Distinct processes contributing to post-submergence recovery determine leaf age-specific flood resilience in...

While the molecular mechanisms mediating submergence tolerance have been extensively studied, those underpinning age-dependent resilience remain poorly characterized. In Arabidopsis thaliana, submergence elicits a leaf-age-dependent phenotype in which senescence and death progress across an age gradient starting with older leaves. Here, we sought to investigate the mechanisms mediating the observed differential flood resilience by interrogating leaf-age-specific transcriptome and proteome changes during submergence and recovery. Following submergence, most age-dependent differences were in the magnitude or speed of transcript abundance changes, whereas qualitative leaf-age-dependent responses were most apparent during recovery. This included a strong desiccation response in old leaves despite a stronger Abscisic Acid (ABA)-signaling response. Physiological measurements suggested that faster dehydration was facilitated by submergence-mediated reduction of ABA sensitivity but was not associated with differences in stomatal conductance or cuticle integrity. We also observed a stronger induction in young shoot tissue of genes associated with endoplasmic reticulum (ER) stress and the unfolded protein response (UPR). Mutants disabled in both UPR signaling branches were affected in new leaf formation and in the ability to restore the proteome, but not in senescence, suggesting that young tissues activate ER stress recovery to permit continuation of growth. Among mitochondrial membrane proteins differentially regulated in young leaves, loss of mitochondrial voltage-dependent anion channel function impacted submergence-recovery tolerance. Our data reveal multiple mechanisms underlying leaf-age-dependent differential submergence recovery and demonstrate how an interplay between age-related developmental traits and stress signaling pathways determines tolerance.