WUSCHEL modulates jasmonate signaling to control the balance between growth and defense in the shoot apical meristem

Abstract

The growth-defense trade-off is an essential survival strategy for plants under environmental stress. However, how this balance is maintained at the meristematic level remains unclear. Here, we show that wounding of rosette leaves systemically inhibits inflorescence stem growth, associated with reduced cell proliferation in the inner cell layers of the shoot apical meristem (SAM), but not in the apical stem cell domain. Mechanistically, this selective cell behavior is dependent on the interplay between the growth-repressing jasmonate (JA) signaling and the growth-promoting stem cell regulator WUSCHEL (WUS). WUS mitigates wounding-induced growth inhibition by repressing JA-responsive gene expression via promoting the accumulation of JASMONATE-ZIM DOMAIN 3 (JAZ3), which encodes a JA signaling repressor. WUS on the one hand induces JAZ3 mRNA accumulation and on the other hand directly competes with the JA receptor CORONATINE INSENSITIVE1 (COI1) for JAZ3 binding, thereby inhibiting JAZ3 protein degradation. Our findings identify a WUS-JAZ3-COI1 regulatory module that coordinates the growth-defense balance in the SAM upon systemic wounding, revealing a cell-type-specific mechanism for sustaining developmental robustness of the meristem during stress response.