The Arabidopsis SYN3 cohesin protein is important for early meiotic events

Plant Journal

Volumn 71, Issue 1, 2012, Pages 147-160

  Yuan, Li ^a   Yang, Xiaohui ^a   Ellis, Jessie L ^a   Fisher, Nicole M ^a   Makaroff, Christopher A ^a  

^a MIAMI UNIVERSITY   (United States)

Author keywords

Arabidopsis thaliana; cohesin; cohesion; kleisin; meiosis; recombination; synapsis

Indexed keywords

ARABIDOPSIS THALIANA; COHESINS; COHESION; KLEISIN; MEIOSIS; RECOMBINATION; SYNAPSIS;

CHROMOSOMES; ENCODING (SYMBOLS); GENE EXPRESSION; PLANTS (BOTANY);

PROTEINS;

ARABIDOPSIS PROTEIN; CELL CYCLE PROTEIN; SYN3 PROTEIN, ARABIDOPSIS; ZYP1A PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; ARTICLE; CHROMOSOME PAIRING; FLOWER; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MEIOSIS; METABOLISM; PROMOTER REGION; RNA INTERFERENCE; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL CYCLE PROTEINS; CHROMOSOME PAIRING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GERM CELLS, PLANT; MEIOSIS; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; RNA INTERFERENCE;

ARABIDOPSIS; ARABIDOPSIS THALIANA; SYNAPSIS;

EID: 84862578624     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2012.04979.x     Document Type: Article

References (83)

1. Armstrong, S., Franklin, F., and, Jones, G., (2001) Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana. J. Cell Sci. 114, 4207-04217.
2. Armstrong, S., Caryl, A., Jones, G., and, Franklin, F., (2002) Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J. Cell Sci. 115, 3645-3655.
3. Arumugam, P., Gruber, S., Tanaka, K., Haering, C.H., Mechtler, K., and, Nasmyth, K., (2003) ATP hydrolysis is required for cohesin's association with chromosomes. Curr. Biol. 13, 1941-1953. (Pubitemid 37425203)
4. Bai, X., Peirson, B., Dong, F., Cai, X., and, Makaroff, C., (1999) Isolation and characterization of SYN1, a RAD21-like gene essential for meiosis in Arabidopsis. Plant Cell, 11, 417-430.
5. Bhatt, A.M., Lister, C., Page, T., Fransz, P., Findlay, K., Jones, G.H., Dickinson, H.G., and, Dean, C., (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.
6. Bleuyard, J.Y., Gallego, M.E., Savigny, F., and, White, C.I., (2005) Differing requirements for the Arabidopsis Rad51 paralogs in meiosis and DNA repair. Plant J. 41, 533-545. (Pubitemid 40307415)
7. Borck, G., Zarhrate, M., Cluzeau, C., Bal, E., Bonnefont, J., Munnich, A., Cormier-Daire, V., and, Colleaux, L., (2006) Father-to daughter transmission of Cornelia de Lange syndrome caused by a mutation in the 5' untranslated region of the NIPBL gene. Hum. Mutat. 27, 731-735. (Pubitemid 44205065)
8. Borde, V., (2007) The multiple roles of the Mre11 complex for meiotic recombination. Chromosome Res. 15, 551-563. (Pubitemid 47221374)
9. Brar, G.A., Hochwagen, A., Ee, L.S., and, Amon, A., (2009) The multiple roles of cohesin in meiotic chromosome morphogenesis and pairing. Mol. Biol. Cell, 20, 1030-1047.
10. Buonomo, S.B.C., Clyne, R.K., Fuchs, J., Loidl, J., Uhlmann, F., and, Nasmyth, K., (2000) Disjunction of homologous chromosomes in meiosis I depends on proteolytic cleavage of the meiotic cohesin Rec8 by separin. Cell, 103, 387-398.
11. Cai, X., Dong, F.G., Edelmann, R.E., and, Makaroff, C.A., (2003) The Arabidopsis SYN1 cohesin protein is required for sister chromatid arm cohesion and homologous chromosome pairing. J. Cell Sci. 116, 2999-3007. (Pubitemid 36926988)
12. Caryl, A.P., Armstrong, S.J., Jones, G.H., and, Franklin, F.C.H., (2000) A homologue of the yeast HOP1 gene is inactivated in the Arabidopsis meiotic mutant asy1. Chromosoma, 109, 62-71. (Pubitemid 30433298)
13. Chen, C.B., Zhang, W., Timofejeva, L., Gerardin, Y., and, Ma, H., (2006) The Arabidopsis ROCK-N-ROLLERS gene encodes a homolog of the yeast ATP-dependent DNA helicase MER3 and is required for normal meiotic crossover formation. Plant J. 43, 321-334. (Pubitemid 41577001)
14. Chen, Z., Higgins, J.D., Hui, J.T.L., Li, J., Franklin, F.C.H., and, Berger, F., (2011) Retinoblastoma protein is essential for early meiotic events in Arabidopsis. EMBO J. 30, 744-755.
15. Christensen, C.A., Subramanian, S., and, Drews, G.N., (1998) Identification of gametophytic mutations affecting female gametophyte development in Arabidopsis. Dev. Biol. 202, 136-151. (Pubitemid 28467253)
16. Ciosk, R., Shirayama, M., Shevchenko, A., Tanaka, T., Toth, A., and, Nasmyth, K., (2000) Cohesin's binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. Mol. Cell, 5, 243-254. (Pubitemid 30628083)
17. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
18. da Costa-Nunes, J.A., Bhatt, A.M., O'Shea, S., West, C.E., Bray, C.M., Grossniklaus, U., and, Dickinson, H.G., (2006) Characterization of the three Arabidopsis thaliana RAD21 cohesins reveals differential responses to ionizing radiation. J. Exp. Bot. 57, 971-983.
19. Degner, S.C., Wong, T.P., Jankevicius, G., and, Feeney, A.J., (2009) Cutting edge: developmental stage-specific recruitment of cohesin to CTCF sites throughout immunoglobulin loci during B lymphocyte development. J. Immunol. 182, 44-48.
20. Dion, E., Li, L.L., Jean, M., and, Beizile, F., (2007) An Arabidopsis MLH1 mutant exhibits reproductive defects and reveals a dual role for this gene in mitotic recombination. Plant J. 51, 431-440. (Pubitemid 47106540)
21. Dong, F., Cai, X., and, Makaroff, C., (2001) Cloning and characterization of two Arabidopsis genes that belong to the RAD21/REC8 family of chromosome cohesin proteins. Gene, 271, 99-108. (Pubitemid 32539150)
22. Dorsett, D., (2009) Cohesin, gene expression and development: lessons from Drosophila. Chromosome Res. 17, 185-200.
23. Dorsett, D., (2011) Cohesin: genomic insights into controlling gene transcription and development. Curr. Opin. Genet. Dev. 21, 199-206.
24. Doutriaux, M.P., Couteau, F., Bergounioux, C., and, White, C., (1998) Isolation and characterisation of the RAD51 and DMC1 homologs from Arabidopsis thaliana. Mol. Gen. Genet. 257, 283-291.
25. Fransz, P., Alonso-Blanco, C., Liharska, T.B., Peeters, A.J.M., Zabel, P., and, Hans de Jung, J., (1996) High resolution physical mapping in Arabidopsis thaliana and tomato by fluorescence in situ hybridization to extended DNA fibers. Plant J. 9, 421-430.
26. Golubovskaya, I.N., Hamant, O., Timofejeva, L., Wang, C.J.R., Braun, D., Meeley, R., and, Cande, W.Z., (2006) Alleles of afd1 dissect REC8 functions during meiotic prophase I. J. Cell Sci. 119, 3306-3315. (Pubitemid 44405216)
27. Grelon, M., Vezon, D., Gendrot, G., and, Pelletier, G., (2001) AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO J. 20, 589-600. (Pubitemid 32126994)
28. Gruber, S., Arumugam, P., Katou, Y., Kuglitsch, D., Helmhart, W., Shirahige, K., and, Nasmyth, K., (2006) Evidence that loading of cohesin onto chromosomes involves opening of its SMC hinge. Cell, 127, 523-537. (Pubitemid 44647422)
29. Gullerova, M., and, Proudfoot, N.J., (2008) Cohesin complex promotes transcriptional termination between convergent genes in S. pombe. Cell, 132, 983-995. (Pubitemid 351381746)
30. Guo, H.-S., Fei, J.-F., Xie, Q., and, Chua, N.-H., (2003) A chemical-regulated inducible RNAi system in plants. Plant J. 34, 383-392. (Pubitemid 36579862)
31. Hadjur, S., Williams, L.M., Ryan, N.K., Cobb, B.S., Sexton, T., Fraser, P., Fisher, A.G., and, Merkenschlager, M., (2009) Cohesins form chromosomal cis-interactions at the developmentally regulated IFNG locus. Nature, 460, 410-414.
32. Hauf, S., Waizenegger, I.C., and, Peters, J.M., (2001) Cohesin cleavage by separase required for anaphase and cytokinesis in human cells. Science, 293, 1320-1323. (Pubitemid 32777422)
33. Hauf, S., Roitinger, E., Koch, B., Dittrich, C.M., Mechtler, K., and, Peters, J.M., (2005) Dissociation of cohesin from chromosome arms and loss of arm cohesion during early mitosis depends on phosphorylation of SA2. PLoS Biol. 3, 419-432.
34. Heyting, C., (1996) Synaptonemal complexes: structure and function. Curr. Opin. Cell Biol. 8, 389-396. (Pubitemid 26179219)
35. Higgins, J.D., Armstrong, S.J., Franklin, F.C.H., and, 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. (Pubitemid 39362897)
36. Higgins, J.D., Sanchez-Moran, E., Armstrong, S.J., Jones, G.H., and, 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. (Pubitemid 41483696)
37. Horsfield, J.A., Anagnostou, S.H., Hu, J.K.H., Cho, K.H.Y., Geisler, R., Lieschke, G., Crosier, K.E., and, Crosier, P.S., (2007) Cohesin-dependent regulation of Runx genes. Development, 134, 2639-2649. (Pubitemid 47225960)
38. Hou, C.H., Dale, R., and, Dean, A., (2010) Cell type specificity of chromatin organization mediated by CTCF and cohesin. Proc. Natl Acad. Sci. USA, 107, 3651-3656.
39. Ishiguro, K., Kim, J., Fujiyama-Nakamura, S., Kato, S., and, Watanabe, Y., (2011) A new meiosis-specific cohesin complex implicated in the cohesin code for homologous pairing. EMBO Rep. 12, 267-275.
40. Jiang, L., Xia, M., Strittmatter, L.I., and, Makaroff, C.A., (2007) The Arabidopsis cohesin protein SYN3 localizes to the nucleolus and is essential for gametogenesis. Plant J. 50, 1020-1034. (Pubitemid 46904109)
41. Kagey, M.H., Newman, J.J., Bilodeau, S., et al. (2010) Mediator and cohesin connect gene expression and chromatin architecture. Nature, 472, 430-435.
42. Kim, K.P., Weiner, B.M., Zhang, L.R., Jordan, A., Dekker, J., and, Kleckner, N., (2011) Sister cohesion and structural axis components mediate homolog bias of meiotic recombination. Cell, 143, 924-937.
43. Kitajima, T.S., Kawashima, S.A., and, Watanabe, Y., (2004) The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature, 427, 510-517. (Pubitemid 38209104)
44. Kleckner, N., Zickler, D., Jones, G.H., Dekker, J., Padmore, R., Henle, J., and, Hutchinson, J., (2004) A mechanical basis for chromosome function. Proc. Natl Acad. Sci. USA, 101, 12592-12597. (Pubitemid 39122069)
45. Klimyuk, V.I., and, Jones, J.D.G., (1997) AtDMC1, the Arabidopsis homologue of the yeast DMC1 gene: characterization, transposon-induced allelic variation and meiosis-associated expression. Plant J. 11, 1-14. (Pubitemid 27108352)
46. Lam, W.S., Yang, X.H., and, Makaroff, C.A., (2005) Characterization of Arabidopsis thaliana SMC1 and SMC3: evidence that ASMC3 may function beyond chromosome cohesion. J. Cell Sci. 118, 3037-3048. (Pubitemid 41149908)
47. Lee, J., and, Hirano, T., (2011) RAD21L, a novel cohesin subunit implicated in linking homologous chromosomes in mammalian meiosis. J. Cell Biol. 192, 263-276.
48. Lengronne, A., McIntyre, J., Katou, Y., Kanoh, Y., Hopfner, K.P., Shirahige, K., and, Uhlmann, F., (2006) Establishment of sister chromatid cohesion at the S. cerevisiae replication fork. Mol. Cell, 23, 787-799. (Pubitemid 44344523)
49. Lin, W.Q., Jin, H., Liu, X.W., Hampton, K., and, Yu, H.G., (2011a) Scc2 regulates gene expression by recruiting cohesin to the chromosome as a transcriptional activator during yeast meiosis. Mol. Biol. Cell, 22, 1985-1996.
50. Lin, W.Q., Wang, M.A., Jin, H., and, Yu, H.G., (2011b) Cohesin plays a dual role in gene regulation and sister-chromatid cohesion during meiosis in Saccharomyces cerevisiae. Genetics, 187, 1041-1051.
51. Losada, A., Hirano, M., and, Hirano, T., (2002) Cohesin release is required for sister chromatid resolution, but not for condensin-mediated compaction, at the onset of mitosis. Genes Dev. 23, 3004-3016. (Pubitemid 35424189)
52. Martinez-Zapater, J.M., Estelle, M.A., and, Somerville, C.R., (1986) A highly repeated DNA sequence in Arabidopsis thaliana. Mol. Gen. Genet. 204, 417-423.
53. Merkenschlager, M., (2010) Cohesin: a global player in chromosome biology with local ties to gene regulation. Curr. Opin. Genet. Dev. 20, 555-561.
54. Mishiro, T., Ishihara, K., Hino, S., Tsutsumi, S., Aburatani, H., Shirahige, K., Kinoshita, Y., and, Nakao, M., (2009) Architectural roles of multiple chromatin insulators at the human apolipoprotein gene cluster. EMBO J. 28, 1234-1245.
55. Mito, Y., Sugimoto, A., and, Yamamoto, M., (2003) Distinct developmental function of two Caenorhabditis elegans homologs of the cohesin subunit Scc1/Rad21. Mol. Biol. Cell, 14, 2399-2409. (Pubitemid 36724329)
56. Moldovan, G.L., Pfander, B., and, Jentsch, S., (2006) PCNA controls establishment of sister chromatid cohesion during S phase. Mol. Cell, 23, 723-732. (Pubitemid 44292556)
57. Nasmyth, K., and, Haering, C.H., (2009) Cohesin: its roles and mechanisms. Annu. Rev. Genet. 43, 525-558.
58. Nativio, R., Wendt, K.S., Ito, Y., Huddleston, J.E., Uribe-Lewis, S., Woodfine, K., Krueger, C., Reik, W., Peters, J.M., and, Murrell, A., (2009) Cohesin is required for higher-Order chromatin conformation at the imprinted IGF2-H19 Locus. PLoS Genet. 5, 1-15.
59. Parelho, V., Hadjur, S., Spivakov, M., et al. (2008) Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell, 132, 422-433.
60. Pasierbek, P., Jantsch, M., Melcher, M., Schleiffer, A., Schweizer, D., and, Loidl, J., (2001) A Caenorhabditis elegans cohesion protein with functions in meiotic chromosome pairing and disjunction. Genes Dev. 15, 1349-1360. (Pubitemid 32524642)
61. Pauli, A., van Bemmel, J.G., Oliveira, R.A., Itoh, T., Shirahige, K., van Steensel, B., and, Nasmyth, K., (2010) A direct role for cohesin in gene regulation and ecdysone response in Drosophila salivary glands. Curr. Biol. 20, 1787-1798.
62. Peirson, B.N., Bowling, S.E., and, Makaroff, C.A., (1997) A defect in synapsis causes male sterility in a T-DNA-tagged Arabidopsis thaliana mutant. Plant J. 11, 659-669. (Pubitemid 27206977)
63. Pelttari, J., Hoja, M.R., Yuan, L., et al. (2001) A meiotic chromosomal core consisting of cohesin complex proteins recruits DNA recombination proteins and promotes synapsis in the absence of an axial element in mammalian meiotic cells. Mol. Cell. Biol. 21, 5667-5677. (Pubitemid 32702469)
64. Peric-Hupkes, D., and, van Steensel, B., (2008) Linking cohesin to gene regulation. Cell, 132, 925-928. (Pubitemid 351381747)
65. Riedel, C.G., Katis, V.L., Katou, Y., et al. (2006) Protein phosphatase 2A protects centromeric sister chromatid cohesion during meiosis I. Nature, 441, 53-61.
66. Ronceret, A., Doutriaux, M.P., Golubovskaya, I.N., and, Pawlowski, W.P., (2009) PHS1 regulates meiotic recombination and homologous chromosome pairing by controlling the transport of RAD50 to the nucleus. Proc. Natl Acad. Sci. USA, 106, 20121-20126.
67. Ross, K.J., Fransz, P., and, Jones, G.H., (1996) A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosome Res. 4, 507-516. (Pubitemid 26399918)
68. Rubio, E.D., Reiss, D.J., Weicsh, P.L., Disteche, C.M., Filippova, G.N., Baliga, N.S., Aebersold, R., Ranish, J.A., and, Krumm, A., (2008) CTCF physically links cohesin to chromatin. Proc. Natl Acad. Sci. USA, 105, 8309-8314. (Pubitemid 351904752)
69. Sanchez-Moran, E., Osman, K., Higgins, J.D., Pradillo, M., Cunado, N., Jones, G.H., and, Franklin, F.C.H., (2008) ASY1 coordinates early events in the plant meiotic recombination pathway. Cytogenet. Genome Res. 120, 302-312. (Pubitemid 351751928)
70. Schuldiner, O., Berdnik, D., Levy, J.M., Wu, J.S., Luginbuhl, D., Camille, A., and, Luo, L.Q., (2008) piggyBac-based mosaic screen identifies a postmitotic function for cohesin in regulating developmental axon pruning. Dev. Cell, 14, 227-238. (Pubitemid 351189171)
71. Severson, A.F., Ling, L., van Zuylen, V., and, Meyer, B.J., (2009) The axial element protein HTP-3 promotes cohesin loading and meiotic axis assembly in C. elegans to implement the meiotic program of chromosome segregation. Genes Dev. 23, 1763-1778.
72. Siomos, M.F., Badrinath, A., Pasierbek, P., Livingstone, D., White, J., Glotzer, M., and, Nasmyth, K., (2001) Separase is required for chromosome segregation during meiosis I in Caenorhabditis elegans. Curr. Biol. 23, 1825-1835. (Pubitemid 33136522)
73. Skibbens, R., Corson, L., Koshland, D., and, Hieter, P., (1999) Ctf7p is essential for sister chromatid cohesion and links mitotic chromosome structure to the DNA replication machinery. Genes Dev. 13, 307-319. (Pubitemid 29095802)
74. Stacey, N.J., Kuromori, T., Azumi, Y., Roberts, G., Breuer, C., Wada, T., Maxwell, A., Roberts, K., and, Sugimoto-Shirasu, K., (2006) Arabidopsis SPO11-2 functions with SPO11-1 in meiotic recombination. Plant J. 48, 206-216. (Pubitemid 44484862)
75. Sumara, I., Vorlaufer, E., Stukenberg, P., Kelm, O., Redemann, N., Nigg, E., and, Peters, J., (2002) The dissociation of cohesin from chromosomes in prophase is regulated by Polo-like kinase. Mol. Cell, 9, 515-525. (Pubitemid 34273783)
76. Tang, Z.Y., Sun, Y.X., Harley, S.E., Zou, H., and, Yu, H.T., (2004) Human Bub1 protects centromeric sister-chromatid cohesion through Shugoshin during mitosis. Proc. Natl. Acad. Sci. USA, 101, 18012-18017. (Pubitemid 40054066)
77. Toth, A., Ciosk, R., Uhlmann, F., Galova, M., Schleiffer, A., and, Nasmyth, K., (1999) Yeast cohesin complex requires a conserved protein, Eco1p(Ctf7), to establish cohesion between sister chromatids during DNA replication. Genes Dev. 13, 320-333. (Pubitemid 29095803)
78. Uhlmann, F., Lottspeich, F., and, Nasmyth, K., (1999) Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1. Nature, 400, 37-42. (Pubitemid 29315102)
79. Waizenegger, I.C., Hauf, S., Meinke, A., and, Peters, J.M., (2000) Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase. Cell, 103, 399-410.
80. Wendt, K.S., Yoshida, K., Itoh, T., et al. (2008) Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature, 451, 796-801. (Pubitemid 351253176)
81. Xiong, B., and, Gerton, J.L., (2010) Regulators of the cohesin network. Annu. Rev. Biochem. 79, 131-153.
82. Yang, X., Timofejeva, L., Ma, H., and, Makaroff, C.A., (2006) The Arabidopsis SKP1 homologue ASK1 controls meiotic chromosome remodeling and release of chromatin from the nuclear membrane and nucleolus. J. Cell Sci. 19, 4025-4032.
83. Zickler, D., and, Kleckner, N., (1999) Meiotic chromosomes: integrating structure and function. Annu. Rev. Genet. 33, 603-754. (Pubitemid 30083134)