DNA-protein cross-links (DPCs) are highly toxic DNA lesions consisting of proteins covalently attached to chromosomal DNA. Unrepaired DPCs physically block DNA replication and transcription. Three DPC repair pathways have been identified in Arabidopsis (Arabidopsis thaliana) to date: the endonucleolytic cleavage of DNA by the structure-specific endonuclease MUS81; proteolytic degradation of the crosslinked protein by the metalloprotease WSS1A; and cleavage of the cross-link phosphodiester bonds by the tyrosyl phosphodiesterases TDP1 and TDP2. Here we describe the evolutionary conserved STRUCTURAL MAINTENANCE OF CHROMOSOMEs SMC5/6 complex as a crucial component involved in DPC repair. We identified multiple alleles of the SMC5/6 complex core subunit gene SMC6B via a forward-directed genetic screen designed to identify the factors involved in the repair of DPCs induced by the cytidine analog zebularine. We monitored plant growth and cell death in response to DPC-inducing chemicals, which revealed that the SMC5/6 complex is essential for the repair of several types of DPCs. Genetic interaction and sensitivity assays showed that the SMC5/6 complex works in parallel to the endonucleolytic and proteolytic pathways. The repair of zebularine-induced DPCs was associated with SMC5/6-dependent SUMOylation of the damage sites. Thus, we present the SMC5/6 complex as an important factor in plant DPC repair.

Botanical Institute Molecular Biology and Biochemistry Karlsruhe Institute of Technology Fritz Haber Weg 4 Karlsruhe 76131 Germany

Department of Cell Biology and Genetics Faculty of Science Palacký University Šlechtitelů 27 77900 Olomouc Czech Republic

Department of Plant Breeding and Genetics Max Planck Institute for Plant Breeding Research Carl von Linné Weg 10 50829 Cologne Germany

Field Crops Research Institute Agricultural Research Centre 9 Gamma Street Giza 12619 Cairo Egypt

Functional Genomics and Proteomics National Centre for Biomolecular Research Faculty of Science Masaryk University Kamenice 5 62500 Brno Czech Republic

Institute of Experimental Botany of the Czech Academy of Sciences Centre of Plant Structural and Functional Genomics Šlechtitelů 31 77900 Olomouc Czech Republic

Erratum In

Plant Cell. 2023 Aug 2;35(8):3152. doi: 10.1093/plcell/koad120. PubMed

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