Ethylene-mediated phosphorylation of ORESARA1 induces sequential leaf death during flooding in Arabidopsis

The volatile phytohormone ethylene is a major regulator of plant adaptive responses to flooding. In flooded plant tissues, it quickly increases to high concentrations due to its low solubility and diffusion rates in water. The passive, quick and consistent accumulation of ethylene in submerged plant tissues makes it a reliable cue for plants to trigger flood-acclimative responses. However, persistent ethylene accumulation can also have negative effects, notably accelerated leaf senescence. Ethylene is a well-established positive regulator of senescence which is a natural element of plant ageing. However stress-induced senescence hampers the photosynthetic capacity and stress recovery of plants. In submerged Arabidopsis shoots, senescence follows a strict age-dependent pattern starting with the older leaves. Although mechanisms underlying ethylene-mediated senescence have been uncovered, it is unclear how submerged plants avoid an indiscriminate breakdown of leaves despite high systemic accumulation of ethylene. Here we demonstrate in Arabidopsis plants that even though submergence triggers a leaf-age independent activation of ethylene signaling via EIN3, senescence was initiated only in the old leaves. This EIN3 stabilization also led to the overall transcript and protein accumulation of the senescence-promoting transcription factor ORESARA1 (ORE1). ORE1 protein accumulated in both old and young leaves during submergence. However, leaf age-dependent senescence could be explained by ORE1 activation via phosphorylation only in old leaves. Our results unravel a mechanism by which plants regulate the speed and pattern of senescence during environmental stresses like flooding. Such an age-dependent phosphorylation of ORE1 ensures that older expendable leaves are dismantled first, thus prolonging the life of younger leaves and meristematic tissues vital to whole plant survival.