AtCAMTA4 negatively regulates salinity stress response via regulation of ROS and Na+/K+ homeostasis.

Abstract

Calmodulin-binding transcription activators (CAMTAs) are key components of calcium-mediated regulation of diverse developmental and stress-responsive processes in plants. Although the functions of several Arabidopsis CAMTA family members have been investigated, the role of CAMTA4 remained largely unexplored. In the present study, we demonstrate that CAMTA4 acts as a negative regulator of salinity tolerance. Integrated physiological, transcriptomic, metabolomic and small RNA analyses revealed that camta4 mutants exhibit reduced membrane damage, lower Na+ and reactive oxygen species (ROS) accumulation, and extensive transcriptional reprogramming under salt stress. Reduced Na + accumulation appears to result primarily from enhanced SOS1-mediated Na + exclusion and attenuated induction of HKT1;1. While stable levels of AKT1 accompanied with elevated levels of TPK1 suggests complementary mechanisms to maintain cellular Na+/K+ homeostasis by preferential mobilization of vacuolar K+ reserves. Lower ROS levels were associated with differential expression of CAT2 and CAT3, together with increased accumulation of proline, glutamine and lysine, indicating coordinated regulation of antioxidant defence and osmo-protective metabolism. In addition, CAMTA4 substantially reshaped the sRNA landscape by regulating conserved salinity-responsive miRNA modules, including miR156-SPL9, miR169-NF-YA and miR408-LAC thereby extending its regulatory influence into post-transcriptional gene regulation. Although CAMTA3/4/6 have all been implicated in salinity responses, their mechanisms appear to be distinct. Unlike the pleiotropic camta3, camta4 mutants exhibited no obvious developmental abnormalities under normal growth conditions, suggesting that CAMTA4 has evolved a specialized regulatory niche. The apparent absence of major developmental defects also identifies CAMTA4 as a promising target for engineering salinity tolerance with minimal pleiotropic effects.