Transcriptome profiling implicates ANNEXIN1 in light sensitivity and hormonal balance maintenance in Arabidopsis thaliana

Annexins are a conserved family of calcium- and phospholipid-binding proteins. Despite their ubiquity and ancient origin, their physiological functions are not fully understood. Numerous studies have shown that the ectopic expression of some annexins can ameliorate the adverse effects of numerous abiotic stresses through modulation of reactive oxygen species accumulation and/or abscisic acid signaling. To gain further insight into the molecular mechanisms of this activity, we studied transgenic Arabidopsis thaliana (Arabidopsis) plants with increased expression of ANNEXIN1 (ATANN1) in the wild-type Col-0 lines (Col-OX) and in GO mutants (GO-OX) synchronously accumulating high levels of hydrogen peroxide in chloroplasts. Comprehensive biochemical and transcriptomic analyses led us to propose that ATANN1 modulates the turnover of ascorbate and glutathione, thereby affecting various redox-dependent processes, including photosynthesis, and phytohormonal signaling. Compared to the non-transgenic line, the overexpression of ATANN1 resulted in a two-to threefold increase in jasmonic acid accumulation in response to high light and oxidative stress in both genetic backgrounds analyzed (about 200 % compared to the control conditions in WT, while about 300-400 % in transgenic lines). This also affected salicylic acid-activated transcriptional reprogramming, although a slight up-regulation of this phytohormone occurred only in GO-OX. Overall, ATANN1 affects the integration of the SA and JA signaling pathways in such conditions. Our results provide compelling evidence that during stress, ATANN1 is involved in the regulation of redox homeostasis and the orchestration of diverse hormone-mediated signaling pathways, thereby fine-tuning the plant response to stress.