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Rankenberg, T.

Publications and source records attributed to Rankenberg, T..

3 recordsLinked to original sources

Leaf-age specific flood resilience in Arabidopsis thaliana is determined by distinct processes contributing to post-submergence recovery

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 this 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 ABA-signaling response. Physiological measurements suggested that faster dehydration was facilitated by a combination of submergence-mediated reduction of ABA sensitivity and higher conductance in old leaves. 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 the two UPR signaling branches were affected in new leaf formation and the ability to restore the proteome, but not in senescence, suggesting that young tissues activate ER stress recovery to permit continuation of growth. Of the 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 tolerance is determined by an interplay between age related developmental traits and stress signaling pathways.

plant biology↗

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 to trigger flood-acclimative responses, including metabolic adjustments to cope with flood-induced hypoxia. However, persistent ethylene accumulation also accelerates leaf senescence. Stress-induced senescence hampers the photosynthetic capacity and stress recovery. 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 ethylene accumulation. 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, and independent of the N-degron pathway of oxygen sensing. 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 protein activation specifically in old leaves, independent of the previously identified age-dependent control of ORE1 via miR164. Our results unravel a mechanism by which plants regulate the speed and pattern of senescence during environmental stresses like flooding. The age-dependent activity 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. Significance statementFlooded plants systemically accumulate saturating concentrations of the senescence promoting volatile hormone ethylene. Yet, leaf senescence follows a strict age-dependent gradient, thus prolonging the survival of young leaves and meristematic tissue. Here we show that in flooded plants, age-independent activation of ethylene signaling via EIN3, induces the systemic accumulation of the senescence-inducing transcription factor ORE1. Premature senescence of younger tissues is prevented by the posttranslational activation of ORE1 specifically in old leaves, where it induces the transcription of senescence-associated genes. Our results highlight how a systemic stress signal (ethylene accumulation upon flooding) induces a signaling cascade that diverges in an age-dependent manner, and eventually leads to an age-dependent physiological output (leaf senescence).

plant biology↗

Ethylene augments root hypoxia tolerance through amelioration of reactive oxygen species and growth cessation

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 hypoxia survival.

plant biology↗