The early flooding signal ethylene acclimates plants to survive low-oxygen stress

Abstract

Anthropogenic climate change has contributed to a significant increase in the frequency and severity of flooding events worldwide. Floods have a devastating impact on plant biodiversity and agricultural crop productivity, challenging global food security. In order to enhance flooding tolerance in crops, it is crucial to understand the processes that cause stunted plant growth under water and how plants control flood-adaptive mechanisms. Dynamic changes in gases are important cues for plants to sense environmental perturbations, such as submergence. In the plant model species Arabidopsis thaliana, changes in oxygen and nitric oxide (NO) control the stability of group VII Ethylene Response Factor (ERFVII) transcription factors. ERFVII proteolysis is regulated by the N-degron pathway and mediates adaptation to flooding-induced oxygen deprivation (hypoxia). However, how plants detect and transduce initial early submergence signals before hypoxia occurs, remains elusive. In this thesis we show that plants can rapidly detect submergence through passive ethylene entrapment and use this signal to pre-adapt to impending hypoxia. Moreover, using the model plants species Arabidopsis thaliana, we show that ethylene can enhance ERFVII stability prior to hypoxia by increasing the NO-scavenger PHYTOGLOBIN1. This ethylene-mediated NO depletion impairs ERFVII proteolysis and pre-adapts plants to survive subsequent hypoxia. Moreover, using a quantitative proteomics approach, we identified that ethylene regulates additional key proteins in mitochondrial respiration, oxidative stress amelioration and hypoxia responses. In addition, we show that ethylene confers oxidative stress tolerance in Arabidopsis. Finally, we show that the mechanism of ethylene-mediated hypoxia tolerance is conserved in both tolerant wild and cultivated Solanum species, but is impaired in flooding-intolerant Solanum species such as tomato. Our results reveal the biological link between three gaseous signals for the regulation of flooding survival and identifies potential regulatory targets for early stress perception that could be pivotal for developing flood-tolerant crops.