Condensin II Alleviates DNA Damage and Is Essential for Tolerance of Boron Overload Stress in Arabidopsis  

Abstract

Although excess boron (B) is known to negatively affect plant growth, its molecular mechanism of toxicity is unknown. We previously isolated two Arabidopsis thaliana mutants, hypersensitive to excess B (heb1-1 and heb2-1). In this study, we found that HEB1 and HEB2 encode the CAP-G2 and CAP-H2 subunits, respectively, of the condensin II protein complex, which functions in the maintenance of chromosome structure. Growth of Arabidopsis seedlings in medium containing excess B induced expression of condensin II subunit genes. Simultaneous treatment with zeocin, which induces DNA double-strand breaks (DSBs), and aphidicolin, which blocks DNA replication, mimicked the effect of excess B on root growth in the heb mutants. Both excess B and the heb mutations upregulated DSBs and DSB-inducible gene transcription, suggesting that DSBs are a cause of B toxicity and that condensin II reduces the incidence of DSBs. The Arabidopsis T-DNA insertion mutant atr-2, which is sensitive to replication-blocking reagents, was also sensitive to excess B. Taken together, these data suggest that the B toxicity mechanism in plants involves DSBs and possibly replication blocks and that plant condensin II plays a role in DNA damage repair or in protecting the genome from certain genotoxic stressors, particularly excess B.

Condensins: universal organizers of chromosomes with diverse functions

“…As mentioned earlier, a recent genetic study in A. thaliana has shown that condensin II is likely to be involved in DSB response and repair (Sakamoto et al 2011). A genetic screen for mutants that exhibit hypersensitivity to excess boron identified two mutants (heb1-1 and heb2-1) that turned out to be defective in the genes encoding the CAP-G2 and CAP-H2 subunits of condensin II, respectively.…”

“…Whereas the A. thaliana genome has a single essential gene (AtCAP-C) encoding SMC4 (Siddiqui et al 2006), it possesses two paralogous genes for SMC2, known as AtCAP-E1 and AtCAP-E2 (Siddiqui et al 2003 +/À E2 À/À plant results in meristem disorganization and fasciation, indicating that SMC2 activity above a certain threshold is required for proper development of A. thaliana. Very recently, a genetic screen for mutants that exhibit hypersensitivity to excess boron has led to the somewhat surprising conclusion that condensin II is nonessential for mitosis and instead plays a role in alleviating DNA damage (Sakamoto et al 2011). Whereas genetic studies have yet to be reported for the genes encoding condensin I-specific subunits, it is anticipated that condensin I is sufficient for mitotic chromosome assembly and segregation in this organism.…”

Chromosome Dynamics during Mitosis

“…Moreover, the condensin II-specific subunits apparently play less-important roles than the condensin I-specific subunits during the mitotic chromosome cycle in organisms, such as Drosophila (Savvidou et al 2005;Herzog et al 2013), Arabidopsis thaliana (Sakamoto et al 2011), and C. merolae (Fujiwara et al 2013). Consistent with this view, genome-wide screens for genes affecting chromosome condensation in yeasts and Drosophila have identified condensin I and topoisomerase II (Hirano et al 1986;Samejima et al 1993;Goshima et al 2007;Petrova et al 2012), implicating that no more "major" condensation factors remain to be discovered, at least in these organisms.…”

AtMMS21, an SMC5/6 Complex Subunit, Is Involved in Stem Cell Niche Maintenance and DNA Damage Responses in Arabidopsis Roots

“…To examine whether the mms21-1 roots had constitutive activation of DNA damage responses, we first measured the expression of the DSB-inducible genes PARP1, BRCA1, and RAD51 by qRT-PCR (Inagaki et al, 2006;Sakamoto et al, 2011). Plants were grown under normal growth conditions, and the transcript levels of all three genes were higher in the mms21-1 roots than in the wild-type plants (Fig.…”