The maintenance of genome integrity over cell divisions is critical for plant development and the correct transmission of genetic information to the progeny. A key factor involved in this process is the STRUCTURAL MAINTENANCE OF CHROMOSOME5 (SMC5) and SMC6 (SMC5/6) complex, related to the cohesin and condensin complexes that control sister chromatid alignment and chromosome condensation, respectively. Here, we characterize NON-SMC ELEMENT4 (NSE4) paralogs of the SMC5/6 complex in Arabidopsis (Arabidopsis thaliana). NSE4A is expressed in meristems and accumulates during DNA damage repair. Partial loss-of-function nse4a mutants are viable but hypersensitive to DNA damage induced by zebularine. In addition, nse4a mutants produce abnormal seeds, with noncellularized endosperm and embryos that maximally develop to the heart or torpedo stage. This phenotype resembles the defects in cohesin and condensin mutants and suggests a role for all three SMC complexes in differentiation during seed development. By contrast, NSE4B is expressed in only a few cell types, and loss-of-function mutants do not have any obvious abnormal phenotype. In summary, our study shows that the NSE4A subunit of the SMC5-SMC6 complex is essential for DNA damage repair in somatic tissues and plays a role in plant reproduction.

Department of Applied Biological Science Faculty of Science and Technology Tokyo University of Science Chiba 278 8510 Japan

Department of Plant and Microbial Biology and Zürich Basel Plant Science Center University of Zürich 8008 Zürich Switzerland

Department of Plant Breeding and Genetics Max Planck Institute for Plant Breeding Research 50829 Cologne Germany

Polish Academy of Sciences Franciszek Gorski Institute of Plant Physiology 30 239 Krakow Poland

The Czech Academy of Sciences Institute of Experimental Botany Centre of the Region Haná for Biotechnological and Agricultural Research 77900 Olomouc Czech Republic

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SMC5/6 complex-mediated SUMOylation stimulates DNA-protein cross-link repair in Arabidopsis

Multiple Roles of SMC5/6 Complex during Plant Sexual Reproduction

Zebularine induces enzymatic DNA-protein crosslinks in 45S rDNA heterochromatin of Arabidopsis nuclei

Kleisin NSE4 of the SMC5/6 complex is necessary for DNA double strand break repair, but not for recovery from DNA damage in Physcomitrella (Physcomitrium patens)

Structural Maintenance of Chromosomes 5/6 Complex Is Necessary for Tetraploid Genome Stability in Arabidopsis thaliana

Defects in meiotic chromosome segregation lead to unreduced male gametes in Arabidopsis SMC5/6 complex mutants

A role of the Nse4 kleisin and Nse1/Nse3 KITE subunits in the ATPase cycle of SMC5/6

Arabidopsis NSE4 Proteins Act in Somatic Nuclei and Meiosis to Ensure Plant Viability and Fertility