Characterization of the three Arabidopsis thaliana RAD21 cohesins reveals differential responses to ionizing radiation

Costa-Nunes, José A. da; Bhatt, Anuj M.; O'Shea, Shannon; West, Claudia; Bray, Clifford M.; Grossniklaus, Ueli; Dickinson, H. G.

doi:10.1093/jxb/erj083

Cited by 41 publications

(66 citation statements)

References 75 publications

(138 reference statements)

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“…Constitutive expression of cohesin subunits using 35S promoter was shown to perturb Arabidopsis development (Yuan et al, 2014). To avoid this effect, we used the ABA INSENSITIVE 3 (ABI3) promoter, which is relatively weak and, in seeds, mostly embryo specific (Devic et al, 1996;Ng et al, 2004), to drive expression of TagRFP fusions of the four known Arabidopsis kleisin subunits, RAD21.1/SYN2, RAD21.1.2/SYN3, RAD21.3/SYN4 and Rec8/SYN1 (da Costa-Nunes et al, 2006;Dong et al, 2001). The obtained constructs were introduced into wild-type and Atscc4-1/AtSCC4 backgrounds.…”

Section: In Vivo Imaging Of Cohesin Loadingmentioning

confidence: 99%

“…The Arabidopsis genome encodes four kleisin subunits (Fig. 1A): the meiosis-specific SYN1 (Cai et al, 2003) and SYN3, involved in gene expression of meiotic genes, but also expressed in somatic cells (Yuan et al, 2012;Jiang et al, 2007), and SYN2 and SYN4, which have been suggested to participate in mitotic cell division (da Costa-Nunes et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

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The Arabidopsis homolog of Scc4/MAU2 is essential for embryogenesis

Minina¹,

Reza²,

Gutiérrez-Beltrán³

et al. 2017

Development

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Factors regulating dynamics of chromatin structure have direct impact on expression of genetic information. Cohesin is a multi-subunit protein complex that is crucial for pairing sister chromatids during cell division, DNA repair and regulation of gene transcription and silencing. In non-plant species, cohesin is loaded on chromatin by the Scc2-Scc4 complex (also known as the NIBPL-MAU2 complex). Here, we identify the Arabidopsis homolog of Scc4, which we denote Arabidopsis thaliana (At)SCC4, and show that it forms a functional complex with AtSCC2, the homolog of Scc2. We demonstrate that AtSCC2 and AtSCC4 act in the same pathway, and that both proteins are indispensable for cell fate determination during early stages of embryo development. Mutant embryos lacking either of these proteins develop only up to the globular stage, and show the suspensor overproliferation phenotype preceded by ectopic auxin maxima distribution. We further establish a new assay to reveal the AtSCC4-dependent dynamics of cohesin loading on chromatin in vivo. Our findings define the Scc2-Scc4 complex as an evolutionary conserved machinery controlling cohesin loading and chromatin structure maintenance, and provide new insight into the plant-specific role of this complex in controlling cell fate during embryogenesis.

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Section: In Vivo Imaging Of Cohesin Loadingmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The Arabidopsis homolog of Scc4/MAU2 is essential for embryogenesis

Minina¹,

Reza²,

Gutiérrez-Beltrán³

et al. 2017

Development

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“…Mutants of cohesin genes, smc1 (titan8) and smc3 (titan7), show aberrant seed development in Arabidopsis (Liu et al, 2002). One of the four a-kleisin paralogs in Arabidopsis, SYN1/DETERMINATE, INFERTILE1, is necessary for sister chromatid cohesion and correct chromosome segregation during meiosis but is expressed also in meristematic tissues (Peirson et al, 1997;Bai et al, 1999;Bhatt et al, 1999;Cai et al, 2003;da Costa-Nunes et al, 2006). The other three paralogs, SYN2/RAD21.1, SYN3/RAD21.2, and SYN4/RAD21.3, are expressed in all plant tissues and may participate in sister chromatid cohesion.…”

Section: Structural Maintenance Of Chromosomes (Smc)mentioning

confidence: 99%

The STRUCTURAL MAINTENANCE OF CHROMOSOMES 5/6 Complex Promotes Sister Chromatid Alignment and Homologous Recombination after DNA Damage inArabidopsis thaliana

et al. 2009

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Sister chromatids are often arranged as incompletely aligned entities in interphase nuclei of Arabidopsis thaliana. The STRUCTURAL MAINTENANCE OF CHROMOSOMES (SMC) 5/6 complex, together with cohesin, is involved in double-strand break (DSB) repair by sister chromatid recombination in yeasts and mammals. Here, we analyzed the function of genes in Arabidopsis. The wild-type allele of SMC5 is essential for seed development. Each of the two SMC6 homologs of Arabidopsis is required for efficient repair of DNA breakage via intermolecular homologous recombination in somatic cells. Alignment of sister chromatids is enhanced transiently after X-irradiation (and mitomycin C treatment) in wild-type nuclei. In the smc5/6 mutants, the x-ray-mediated increase in sister chromatid alignment is much lower and delayed. The reduced S phase-established cohesion caused by a knockout mutation in one of the a-kleisin genes, SYN1, also perturbed enhancement of sister chromatid alignment after irradiation, suggesting that the S phase-established cohesion is a prerequisite for correct DSB-dependent cohesion. The radiation-sensitive51 mutant, deficient in heteroduplex formation during DSB repair, showed wild-type frequencies of sister chromatid alignment after X-irradiation, implying that the irradiation-mediated increase in sister chromatid alignment is a prerequisite for, rather than a consequence of, DNA strand exchange between sister chromatids. Our results suggest that the SMC5/6 complex promotes sister chromatid cohesion after DNA breakage and facilitates homologous recombination between sister chromatids.

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“…The Arabidopsis (Arabidopsis thaliana) genome contains orthologs for many of the cohesion-associated genes that have been identified in yeast, and studies have shown that the cohesion machinery is generally conserved in Arabidopsis (Bai et al, 1999;Bhatt et al, 1999;Dong et al, 2001;Chelysheva et al, 2005;Lam et al, 2005;da Costa-Nunes et al, 2006;Liu and Makaroff, 2006;Jiang et al, 2007). However, essentially nothing is known about how sister chromatid cohesion is established in plants.…”

mentioning

confidence: 99%

Proper Levels of the Arabidopsis Cohesion Establishment Factor CTF7 Are Essential for Embryo and Megagametophyte, But Not Endosperm, Development

Jiang

Xia

et al. 2010

Plant Physiology

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CTF7 is an essential gene in yeast that is required for the formation of sister chromatid cohesion. While recent studies have provided insights into how sister chromatid cohesion is established, less is known about how specifically CTF7 facilitates the formation of cohesion, and essentially nothing is known about how sister chromatid cohesion is established in plants. In this report, we describe the isolation and characterization of CTF7 from Arabidopsis (Arabidopsis thaliana). Arabidopsis CTF7 is similar to Saccharomyces cerevisiae CTF7 in that it lacks an amino-terminal extension, exhibits acetyltransferase activity, and can complement a yeast ctf7 temperature-sensitive mutation. CTF7 transcripts are found throughout the plant, with the highest levels present in buds. Seeds containing T-DNA insertions in CTF7 exhibit mitotic defects in the zygote. Interestingly, the endosperm developed normally in ctf7 seeds, suggesting that CTF7 is not essential for mitosis in endosperm nuclei. Minor defects were observed in female gametophytes of ctf7 1/2 plants, and plants that overexpress CTF7 exhibited female gametophyte lethality. Pollen development appeared normal in both CTF7 knockout and overexpression plants. Therefore, proper levels of CTF7 are critical for female gametophyte and embryo development but not for the establishment of mitotic cohesion during microgametogenesis or during endosperm development.The proper formation of sister chromatid cohesion and its subsequent release at the metaphase-to-anaphase transition is essential for the proper segregation of genetic material during cell division. It is critical for the compaction of chromosomes and their bipolar attachment to the spindle, DNA double-strand break repair, and the regulation of gene expression (for review, see Nasmyth and Haering, 2009). Sister chromatid cohesion is controlled by the cohesin complex, which consists of a heterodimer of Structural Maintenance of Chromosome (SMC) proteins, SMC1 and SMC3, Sister Chromatid Cohesion (SCC) protein SCC3, and SCC1, an a-kleisin protein. Perhaps the most widely accepted model of how cohesin functions has been referred to as the ring model, where the cohesin ring encircles the replicated sisters, holding them together until SCC1 cleavage by separase at the metaphase-to-anaphase transition opens the ring, allowing the release of the sister chromatids (for review, see Nasmyth and Haering, 2009).

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Characterization of the three Arabidopsis thaliana RAD21 cohesins reveals differential responses to ionizing radiation

Cited by 41 publications

References 75 publications

The Arabidopsis homolog of Scc4/MAU2 is essential for embryogenesis

The Arabidopsis homolog of Scc4/MAU2 is essential for embryogenesis

The STRUCTURAL MAINTENANCE OF CHROMOSOMES 5/6 Complex Promotes Sister Chromatid Alignment and Homologous Recombination after DNA Damage inArabidopsis thaliana

Proper Levels of the Arabidopsis Cohesion Establishment Factor CTF7 Are Essential for Embryo and Megagametophyte, But Not Endosperm, Development

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