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Summary The multifunctional protein kinase CK2 is involved in several aspects of the DNA damage response (DDR) in mammals. To gain insight into the role of CK2 in plant genome maintenance, we studied the response to genotoxic agents of an Arabidopsis CK2 dominant-negative mutant (CK2mut plants). CK2mut plants were hypersensitive to a wide range of genotoxins that produce a variety of DNA lesions. However, they were able to activate the DDR after exposure to γ irradiation, as shown by accumulation of phosphorylated histone H2AX and up-regulation of sets of radio-modulated genes. Moreover, functional assays showed that mutant plants quickly repair the DNA damage produced by genotoxins, and that they exhibit preferential use of non-conservative mechanisms, which may explain plant lethality. The chromatin of CK2mut plants was more sensitive to digestion with micrococcal nuclease, suggesting compaction changes that agreed with the transcriptional changes detected for a number of genes involved in chromatin structure. Furthermore, CK2mut plants were prone to transcriptional gene silencing release upon genotoxic stress. Our results suggest that CK2 is required in the maintenance and control of genomic stability and chromatin structure in plants, and that this process affects several functions, including the DNA damage response and DNA repair.

Protein kinase CK2 is a pleiotropic Ser/Thr kinase, evolutionary conserved in eukaryotes. Studies performed in different organisms, from yeast to humans, have highlighted the importance of CK2 in cell growth and cell-cycle control. However, the signalling pathways in which CK2 is involved have not been fully identified. In plants, the phytohormone auxin is a major regulator of cell growth. Recent discoveries have demonstrated that differential distribution of within auxin plant tissues is essential for developmental processes, and that this distribution is dependent on polar auxin transport. We report here that a dominant-negative mutant of CK2 (CK2mut) in Arabidopsis thaliana shows phenotypic traits that are typically linked to alterations in auxin-dependent processes. However, CK2mut plants exhibit normal responses to exogenous indole-3-acetic acid (IAA) indicating that they are not affected in the perception of the hormone but upstream in the pathway. We demonstrate that mutant plants are not deficient in IAA but are impaired in its transport. Using genetic and pharmacological tools we show that CK2 activity depletion hinders correct formation of auxin gradients and leads to widespread changes in the expression of auxin-related genes. In particular, members of the auxin efflux carrier family (PINs), and the protein kinase PINOID, both key regulators of auxin fluxes, were misexpressed. PIN4 and PIN7 were also found mislocalized, with accumulation in endosomal bodies. We propose that CK2 functions in the regulation of auxin-signalling pathways, particularly in auxin transport.