Differential leaf flooding resilience in Arabidopsis thaliana is controlled by ethylene signaling-activated and age-dependent phosphorylation of ORESARA1.

The phytohormone ethylene is a major regulator of plant adaptive responses to flooding. In flooded plant tissues, ethylene quickly increases to high concentrations owing to its low solubility and diffusion rates in water. Ethylene accumulation in submerged plant tissues makes it a reliable cue for triggering flood acclimation responses, including metabolic adjustments to cope with flood-induced hypoxia. However, persistent ethylene accumulation also accelerates leaf senescence. Stress-induced senescence hampers photosynthetic capacity and stress recovery. In submerged Arabidopsis, 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 indiscriminate breakdown of leaves despite high systemic ethylene accumulation. We demonstrate that although submergence triggers leaf-age-independent activation of ethylene signaling via EIN3 in Arabidopsis, senescence is initiated only in old leaves. EIN3 stabilization also leads to overall transcript and protein accumulation of the senescence-promoting transcription factor ORESARA1 (ORE1) in both old and young leaves during submergence. However, leaf-age-dependent senescence can be explained by ORE1 protein activation via phosphorylation specifically in old leaves, independent of the previously identified age-dependent control of ORE1 via miR164. A systematic analysis of the roles of the major flooding stress cues and signaling pathways shows that only the combination of ethylene and darkness is sufficient to mimic submergence-induced senescence involving ORE1 accumulation and phosphorylation. Hypoxia, most often associated with flooding stress in plants, appears to have no role in these processes. Our results reveal a mechanism by which plants regulate the speed and pattern of senescence during environmental stresses such as flooding. Age-dependent ORE1 activity ensures that older, expendable leaves are dismantled first, thus prolonging the life of younger leaves and meristematic tissues that are vital to whole-plant survival.

Ethylene augments root hypoxia tolerance via growth cessation and reactive oxygen species amelioration.

Flooded plants experience impaired gas diffusion underwater, leading to oxygen deprivation (hypoxia). The volatile plant hormone ethylene is rapidly trapped in submerged plant cells and is instrumental for enhanced hypoxia acclimation. However, the precise mechanisms underpinning ethylene-enhanced hypoxia survival remain unclear. We studied the effect of ethylene pretreatment on hypoxia survival of Arabidopsis (Arabidopsis thaliana) primary root tips. Both hypoxia itself and re-oxygenation following hypoxia are highly damaging to root tip cells, and ethylene pretreatments reduced this damage. Ethylene pretreatment alone altered the abundance of transcripts and proteins involved in hypoxia responses, root growth, translation, and reactive oxygen species (ROS) homeostasis. Through imaging and manipulating ROS abundance in planta, we demonstrated that ethylene limited excessive ROS formation during hypoxia and subsequent re-oxygenation and improved oxidative stress survival in a PHYTOGLOBIN1-dependent manner. In addition, we showed that root growth cessation via ethylene and auxin occurred rapidly and that this quiescence behavior contributed to enhanced hypoxia tolerance. Collectively, our results show that the early flooding signal ethylene modulates a variety of processes that all contribute to hypoxia survival.

Age-Dependent Abiotic Stress Resilience in Plants.

Developmental age is a strong determinant of stress responses in plants. Differential susceptibility to various environmental stresses is widely observed at both the organ and whole-plant level. While it is clear that age determines stress susceptibility, the causes, regulatory mechanisms, and functions are only now beginning to emerge. Compared with concepts on age-related biotic stress resilience, advancements in the abiotic stress field are relatively limited. In this review, we focus on current knowledge of ontogenic resistance to abiotic stresses, highlighting examples at the organ (leaf) and plant level, preceded by an overview of the relevant concepts in plant aging. We also discuss age-related abiotic stress resilience mechanisms, speculate on their functional relevance, and outline outstanding questions.

A stress recovery signaling network for enhanced flooding tolerance in Arabidopsis thaliana.

Abiotic stresses in plants are often transient, and the recovery phase following stress removal is critical. Flooding, a major abiotic stress that negatively impacts plant biodiversity and agriculture, is a sequential stress where tolerance is strongly dependent on viability underwater and during the postflooding period. Here we show that in Arabidopsis thaliana accessions (Bay-0 and Lp2-6), different rates of submergence recovery correlate with submergence tolerance and fecundity. A genome-wide assessment of ribosome-associated transcripts in Bay-0 and Lp2-6 revealed a signaling network regulating recovery processes. Differential recovery between the accessions was related to the activity of three genes: RESPIRATORY BURST OXIDASE HOMOLOG D, SENESCENCE-ASSOCIATED GENE113, and ORESARA1, which function in a regulatory network involving a reactive oxygen species (ROS) burst upon desubmergence and the hormones abscisic acid and ethylene. This regulatory module controls ROS homeostasis, stomatal aperture, and chlorophyll degradation during submergence recovery. This work uncovers a signaling network that regulates recovery processes following flooding to hasten the return to prestress homeostasis.