424 doi:10.1242/jcs.064113
52. Zhou X, Graumann K, Evans DE, Meier I, (2012) Novel plant SUN-KASH bridges are involved in RanGAP anchoring and nuclear shape determination. J Cell Biol 196: 203–211 doi:10.1083/jcb.201108098
53. Wickstead B, Gull K, (2007) Dyneins across eukaryotes: a comparative genomic analysis. Traffic 8: 1708–1721 doi:10.1111/j.1600-0854.2007.00646.x
54. Tessé S, Storlazzi A, Kleckner NE, Gargano S, Zickler D, (2003) Localization and roles of Ski8p protein in Sordaria meiosis and delineation of three mechanistically distinct steps of meiotic homolog juxtaposition. Proc Natl Acad Sci U S A 100: 12865–12870 doi:10.1073/pnas.2034282100
55. Storlazzi A, Gargano S, Ruprich-Robert G, Falque M, David M, et al. (2010) Recombination proteins mediate meiotic spatial chromosome organization and pairing. Cell 141: 94–106 doi:10.1016/j.cell.2010.02.041
56. Thacker D, Mohibullah N, Zhu X, Keeney S, (2014) Homologue engagement controls meiotic DNA break number and distribution. Nature 510: 241–246 doi:10.1038/nature13120
57. Kim KP, Weiner BM, Zhang L, Jordan A, Dekker J, et al. (2010) Sister cohesion and structural axis components mediate homolog bias of meiotic recombination. Cell 143: 924–937 doi:10.1016/j.cell.2010.11.015
58. Lee C-Y, Conrad MN, Dresser ME, (2012) Meiotic chromosome pairing is promoted by telomere-led chromosome movements independent of bouquet formation. PLoS Genet 8: e1002730 doi:10.1371/journal.pgen.1002730
59. Uanschou C, Ronceret A, Von Harder M, De Muyt A, Vezon D, et al. (2013) Sufficient amounts of functional HOP2/MND1 complex promote interhomolog DNA repair but are dispensable for intersister DNA repair during meiosis in Arabidopsis. Plant Cell 25: 4924–4940 doi:10.1105/tpc.113.118521
60. Kleckner NE, Zickler D, Jones GH, Dekker J, Padmore R, et al. (2004) A mechanical basis for chromosome function. Proc Natl Acad Sci U S A 101: 12592–12597 doi:10.1073/pnas.0402724101
61. Zhang L, Liang Z, Hutchinson J, Kleckner NE, (2014) Crossover Patterning by the Beam-Film Model: Analysis and Implications. PLoS Genet 10: e1004042 doi:10.1371/journal.pgen.1004042
62. Higgins JD, Vignard J, Mercier R, Pugh AG, Franklin FCH, et al. (2008) AtMSH5 partners AtMSH4 in the class I meiotic crossover pathway in Arabidopsis thaliana, but is not required for synapsis. Plant J 55: 28–39 doi:10.1111/j.1365-313X.2008.03470.x
63. Chelysheva L, Gendrot G, Vezon D, Doutriaux M-P, Mercier R, et al. (2007) Zip4/Spo22 is required for class I CO formation but not for synapsis completion in Arabidopsis thaliana. PLoS Genet 3: e83 doi:10.1371/journal.pgen.0030083
64. Francis Lam SY, Harrison BD, Bey AL, Berchowitz LE, et al. (2007) Pollen tetrad-based visual assay for meiotic recombination in Arabidopsis. Proc Natl Acad Sci U S A 104: 3913–3918 doi:10.1073/pnas.0608936104
65. Cromer L, Jolivet S, Horlow C, Chelysheva L, Heyman J, et al. (2013) Centromeric cohesion is protected twice at meiosis, by SHUGOSHINs at anaphase I and by PATRONUS at interkinesis. Curr Biol 23: 2090–2099 doi:10.1016/j.cub.2013.08.036
66. Voinnet O, Rivas S, Mestre P, Baulcombe D, (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J 33: 949–956.
67. Perkins DD, (1949) Biochemical Mutants in the Smut Fungus Ustilago Maydis. Genetics 34: 607–626.
68. Alexander MP, (1969) Differential staining of aborted and nonaborted pollen. Stain Technol 44: 117–122.