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

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 pre-treatment 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 pre-treatments reduced this damage. Ethylene pre-treatment 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

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

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

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

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

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

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

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 pre-treatment 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 pre-treatments reduced this damage. Ethylene pre-treatment 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