Balancing trade-offs between biotic and abiotic stress responses through leaf age-dependent variation in stress hormone cross-talk

Significance

Plants are exposed to conflicting stresses simultaneously in nature. As stress responses are costly, plants likely coordinate these responses to minimize fitness costs. The nature and extent to which plants employ inducible mechanisms to cope with combined physical and biological stresses remains unknown. We identify a genetic mechanism by which leaves of distinct ages differentially control stress-response cross-talk. At the organism level, this mechanism balances stress-response trade-offs to maintain plant growth and reproduction during combined stresses. We also show that this leaf age-dependent stress-response prioritization influences the establishment of plant-associated leaf bacterial communities. This study illustrates the importance of active balancing of stress-response trade-offs for plant fitness maintenance and for interaction with the plant microbiota.

Abstract

In nature, plants must respond to multiple stresses simultaneously, which likely demands cross-talk between stress-response pathways to minimize fitness costs. Here we provide genetic evidence that biotic and abiotic stress responses are differentially prioritized in Arabidopsis thaliana leaves of different ages to maintain growth and reproduction under combined biotic and abiotic stresses. Abiotic stresses, such as high salinity and drought, blunted immune responses in older rosette leaves through the phytohormone abscisic acid signaling, whereas this antagonistic effect was blocked in younger rosette leaves by PBS3, a signaling component of the defense phytohormone salicylic acid. Plants lacking PBS3 exhibited enhanced abiotic stress tolerance at the cost of decreased fitness under combined biotic and abiotic stresses. Together with this role, PBS3 is also indispensable for the establishment of salt stress- and leaf age-dependent phyllosphere bacterial communities. Collectively, our work reveals a mechanism that balances trade-offs upon conflicting stresses at the organism level and identifies a genetic intersection among plant immunity, leaf microbiota, and abiotic stress tolerance.