SignificanceFlooding due to extreme weather events can be highly detrimental to plant development and yield. Speedy recovery following stress removal is an important determinant of tolerance, yet mechanisms regulating this remain largely uncharacterized. We identified a regulatory network in Arabidopsis thaliana that controls water loss and senescence to influence recovery from prolonged submergence. Targeted control of the molecular mechanisms facilitating stress recovery identified here could potentially improve performance of crops in flood-prone areas.

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. The Concept of AgingThe definitions of plant aging (see Glossary) are diverse. One might think of aging to comprehend the entire plant life cycle: from seed to senescence. However, this cycle is different for annuals and perennials. Annuals and biennials are semelparous (monocarpic) species that undergo their complete life cycle in one or two growing seasons, respectively. Perennials are iteroparous (polycarpic) species that live for many years with a clear disjunction between plant and organ lifespan. In this review, we mainly focus on age-related aspects of annuals, but some concepts are equivalent to specific organs of perennials that undergo repeated yearly cycles. HighlightsThe processes of aging, such as leaf development, senescence, and phase transitions from juvenile to adult plants, are genetically programmed and highly controlled by complex regulatory pathways.During aging, plants alter their organ morphology, sink-source balances, and chemical composition, including changes in redox status and hormone levels, which will collectively determine how abiotic stress signals are perceived and processed.

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.

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.

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 primary Arabidopsis thaliana 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 demonstrate that ethylene limits excessive ROS formation during hypoxia and subsequent re-oxygenation and improves oxidative stress survival. In addition, we show that ethylene leads to rapid root growth cessation and this quiescence behaviour contributes to enhanced hypoxia tolerance. Collectively, our results show that the early flooding signal ethylene modulates a variety of processes that all contribute to successful hypoxia survival.

Flooding events lead to major crop losses every year, this is expected to increase due to climate change. The resilience to flooding stress is not uniform throughout a plant: the older leaves are typically the first to die whereas the young leaves and the meristem survive for longer. In this thesis I describe some of the mechanisms that control this age-dependent flooding tolerance using the model organism Arabidopsis thaliana. During a flooding event, old leaves went into a state of senescence faster than young leaves. This process was found to be in part controlled by the transcription factor ORESARA1 (ORE1), which induced the expression of senescence-related genes primarily in old leaves. Although ORE1 protein accumulated in both old and young leaves during flooding, it was activated by phosphorylation specifically in old leaves. Knocking out ORE1 reduced the senescence of old leaves during flooding and improved flooding tolerance. When floodwaters subside, this typically poses a second round of stress for plants as they are suddenly exposed to light and air. Leaves can rapidly dehydrate during the post-flooding phase, and this was found to be more severe in old leaves than young leaves. Although old leaves recovering from flooding stress showed a strong transcriptional response to dehydration and abscisic acid (ABA), their stomata had a reduced sensitivity to ABA which could contribute to their increased water loss. The results presented in this thesis highlight how different processes lead to variation with leaf age in flooding resilience. Understanding these mechanisms can help in developing novel crop varieties that are more tolerant to flooding stress across all of their tissues.