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.

Ethylene aplenty signals soil compaction: It's tough to drive a spade through compacted soil, and plant roots seem to have the same problem when growing in compacted ground. Pandey et al. found that the problem is not, however, one of physical resistance but rather inhibition of growth through a signaling pathway. The volatile plant hormone ethylene will diffuse through aerated soil, but compacted soil reduces such diffusion, increasing the concentration of ethylene near root tissues. The cellular signaling cascades triggered by too much ethylene stop root growth. Therefore, gaseous diffusion serves as a readout of soil compaction for plant roots growing in search of productive nutrition. Science , this issue p. 276

Summary: Submerged plants ultimately suffer from shortage in cellular oxygen availability (hypoxia) as a result of impaired gas diffusion underwater. The gaseous plant hormone ethylene is rapidly entrapped in submerged plant tissues and is an established regulator of morphological and anatomical flood‐adaptive responses. Multiple recent discoveries suggest that ethylene also plays a crucial role in hypoxia anticipation and metabolic acclimation during plant submergence. Ethylene was shown to accelerate and enhance the hypoxic response through enhanced stability of specific transcription factors (group VII ethylene response factors). Moreover, we suggest that ethylene could play an important role in the induction of autophagy and promote reactive oxygen species amelioration, thereby contributing to enhanced survival during flooding, hypoxia, and reoxygenation stress.

The polycomb repressive complex 2 (PRC2) regulates epigenetic gene repression in eukaryotes. Mechanisms controlling its developmental specificity and signal-responsiveness are poorly understood. Here, we identify an oxygen-sensitive N-terminal (N-) degron in the plant PRC2 subunit VERNALIZATION(VRN) 2, a homolog of animal Su(z)12, that promotes its degradation via the N-end rule pathway. We provide evidence that this N-degron arose early during angiosperm evolution via gene duplication and N-terminal truncation, facilitating expansion of PRC2 function in flowering plants. We show that proteolysis via the N-end rule pathway prevents ectopic VRN2 accumulation, and that hypoxia and long-term cold exposure lead to increased VRN2 abundance, which we propose may be due to inhibition of VRN2 turnover via its N-degron. Furthermore, we identify an overlap in the transcriptional responses to hypoxia and prolonged cold, and show that VRN2 promotes tolerance to hypoxia. Our work reveals a mechanism for post-translational regulation of VRN2 stability that could potentially link environmental inputs to the epigenetic control of plant development.

Plant submergence is a major abiotic stress that impairs plant performance. Underwater, reduced gas diffusion exposes submerged plant cells to an environment that is enriched in gaseous ethylene and is limited in oxygen (O₂) availability (hypoxia). The capacity for plant roots to avoid and/or sustain critical hypoxia damage is essential for plants to survive waterlogging. Plants use spatiotemporal ethylene and O₂ dynamics as instrumental flooding signals to modulate potential adaptive root growth and hypoxia stress acclimation responses. However, how non-adapted plant species modulate root growth behaviour during actual waterlogged conditions to overcome flooding stress has hardly been investigated. Here we discuss how changes in the root growth rate, lateral root formation, density and growth angle of non-flood adapted plant species (mainly Arabidopsis) could contribute to avoiding and enduring critical hypoxic conditions. In addition, we discuss the current molecular understanding of how ethylene and hypoxia signalling control these adaptive root growth responses. We propose that future research would benefit from less artificial experimental designs to better understand how plant roots respond to and survive waterlogging. This acquired knowledge would be instrumental to guide targeted breeding of flood-tolerant crops with more resilient root systems.