Flooding is detrimental for nearly all higher plants, including crops. The compound stress elicited by slow gas exchange and low light levels under water is responsible for both a carbon and an energy crisis ultimately leading to plant death. The endogenous concentrations of four gaseous compounds, oxygen, carbon dioxide, ethylene, and nitric oxide, change during the submergence of plant organs in water. These gases play a pivotal role in signal transduction cascades, leading to adaptive processes such as metabolic adjustments and anatomical features. Of these gases, ethylene is seen as the most consistent, pervasive, and reliable signal of early flooding stress, most likely in tight interaction with the other gases. The production of reactive oxygen species (ROS) in plant cells during flooding and directly after subsidence, during which the plant is confronted with high light and oxygen levels, is characteristic for this abiotic stress. Low, well-controlled levels of ROS are essential for adaptive signaling pathways, in interaction with the other gaseous flooding signals. On the other hand, excessive uncontrolled bursts of ROS can be highly damaging for plants. Therefore, a fine-tuned balance is important, with a major role for ROS production and scavenging. Our understanding of the temporal dynamics of the four gases and ROS is basal, whereas it is likely that they form a signature readout of prevailing flooding conditions and subsequent adaptive responses.

Timely perception of adverse environmental changes is critical for survival. Dynamic changes in gases are important cues for plants to sense environmental perturbations, such as submergence. In Arabidopsis thaliana, changes in oxygen and nitric oxide (NO) control the stability of ERFVII transcription factors. ERFVII proteolysis is regulated by the N-degron pathway and mediates adaptation to flooding-induced hypoxia. However, how plants detect and transduce early submergence signals remains elusive. Here we show that plants can rapidly detect submergence through passive ethylene entrapment and use this signal to pre-adapt to impending hypoxia. Ethylene can enhance ERFVII stability prior to hypoxia by increasing the NO-scavenger PHYTOGLOBIN1. This ethylene-mediated NO depletion and consequent ERFVII accumulation pre-adapts plants to survive subsequent hypoxia. Our results reveal the biological link between three gaseous signals for the regulation of flooding survival and identifies key regulatory targets for early stress perception that could be pivotal for developing flood-tolerant crops.

The volatile hormone ethylene is an important regulator of plant-adaptive responses to flooding stress.

Significance: Flooding 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 inArabidopsis thalianathat 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.

Plants frequently encounter a range of abiotic stresses and their combinations. Even though stresses rarely occur in isolation, research on plant stress resilience typically focuses on single environmental stressors. Plant responses to abiotic stress combinations are often distinct from corresponding individual stresses. Factors determining the outcomes of combined stresses are complex and multifaceted. In this review, we summarize advancements in our understanding of the mechanisms underlying plant responses to co-occurring (combined and sequential) abiotic stresses, focusing on morphological, physiological, developmental, and molecular aspects. Comprehensive understanding of plant acclimation, including the signaling and response mechanisms to combined and individual stresses, can contribute to the development of strategies for enhancing plant resilience in dynamic environments.