Phytosulfokine peptide regulates growth-immunity tradeoff through CAMTA3-mediated transcriptional signaling in Arabidopsis.

Abstract

Phytosulfokine (PSK) is a crucial phytohormone that has been identified for over three decades; however, its transcriptional signaling pathway remains largely unexplored. Here, we disclose a PSK-triggered transcriptional signaling pathway that fine-tunes the tradeoff between growth and immunity in Arabidopsis thaliana. Through forward genetics, we identified the Growth Retardation and Autoimmunity 1 (GRA1) gene, which encodes tyrosylprotein sulfotransferase (TPST), a key enzyme essential for the biosynthesis of sulfated peptides. Notably, similar to the gra1 mutant, the PSK receptor double mutants pskr1 pskr2 also exhibit the gra1-like phenotype, characterized by growth retardation and autoimmunity. Exogenous PSK application rescued the growth defects in gra1 mutants, while overexpression of the PSK precursor gene PSK3 significantly enhanced plant growth. Integrated transcriptomic, genetic, and biochemical analyses demonstrated that PSK represses salicylic acid (SA)-dependent autoimmunity via the transcription factor CAMTA3 to promote plant growth. Mechanistically, PSK attenuates CAMTA3 phosphorylation, thereby enhancing CAMTA3 protein stability and facilitating its nuclear accumulation to constrain SA-mediated autoimmunity. CaM6 and CaM7, two calmodulins that interact with the PSK receptor PSKR1, directly bind to and stabilize CAMTA3. Ectopic expression of CAMTA3 triggers autoimmunity in the cam6 cam7 double mutants but enhances plant growth in wild-type plants, demonstrating that CaM6/7 are indispensable for CAMTA3-dependent growth promotion downstream of PSK signaling. In summary, this study uncovers a previously uncharacterized transcriptional regulatory pathway through which PSK orchestrates the balance between plant growth and immunity.