Complex functions of two conserved plant metacaspases reveal multiple wound-induced pathways involved in defense and growth control

Response to wounding in multicellular organisms such as plants is critical for heightened pathogen defense as well as for induction of tissue healing and regeneration. While there is evidence for common induction of defense related genes between responses upon wounding to those activated in basal immunity, the key regulator(s) for wound-induced gene expression and the extent of signaling overlap with those of plant defense are unknown. In this work, we examined the roles for two subgroups of Type II metacaspases, highly conserved cysteine proteases that are structural homologs to metazoan caspases, on wound-induced changes in the transcript landscape of Arabidopsis. Using comparative transcriptomics with different genetic backgrounds, we sought to determine how these conserved plant proteases may serve as key mediators for transcriptional response to wounding. Remarkably, we found between 84% to 99% of the hundreds of highly activated genes (greater than 8-fold increased) are dependent on AtMC4 function. About 30% of these AtMC4-dependent wound-induced genes are likely to be mediated through a ProPep1-AtMC4-Pep1 switch for downstream signaling. AtMC9 on the other hand play a significant but less prominent role for mediating distinct and overlapping sets of defense related genes to those regulated by AtMC4. Lastly, our work revealed both AtMC4 and AtMC9 also function as negative regulators for potential downstream target genes that are wound-activated only in the mutant backgrounds. In addition to uncovering their distinct, but overlapping, roles in the global wounding response, our study also revealed the identities of overlapping as well as distinct downstream target genes between wound response and basal immunity.