Molecular Mechanisms of Homologous Chromosome Pairing and Segregation in Plants

Jing Zhang^{a, b},
Bing Zhang^{a, b},
Handong Su^{a, b},
James A. Birchler^{c
, ,},
Fangpu Han^{a
, ,}

a.
State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China
b.
University of Chinese Academy of Sciences, Beijing 100049, China
c.
Division of Biological Sciences, 311 Tucker Hall, University of Missouri, Columbia, MO 65211, USA

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Corresponding author: E-mail address: birchlerj@missouri.edu (James A. Birchler); E-mail address: fphan@genetics.ac.cn (Fangpu Han)

摘要

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Abstract: In most eukaryotic species, three basic steps of pairing, recombination and synapsis occur during prophase of meiosis I. Homologous chromosomal pairing and recombination are essential for accurate segregation of chromosomes. In contrast to the well-studied processes such as recombination and synapsis, many aspects of chromosome pairing are still obscure. Recent progress in several species indicates that the telomere bouquet formation can facilitate homologous chromosome pairing by bringing chromosome ends into close proximity, but the sole presence of telomere clustering is not sufficient for recognizing homologous pairs. On the other hand, accurate segregation of the genetic material from parent to offspring during meiosis is dependent on the segregation of homologs in the reductional meiotic division (MI) with sister kinetochores exhibiting mono-orientation from the same pole, and the segregation of sister chromatids during the equational meiotic division (MII) with kinetochores showing bi-orientation from the two poles. The underlying mechanism of orientation and segregation is still unclear. Here we focus on recent studies in plants and other species that provide insight into how chromosomes find their partners and mechanisms mediating chromosomal segregation.
- Homologous chromosome pairing /
- Orientation and segregation /
- Meiosis

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参考文献(66)

[1]	Bass, H.W., Marshall, W.F., Sedat, J.W. et al. J. Cell Biol., 137 (1997),pp. 5-18
[2]	Campbell, C.S., Desai, A. Tension sensing by Aurora B kinase is independent of survivin-based centromere localization Nature, 498 (2013),pp. 118-121
[3]	Chelysheva, L., Diallo, S., Vezon, D. et al. AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis J. Cell Sci., 118 (2005),pp. 4621-4632
[4]	Chikashige, Y., Ding, D.Q., Funabiki, H. et al. Telomere-led premeiotic chromosome movement in fission yeast Science, 264 (1994),pp. 270-273
[5]	Conrad, M.N., Lee, C.Y., Chao, G. et al. Rapid telomere movement in meiotic prophase is promoted by NDJ1, MPS3, and CSM4 and is modulated by recombination Cell, 133 (2008),pp. 1175-1187
[6]	Cooke, C.A., Heck, M.M., Earnshaw, W.C. The inner centromere protein (INCENP) antigens: movement from inner centromere to midbody during mitosis J. Cell Biol., 105 (1987),pp. 2053-2067
[7]	Corbett, K.D., Yip, C.K., Ee, L.S. et al. The monopolin complex crosslinks kinetochore components to regulate chromosome-microtubule attachments Cell, 142 (2010),pp. 556-567
[8]	Da Ines, O., Abe, K., Goubely, C. et al. PLoS Genet., 8 (2012),p. e1002636
[9]	Demidov, D., Van Damme, D., Geelen, D. et al. Plant Cell, 17 (2005),pp. 836-848
[10]	Dernburg, A.F. RNA plays meiotic matchmarker Science, 336 (2012),pp. 681-682
[11]	Ding, D.Q., Yamamoto, A., Haraguchi, T. et al. Dynamics of homologous chromosome pairing during meiotic prophase in fission yeast Dev. Cell, 6 (2004),pp. 329-341
[12]	Ding, D.Q., Okamasa, K., Yamane, M. et al. Meiosis-specific noncoding RNA mediates robust pairing of homologous chromosomes in meiosis Science, 336 (2012),pp. 732-736
[13]	Gassmann, R., Carvalho, A., Henzing, A.J. et al. Borealin: a novel chromosomal passenger required for stability of the bipolar mitotic spindle J. Cell Biol., 166 (2004),pp. 179-191
[14]	Golubovskaya, I.N., Harper, L.C., Pawlowski, W.P. et al. Genetics, 162 (2002),pp. 1979-1993
[15]	Haarhuis, J.H., Elbatsh, A.M., van den Broek, B. et al. WAPL-mediated removal of cohesin protects against segregation errors and aneuploidy Curr. Biol., 23 (2013)
[16]	Han, F., Gao, Z., Yu, W. et al. Minichromosome analysis of chromosome pairing, disjunction, and sister chromatid cohesion in maize Plant Cell, 19 (2007),pp. 3853-3863
[17]	Harper, L.C., Golubovskaya, I.N., Cande, W.Z. A bouquet of chromosomes J. Cell Sci., 117 (2004),pp. 4025-4032
[18]	Hauf, S., Roitinger, E., Koch, B. et al. Dissociation of cohesin from chromosome arms and loss of arm cohesion during early mitosis depends on phosphorylation of SA2 PLoS Biol., 3 (2005),p. e69
[19]	Hoque, M.T., Ishikawa, F. Cohesin defects lead to premature sister chromatid separation, kinetochore dysfunction, and spindle-assembly checkpoint activation J. Biol. Chem., 277 (2002),pp. 42306-42314
[20]	Hiraoka, Y., Dernburg, A.F., Parmelee, S.J. et al. J. Cell Biol., 120 (1993),pp. 591-600
[21]	Ishiguro, T., Tanaka, K., Sakuno, T. et al. Shugoshin-PP2A counteracts casein-kinase-1-dependent cleavage of Rec8 by separase Nat. Cell Biol., 12 (2010),pp. 500-506
[22]	Jain, D., Cooper, J.P. Telomeric strategies: means to an end Annu. Rev. Genet., 44 (2010),pp. 243-269
[23]	Kelly, A.E., Ghenoiu, C., Xue, J.Z. et al. Survivin reads phosphorylated histone H3 threonine 3 to activate the mitotic kinase Aurora B Science, 330 (2010),pp. 235-239
[24]	Kemp, B., Boumil, R.M., Stewart, M.N. et al. A role for centromere pairing in meiotic chromosome segregation Genes Dev., 18 (2004),pp. 1946-1951
[25]	Kosaka, H., Shinohara, M., Shinohara, A. Csm4-dependent telomere movement on nuclear envelope promotes meiotic recombination PLoS Genet., 4 (2008),p. e1000196
[26]	Kueng, S., Hegemann, B., Peters, B.H. et al. Wapl controls the dynamic association of cohesin with chromatin Cell, 127 (2006),pp. 955-967
[27]	Lee, J.T. Lessons from X-chromosome inactivation: long ncRNA as guides and tethers to the epigenome Genes Dev., 23 (2009),pp. 1831-1842
[28]	Liu, H., Rankin, S., Yu, H. Phosphorylation-enabled binding of SGO1–PP2A to cohesin protects sororin and centromeric cohesion during mitosis Nat. Cell Biol., 15 (2012),pp. 40-49
[29]	Liu, H., Jia, L., Yu, H. Phospho-H2A and cohesin specify distinct tension-regulated Sgo1 pools at kinetochores and inner centromeres Curr. Biol., 23 (2013),pp. 1-7
[30]	Losada, A., Yokochi, T., Kobayashi, R. et al. J. Cell Biol., 150 (2000),pp. 405-416
[31]	Martinez-Perez, E., Shaw, P., Reader, S. et al. Homologous chromosome pairing in wheat J. Cell Sci., 112 (1999),pp. 1761-1769
[32]	Martinez-Perez, E., Shaw, P., Moore, G. Nature, 411 (2001),pp. 204-207
[33]	McCollum, D. Monopolin Curr. Biol., 22 (2012),pp. 937-938
[34]	McKee, B.D. Chromosoma, 105 (1996),pp. 135-141
[35]	Niwa, O., Shimanuki, M., Miki, F. Telomere-led bouquet formation facilitates homologous chromosome pairing and restricts ectopic interaction in fission yeast meiosis EMBO J, 19 (2000),pp. 3831-3840
[36]	Penfold, C.A., Brown, P.E., Lawrence, N.D. et al. Modeling meiotic chromosomes indicates a size dependent contribution of telomere clustering and chromosome rigidity to homologue juxtaposition PLoS Comput. Biol., 8 (2012),p. e1002496
[37]	Petronczki, M., Matos, J., Mori, S. et al. Monopolar attachment of sister kinetochores at meiosis I requires casein kinase 1 Cell, 126 (2006),pp. 1049-1064
[38]	Phillips, D., Nibau, C., Wnetrzak, J. et al. PLoS ONE, 7 (2012),p. e39539
[39]	Rabitsch, K.P., Petronczki, M., Javerzat, J.P. et al. Kinetochore recruitment of two nucleolar proteins is required for homolog segregation in meiosis I Dev. Cell, 4 (2003),pp. 535-548
[40]	Roberts, N.Y., Osman, K., Armstrong, S.J. Cytogenet. Genome Res., 124 (2009),pp. 193-201
[41]	Ronceret, A., Doutriaux, M.P., Golubovskaya, I.N. et al. PHS1 regulates meiotic recombination and homologous chromosome pairing by controlling the transport of RAD50 to the nucleus Proc. Natl. Acad. Sci. USA, 106 (2009),pp. 20121-20126
[42]	Scherthan, H. A bouquet makes ends meet Nat. Rev. Mol. Cell Biol., 2 (2001),pp. 621-627
[43]	Scherthan, H. Telomere attachment and clustering during meiosis Cell Mol. Life Sci., 64 (2007),pp. 117-124
[44]	Severson, A.F., Ling, L., van Zuylen, V. et al. Genes Dev., 23 (2009),pp. 1763-1778
[45]	Takeo, S., Lake, C.M., Morais-de-Sá, E. et al. Curr. Biol., 21 (2011),pp. 1845-1851
[46]	Tanaka, T., Fuchs, J., Loidl, J. et al. Cohesin ensures bipolar attachment of microtubules to sister centromeres and resists their precocious separation Nat. Cell Biol., 2 (2000),pp. 492-499
[47]	Terada, Y., Tatsuka, M., Suzuki, F. et al. AIM-1: a mammalian midbody-associated protein required for cytokinesis EMBO J., 17 (1998),pp. 667-676
[48]	Tomonaga, T., Nagao, K., Kawasaki, Y. et al. Characterization of fission yeast cohesin: essential anaphase proteolysis of Rad21 phosphorylated in the S phase Genes Dev., 14 (2000),pp. 2757-2770
[49]	Tóth, A., Ciosk, R., Uhlmann, F. et al. Yeast cohesin complex requires a conserved protein, Eco1p (Ctf7), to establish cohesion between sister chromatids during DNA replication Genes Dev., 13 (1999),pp. 320-333
[50]	Tóth, A., Rabitsch, K.P., Gálová, M. et al. Functional genomics identifies monopolin: a kinetochore protein required for segregation of homologs during meiosis I Cell, 103 (2000),pp. 1155-1168
[51]	Tsubouchi, T., Roeder, G.S. A synaptonemal complex protein promotes homology-independent centromere coupling Science, 308 (2005),pp. 870-873
[52]	Tsubouchi, T., MacQueen, A.J., Roeder, G.S. Initiation of meiotic chromosome synapsis at centromeres in budding yeast Genes Dev., 22 (2008),pp. 3217-3226
[53]	Vader, G., Lens, S. Chromosome segregation: taking the passenger seat Curr. Biol., 20 (2010),pp. 879-881
[54]	Wanat, J.J., Kim, K.P., Koszul, R. et al. Csm4, in collaboration with Ndj1, mediates telomere-led chromosome dynamics and recombination during yeast meiosis PLoS Genet., 4 (2008),p. e1000188
[55]	Wang, F., Dai, J., Daum, J.R. et al. Histone H3 Thr-3 phosphorylation by Haspin positions Aurora B at centromeres in mitosis Science, 330 (2010),pp. 231-235
[56]	Wang, F., Ulyanova, N.P., Daum, J.R. et al. Haspin inhibitors reveal centromeric functions of Aurora B in chromosome segregation J. Cell Biol., 199 (2012),pp. 251-268
[57]	Watanabe, Y. Temporal and spatial regulation of targeting aurora B to the inner centromere Cold Spring Harb. Symp. Quant. Biol., 75 (2010),pp. 419-423
[58]	Watanabe, Y., Yamamoto, M.S. Cell, 78 (1994),pp. 487-498
[59]	Welburn, J.P., Vleugel, M., Liu, D. et al. Aurora B phosphorylates spatially distinct targets to differentially regulate the kinetochore-microtubule interface Mol. Cell, 38 (2010),pp. 383-392
[60]	Wen, R., Moore, G., Shaw, P.J. PLoS ONE, 7 (2012),p. e44681
[61]	Xu, N., Tsai, C.L., Lee, J.T. Transient homologous chromosome pairing marks the onset of X inactivation Science, 311 (2006),pp. 1149-1152
[62]	Yamagishi, Y., Honda, T., Tanno, Y. et al. Two histone marks establish the inner centromere and chromosome bi-orientation Science, 330 (2010),pp. 239-243
[63]	Yu, H.G., Dawe, R.K. Functional redundancy in the maize meiotic kinetochore J. Cell Biol., 151 (2000),pp. 131-141
[64]	Zhang, B., Lv, Z., Pang, J. et al. Formation of a functional maize centromere after loss of centromeric sequences and gain of ectopic sequences Plant Cell, 25 (2013),pp. 1979-1989
[65]	Zhang, J., Pawlowski, W.P., Han, F. Centromere pairing in early meiotic prophase requires active centromeres and precedes installation of the synaptonemal complex in maize Plant Cell, 25 (2013),pp. 3900-3909
[66]	Zheng, Y.Z., Roseman, R.R., Carlson, W.R. Time course study of the chromosome-type breakage-fusion-bridge cycle in maize Genetics, 153 (1999),pp. 1435-1444