5.9
CiteScore
5.9
Impact Factor
Volume 41 Issue 3
Mar.  2014
Turn off MathJax
Article Contents

Expression of Epitope-Tagged SYN3 Cohesin Proteins Can Disrupt Meiosis in Arabidopsis

doi: 10.1016/j.jgg.2013.11.006
More Information
  • Corresponding author: E-mail address: makaroca@miamioh.edu (Christopher A. Makaroff)
  • Received Date: 2013-07-24
  • Accepted Date: 2013-11-26
  • Rev Recd Date: 2013-11-23
  • Available Online: 2013-12-13
  • Publish Date: 2014-03-20
  • α-kleisins are core components of meiotic and mitotic cohesin complexes. Arabidopsis contains genes encoding four α-kleisins. SYN1, a REC8 ortholog, is essential for meiosis, while SYN2 and SYN4 appear to be SCC1 orthologs and function in mitosis. SYN3 is enriched in the nucleolus of meiotic and mitotic cells and is essential for megagametogenesis. It was recently shown that expression of SYN3-RNAi constructs in buds cause changes in meiotic gene expression that result in meiotic alterations. In this report we show that expression of SYN3 from the 35S promoter with either a c-terminal Myc or FAST tag causes a reduction in SYN1 mRNA levels that results in alterations in sister chromatid cohesion, homologous chromosome synapsis and synaptonemal complex formation during both male and female meiosis.
  • loading
  • [1]
    Anderson, L.K., Royer, S.M., Page, S.L. et al. Proc. Natl. Acad. Sci. USA, 102 (2005),pp. 4482-4487
    [2]
    Bai, X., Peirsion, B., Dong, F. et al. Plant Cell, 11 (1999),pp. 417-430
    [3]
    Bauerschmidt, C., Arrichiello, C., Burdak-Rothkamm, S. et al. Cohesin promotes the repair of ionizing radiation-induced DNA double-strand breaks in replicated chromatin Nuc. Acids Res., 38 (2010),pp. 477-487
    [4]
    Ben-Shahar, T.R., Heeger, S., Lehane, C. et al. Eco1-dependent cohesin acetylation during establishment of sister chromatid cohesion Science, 321 (2008),pp. 563-566
    [5]
    Bhatt, A.M., Lister, C., Page, T. et al. Plant J., 19 (1999),pp. 463-472
    [6]
    Cai, X., Dong, F.G., Edelmann, R.E. et al. J. Cell Sci., 116 (2003),pp. 2999-3007
    [7]
    Chen, C.B., Zhang, W., Timofejeva, L. et al. Plant J., 43 (2005),pp. 321-334
    [8]
    Chen, Z., Hui, J.T.L., Ingouff, M. et al. Development, 135 (2008),pp. 65-73
    [9]
    Christensen, C.A., King, E.J., Jordan, J.R. et al. Sex. Plant Reprod., 10 (1997),pp. 49-64
    [10]
    Christensen, C.A., Subramanian, S., Drews, G.N. Dev. Biol., 202 (1998),pp. 136-151
    [11]
    Ciosk, R., Shirayama, M., Shevchenko, A. et al. Cohesin's binding to chromosomes depends on a separate complex consisting of SCC2 and SCC4 proteins Mol. Cell, 5 (2000),pp. 243-254
    [12]
    Clough, S.J., Bent, A.F. Plant J., 16 (1998),pp. 735-743
    [13]
    da Costa-Nunes, J.A., Bhatt, A.M., O'Shea, S. et al. J. Exp. Bot., 57 (2006),pp. 971-983
    [14]
    Dong, F., Cai, X., Makaroff, C. Gene, 271 (2001),pp. 99-108
    [15]
    Dorsett, D. Chromosome Res., 17 (2009),pp. 185-200
    [16]
    Dorsett, D. Cohesin: genomic insights into controlling gene transcription and development Curr. Opin. Genet. Dev., 21 (2011),pp. 199-206
    [17]
    Dorsett, D., Merkenschlager, M. Cohesin at active genes: a unifying theme for cohesin and gene expression from model organisms to humans Curr. Opin. Cell Biol., 25 (2013),pp. 11-17
    [18]
    Dorsett, D., Strom, L. The ancient and evolving roles of cohesin in gene expression and DNA repair Curr. Biol., 22 (2012),pp. R240-R250
    [19]
    Frank, A.C., Johnson, M.A. Expressing the diphtheria toxin α subunit from the HAP2(GCS1) promoter blocks sperm maturation and produces single sperm-like cells capable of fertilization Plant Physiol., 151 (2009),pp. 1390-1400
    [20]
    Gandhi, R., Gillespie, P.J., Hirano, T. Human WAPLl is a cohesin-binding protein that promotes sister-chromatid resolution in mitotic prophase Curr. Biol., 16 (2006),pp. 2406-2417
    [21]
    Grelon, M., Vezon, D., Gendrot, G. et al. AtSPO11-1 is necessary for efficient meiotic recombination in plants EMBO J., 20 (2001),pp. 589-600
    [22]
    Guillou, E., Ibarra, A., Coulon, V. et al. Cohesin organizes chromatin loops at DNA replication factories Genes Dev., 24 (2011),pp. 2812-2822
    [23]
    Gullerova, M., Proudfoot, N.J. Cell, 132 (2008),pp. 983-995
    [24]
    Gusti, A., Baumberger, N., Nowack, M. et al. PLoS ONE, 4 (2009),p. e4780
    [25]
    Hadjur, S., Williams, L.M., Ryan, N.K. et al. Nature, 460 (2009),pp. 410-413
    [26]
    Haering, C.H., Jessberger, R. Cohesin in determining chromosome architecture Exp. Cell Res., 318 (2012),pp. 1386-1393
    [27]
    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),pp. 419-432
    [28]
    Hauf, S., Waizenegger, I.C., Peters, J.M. Cohesin cleavage by separase required for anaphase and cytokinesis in human cells Science, 293 (2001),pp. 1320-1323
    [29]
    Higgins, J.D., Vignard, J., Mercier, R. et al. Plant J., 55 (2008),pp. 28-39
    [30]
    Hou, C.H., Dale, R., Dean, A. Cell type specificity of chromatin organization mediated by CTCF and cohesin Proc. Natl. Acad. Sci. USA, 107 (2010),pp. 3651-3656
    [31]
    Huang, Z., Zhu, J., Mu, X. et al. Ann. Bot., 93 (2004),pp. 295-301
    [32]
    Ingouff, M., Sakata, T., Li, J. et al. Curr. Biol., 19 (2009),pp. R19-R20
    [33]
    Ishiguro, K., Kim, J., Fujiyama-Nakamura, S. et al. A new meiosis-specific cohesin complex implicated in the cohesin code for homologous pairing EMBO Rep., 12 (2011),pp. 267-275
    [34]
    Iwakawa, H., Shinmyo, A., Sekine, M. Plant J., 45 (2006),pp. 819-831
    [35]
    Jiang, L., Xia, M., Strittmatter, L.I. et al. Plant J., 50 (2007),pp. 1020-1034
    [36]
    Kagey, M.H., Newman, J.J., Bilodeau, S. et al. Mediator and cohesin connect gene expression and chromatin architecture Nature, 472 (2010),pp. 247-249
    [37]
    Kim, H.J., Oh, S.A., Brownfield, L. et al. Control of plant germline proliferation by SCF(FBL17) degradation of cell cycle inhibitors Nature, 455 (2008),pp. 1134-1138
    [38]
    Kitajima, T.S., Kawashima, S.A., Watanabe, Y. The conserved kinetochore protein Shugoshin protects centromeric cohesion during meiosis Nature, 427 (2004),pp. 510-517
    [39]
    Klimyuk, V.I., Jones, J.D.G. Plant J., 11 (1997),pp. 1-14
    [40]
    Lam, W.S., Yang, X.H., Makaroff, C.A. J. Cell Sci., 118 (2005),pp. 3037-3048
    [41]
    Lee, J., Hirano, T. Rad21l, a novel cohesin subunit implicated in linking homologous chromosomes in mammalian meiosis J. Cell Biol., 192 (2011),pp. 263-276
    [42]
    Maradeo, M.E., Skibbens, R.V. Epitope tag-induced synthetic lethality between cohesin subunits and Ctf7/Eco1 acetyltransferase FEBS Lett., 584 (2010),pp. 4037-4040
    [43]
    Merkenschlager, M., Odom, D.T. CTCF and cohesin: linking gene regulatory elements with their targets Cell, 152 (2013),pp. 1285-1297
    [44]
    Mishiro, T., Ishihara, K., Hino, S. et al. Architectural roles of multiple chromatin insulators at the human apolipoprotein gene cluster EMBO J., 28 (2009),pp. 1234-1245
    [45]
    Mito, Y., Sugimoto, A., Yamamoto, M. Mol. Biol. Cell, 14 (2003),pp. 2399-2409
    [46]
    Murdoch, B., Owen, N., Stevense, M. et al. Altered cohesin gene dosage affects mammalian meiotic chromosome structure and behavior PLoS Genet., 9 (2013),p. e1003241
    [47]
    Nasmyth, K., Haering, C.H. Cohesin: its roles and mechanisms Ann. Rev. Genet., 43 (2009),pp. 525-558
    [48]
    Nativio, R., Wendt, K.S., Ito, Y. et al. PLoS Genet., 5 (2009),p. e1000739
    [49]
    Nishiyama, T., Ladurner, R., Schmitz, J. et al. Sororin mediates sister chromatid cohesion by antagonizing WAPL Cell, 143 (2011),pp. 737-749
    [50]
    Nowack, M.K., Grini, P.E., Jakoby, M.J. et al. A positive signal from the fertilization of the egg cell sets off endosperm proliferation in angiosperm embryogenesis Nat. Genet., 38 (2006),pp. 63-67
    [51]
    Pagnussat, G.C., Yu, H.J., Sundaresana, V. Plant Cell, 19 (2007),pp. 3578-3592
    [52]
    Panizza, S., Tanaka, T.U., Hochwagen, A. et al. PDS5 cooperates with cohesin in maintaining sister chromatid cohesion Curr. Biol., 10 (2000),pp. 1557-1564
    [53]
    Parelho, V., Hadjur, S., Spivakov, M. et al. Cohesins functionally associate with CTCF on mammalian chromosome arms Cell, 132 (2008),pp. 422-433
    [54]
    Pasierbek, P., Jantsch, M., Melcher, M. et al. Genes Dev., 15 (2001),pp. 1349-1360
    [55]
    Pauli, A., van Bemmel, J.G., Oliveira, R.A. et al. Curr. Biol., 20 (2010),pp. 1787-1798
    [56]
    Peirson, B.N., Bowling, S.E., Makaroff, C.A. Plant J., 11 (1997),pp. 659-669
    [57]
    Peric-Hupkes, D., van Steensel, B. Linking cohesin to gene regulation Cell, 132 (2008),pp. 925-928
    [58]
    Peters, J.M. The many functions of cohesin-different rings to rule them all? EMBO J., 31 (2012),pp. 2061-2063
    [59]
    Riedel, C.G., Katis, V.L., Katou, Y. et al. Protein phosphatase 2a protects centromeric sister chromatid cohesion during meiosis I Nature, 441 (2006),pp. 53-61
    [60]
    Ross, K.J., Fransz, P., Jones, G.H. Chromosome Res., 4 (1996),pp. 507-516
    [61]
    Rubio, E.D., Reiss, D.J., Weicsh, P.L. et al. CTCF physically links cohesin to chromatin Proc. Natl. Acad. Sci. USA, 105 (2008),pp. 8309-8314
    [62]
    Rudra, S., Skibbens, R.V. Cohesin codes - interpreting chromatin architecture and the many facets of cohesin function J. Cell Sci., 126 (2013),pp. 31-41
    [63]
    Seitan, V.C., Merkenschlager, M. Cohesin and chromatin organisation Curr. Opin. Genet. Dev., 22 (2012),pp. 93-100
    [64]
    Siomos, M.F., Badrinath, A., Pasierbek, P. et al. Curr. Biol., 23 (2001),pp. 1825-1835
    [65]
    Sofueva, S., Hadjur, S. Cohesin-mediated chromatin interactions-into the third dimension of gene regulation Brief. Funct. Genomics, 11 (2012),pp. 205-216
    [66]
    Sumara, I., Vorlaufer, E., Stukenberg, P. et al. The dissociation of cohesin from chromosomes in prophase is regulated by polo-like kinase Mol. Cell, 9 (2002),pp. 515-525
    [67]
    Sutani, T., Kawaguchi, T., Kanno, R. et al. Budding yeast WPL1 (RAD61)-PDS5 complex counteracts sister chromatid cohesion-establishing reaction Curr. Biol., 19 (2009),pp. 492-497
    [68]
    Uhlmann, F., Lottspeich, F., Nasmyth, K. Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit SCC1 Nature, 400 (1999),pp. 37-42
    [69]
    Waizenegger, I.C., Hauf, S., Meinke, A. et al. Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase Cell, 103 (2000),pp. 399-410
    [70]
    Yang, X., Timofejeva, L., Ma, H. et al. J. Cell Sci., 19 (2006),pp. 4025-4032
    [71]
    Yuan, L., Yang, X., Makaroff, C.A. Plant cohesins, common themes and unique roles Curr. Protein Pept. Sci., 12 (2011),pp. 93-104
    [72]
    Yuan, L., Yang, X.H., Ellis, J.L. et al. Plant J., 71 (2012),pp. 147-160
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Article Metrics

    Article views (76) PDF downloads (2) Cited by ()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return