Haploid Meiosis in Arabidopsis: Double-Strand Breaks Are Formed and Repaired but Without Synapsis and Crossovers

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Cifuentes, Marta ^a   Rivard, Maud ^a   Pereira, Lucie ^a   Chelysheva, Liudmila ^a   Mercier, Raphael ^a  

^a INSTITUT JEAN PIERRE BOURGIN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DMC1 PROTEIN; RAD51 PROTEIN; REC8 PROTEIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ANAPHASE; ARABIDOPSIS THALIANA; ARTICLE; CHROMOSOME CHIASM; CHROMOSOME PAIRING; CONTROLLED STUDY; CROSSING OVER; DIPLOIDY; DOUBLE STRANDED DNA BREAK; GAMETE; GENOTYPE; HAPLOIDY; MALE PLANT; MEIOSIS; METAPHASE; MITOSIS; NONHUMAN; PLANT CHROMOSOME; PLANT REPRODUCTION; PROTEIN LOCALIZATION; SISTER CHROMATID; WILD TYPE;

ADENOSINE TRIPHOSPHATASES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL CYCLE PROTEINS; CHROMOSOME PAIRING; CROSSING OVER, GENETIC; DIPLOIDY; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; FERTILITY; HAPLOIDY; INDOLES; MEIOSIS; MITOSIS; MUTATION; POLLEN; RAD51 RECOMBINASE; REC A RECOMBINASES; STAINING AND LABELING;

EID: 84881350952     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072431     Document Type: Article

References (60)

1. Marston AL, Amon A, (2004) Meiosis: cell-cycle controls shuffle and deal. Nat Rev Mol Cell Biol 5: 983-997. doi:10.1038/nrm1526. PubMed: 15573136.
2. Phadnis N, Hyppa RW, Smith GR, (2011) New and old ways to control meiotic recombination. Trends Genet TIG 27: 411-421. doi:10.1016/j.tig.2011.06.007. PubMed: 21782271.
3. 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. PubMed: 21282472.
4. Zickler D, (2006) From early homologue recognition to synaptonemal complex formation. Chromosoma 115: 158-174. doi:10.1007/s00412-006-0048-6. PubMed: 16570189.
5. 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. PubMed: 12186950.
6. 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. PubMed: 22319460.
7. 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. PubMed: 16230536.
8. 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. PubMed: 21366595.
9. Mercier R, Jolivet S, Vezon D, Huppe E, Chelysheva L, 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. doi:10.1016/j.cub.2005.02.056. PubMed: 15854901.
10. Higgins JD, Armstrong SJ, Franklin FCH, Jones GH, (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. doi:10.1101/gad.317504. PubMed: 15489296.
11. Börner GV, 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. doi:10.1016/S0092-8674(04)00292-2. PubMed: 15066280.
12. Wang M, Wang K, Tang D, Wei C, Li M, et al. (2010) The central element protein ZEP1 of the synaptonemal complex regulates the number of crossovers during meiosis in rice. Plant Cell 22: 417-430. doi:10.1105/tpc.109.070789. PubMed: 20154151.
13. Goldfarb T, Lichten M, (2010) Frequent and Efficient Use of the Sister Chromatid for DNA Double-Strand Break Repair during Budding Yeast Meiosis. PLOS Biol 8: e1000520. doi:10.1371/journal.pbio.1000520. PubMed: 20976044.
14. Pradillo M, Santos JL, (2011) The template choice decision in meiosis: is the sister important? Chromosoma 120: 447-454. doi:10.1007/s00412-011-0336-7. PubMed: 21826413.
15. Germanà MA, (2011) Gametic embryogenesis and haploid technology as valuable support to plant breeding. Plant Cell Rep 30: 839-857. doi:10.1007/s00299-011-1061-7. PubMed: 21431908.
16. Ravi M, Chan SWL, (2010) Haploid plants produced by centromere-mediated genome elimination. Nature 464: 615-618. doi:10.1038/nature08842. PubMed: 20336146.
17. Jenczewski E, Eber F, Grimaud A, Huet S, Lucas MO, et al. (2003) PrBn, a major gene controlling homeologous pairing in oilseed rape (Brassica napus) haploids. Genetics 164: 645-653. PubMed: 12807785.
18. Wagstaff JE, Klapholz S, Esposito RE, (1982) Meiosis in haploid yeast. Proc Natl Acad Sci U S A 79: 2986-2990. doi:10.1073/pnas.79.9.2986. PubMed: 7045878.
19. Cervantes MD, Farah JA, Smith GR, (2000) Meiotic DNA breaks associated with recombination in S. pombe. Mol Cell 5: 883-888. doi:10.1016/S1097-2765(00)80328-7. PubMed: 10882124.
20. Callender TL, Hollingsworth NM, (2010) Mek1 suppression of meiotic double-strand break repair is specific to sister chromatids, chromosome autonomous and independent of Rec8 cohesin complexes. Genetics 185: 771-782. doi:10.1534/genetics.110.117523. PubMed: 20421598.
21. De Massy B, Baudat F, Nicolas a (1994) Initiation of recombination in Saccharomyces cerevisiae haploid meiosis. Proc Natl Acad Sci U S A 91: 11929-11933. doi:10.1073/pnas.91.25.11929. PubMed: 7991559.
22. Voelkel-Meiman K, Moustafa SS, Lefrançois P, Villeneuve AM, MacQueen AJ, (2012) Full-length synaptonemal complex grows continuously during meiotic prophase in budding yeast. PLOS Genet 8: e1002993. doi:10.1371/journal.pgen.1002993. PubMed: 23071451.
23. Loidl J, Nairz K, Klein F, (1991) Meiotic chromosome synapsis in a haploid yeast. Chromosoma 100: 221-228. doi:10.1007/BF00344155. PubMed: 2055133.
24. Loidl J, Nairz K, (1997) Karyotype variability in yeast caused by nonallelic recombination in haploid meiosis. Genetics 146: 79-88. PubMed: 9136002.
25. Gillies CB, (1974) The nature and extent of synaptonemal complex formation in haploid barley. Chromosoma 48: 441-453. doi:10.1007/BF00290998.
26. Sadasivaiah R, Kasha K, (1971) Meiosis in haploid barley-an interpretation of non-homologous chromosome associations. Chromosoma 263: 247-263.
27. Armstrong K, Keller W, (1982) CHROMOSOME PAIRING IN HAPLOIDS OF BRASSICA OLERACEA. Can J Genet Cytol 24: 735-739. doi:10.1139/g82-079.
28. Armstrong K, Keller W, (1981) Chromosome pairing in haploids of Brassica campestris. Theor Appl Genet 52: 49-52.
29. Santos J, Jimenez M, Diez M, (1994) Meiosis in haploid rye: extensive synapsis and low chiasma frequency. Heredity 73: 580-588. doi:10.1038/hdy.1994.165.
30. Gong Z, Liu X, Tang D, Yu H, Yi C, et al. (2011) Non-homologous chromosome pairing and crossover formation in haploid rice meiosis. Chromosoma 120: 47-60. doi:10.1007/s00412-010-0288-3. PubMed: 20706730.
31. Martinez M, Cuadrado C, Laurie DA, Romero C, (2005) Synaptic behaviour of hexaploid wheat haploids with different effectiveness of the diploidizing mechanism. Cytogenet Genome Res 109: 210-214. doi:10.1159/000082402. PubMed: 15753579.
32. Jauhar PP, Almouslem TS, Peterson TS, Joppa LR, (1999) Inter- and intragenomic chromosome pairing in haploids of durum wheat. J Hered 90: 437-445. doi:10.1093/jhered/90.4.437.
33. Cifuentes M, Eber F, Lucas M-O, Lode M, Chèvre A-M, et al. (2010) Repeated polyploidy drove different levels of crossover suppression between homoeologous chromosomes in Brassica napus allohaploids. Plant Cell 22: 2265-2276. doi:10.1105/tpc.109.072991. PubMed: 20639447.
34. Cifuentes M, Grandont L, Moore G, Chèvre AM, Jenczewski E, (2010) Genetic regulation of meiosis in polyploid species: new insights into an old question. New Phytol 186: 29-36. doi:10.1111/j.1469-8137.2009.03084.x. PubMed: 19912546.
35. De Muyt A, Mercier R, Mézard C, Grelon M, (2009) Meiotic recombination and crossovers in plants. Genome Dynam 5: 14-25. doi:10.1159/000166616. PubMed: 18948704.
36. Mercier R, Grelon M, (2008) Meiosis in plants: ten years of gene discovery. Cytogenet Genome Res 120: 281-290. doi:10.1159/000121077. PubMed: 18504357.
37. Marimuthu MPa, Jolivet S, Ravi M, Pereira L, Davda JN, et al. (2011) Synthetic clonal reproduction through seeds. Science 331: 876. doi:10.1126/science.1199682. PubMed: 21330535.
38. Ross KJ, Fransz P, Jones GH, (1996) A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosome Res 4: 507-516. doi:10.1007/BF02261778. PubMed: 8939362.
39. 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. PubMed: 20628250.
40. Grelon M, Vezon D, Gendrot G, Pelletier G, (2001) AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO J 20: 589-600. doi:10.1093/emboj/20.3.589. PubMed: 11157765.
41. De Muyt A, Vezon D, Gendrot G, Gallois J-L, Stevens R, et al. (2007) AtPRD1 is required for meiotic double strand break formation in Arabidopsis thaliana. EMBO J 26: 4126-4137. doi:10.1038/sj.emboj.7601815. PubMed: 17762870.
42. 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. PubMed: 17530928.
43. Bai X, Peirson BN, Dong F, Xue C, Makaroff C a (1999) Isolation and characterization of SYN1, a RAD21-like gene essential for meiosis in Arabidopsis. Plant Cell 11: 417-430. doi:10.2307/3870870. PubMed: 10072401.
44. Bhatt AM, Lister C, Page T, Fransz P, Findlay K, et al. (1999) The DIF1 gene of Arabidopsis is required for meiotic chromosome segregation and belongs to the REC8/RAD21 cohesin gene family. Plant J 19: 463-472. doi:10.1046/j.1365-313X.1999.00548.x. PubMed: 10504568.
45. Li W, Chen C, Markmann-Mulisch U, Timofejeva L, Schmelzer E, et al. (2004) The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis. Proc Natl Acad Sci U S A 101: 10596-10601. doi:10.1073/pnas.0404110101. PubMed: 15249667.
46. Chelysheva L, Diallo S, Vezon D, Gendrot G, Vrielynck N, et al. (2005) AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis. J Cell Sci 118: 4621-4632. doi:10.1242/jcs.02583. PubMed: 16176934.
47. 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. doi:10.1105/tpc.11.9.1623. PubMed: 10488231.
48. 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. PubMed: 17937504.
49. D'Erfurth I, Jolivet S, Froger N, Catrice O, Novatchkova M, et al. (2009) Turning meiosis into mitosis. PLOS Biol 7: e1000124. doi:10.1371/journal.pbio.1000124.
50. Boateng Ka, Bellani Ma, Gregoretti IV, Pratto F, Camerini-Otero RD, (2013) Homologous Pairing Preceding SPO11-Mediated Double-Strand Breaks in Mice. Dev Cell 24: 196-205. doi:10.1016/j.devcel.2012.12.002. PubMed: 23318132.
51. 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. PubMed: 19763177.
52. Arabidopsis, Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815. doi:10.1038/35048692. PubMed: 11130711.
53. Yu J, Hu S, Wang J, Wong GK-S, Li S, et al. (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science (New York, NY) 296: 79-92. doi:10.1126/science.1068037.
54. Chromosomes, Rice (2005) 11 and 12 Sequencing Consortia. Seq Rice Chromosomes 11 and 12, rich in disease resistance genes and recent gene duplications. BMC biology 3: 20 doi:10.1186/1741-7007-3-20.
55. Wang X, Tang H, Bowers JE, Feltus F, Paterson AH, (2007) Extensive concerted evolution of rice paralogs and the road to regaining independence. Genetics 177: 1753-1763. doi:10.1534/genetics.107.073197. PubMed: 18039882.
56. Jenczewski E, Alix K, (2004) From Diploids to Allopolyploids: The Emergence of Efficient Pairing Control Genes in Plants. Crit Rev Plant Sci 23: 21-45. doi:10.1080/07352680490273239.
57. Stacey NJ, Kuromori T, Azumi Y, Roberts G, Breuer C, et al. (2006) Arabidopsis SPO11-2 functions with SPO11-1 in meiotic recombination. Plant J 48: 206-216. doi:10.1111/j.1365-313X.2006.02867.x. PubMed: 17018031.
58. Pradillo M, López E, Linacero R, Romero C, Cuñado N, et al. (2012) Together yes, but not coupled: new insights into the roles of RAD51 and DMC1 in plant meiotic recombination. Plant J 69: 921-933. doi:10.1111/j.1365-313X.2011.04845.x. PubMed: 22066484.
59. Heyman J, Van den Daele H, De Wit K, Boudolf V, Berckmans B, et al. (2011) Arabidopsis ULTRAVIOLET-B-INSENSITIVE4 maintains cell division activity by temporal inhibition of the anaphase-promoting complex/cyclosome. Plant Cell 23: 4394-4410. doi:10.1105/tpc.111.091793. PubMed: 22167059.
60. D'Erfurth I, Jolivet S, Froger N, Catrice O, Novatchkova M, et al. (2008) Mutations in AtPS1 (Arabidopsis thaliana parallel spindle 1) lead to the production of diploid pollen grains. PLOS Genet 4: e1000274. doi:10.1371/journal.pgen.1000274.