Ethylene controls translational gatekeeping to overcome flooding stress in plants.

Protein synthesis is an essential but energetically expensive cellular process that is challenged under environmental stress in plants. Recent work demonstrates that the plant hormone ethylene, through GCN2, represses general translation during flooding stress to conserve energy. Moreover, ethylene also promotes the translation of specific stress-responsive mRNAs to survive submergence stress.

Ethylene inhibits rice root elongation in compacted soil via ABA- and auxin-mediated mechanisms.

Soil compaction represents a major agronomic challenge, inhibiting root elongation and impacting crop yields. Roots use ethylene to sense soil compaction as the restricted air space causes this gaseous signal to accumulate around root tips. Ethylene inhibits root elongation and promotes radial expansion in compacted soil, but its mechanistic basis remains unclear. Here, we report that ethylene promotes abscisic acid (ABA) biosynthesis and cortical cell radial expansion. Rice mutants of ABA biosynthetic genes had attenuated cortical cell radial expansion in compacted soil, leading to better penetration. Soil compaction-induced ethylene also up-regulates the auxin biosynthesis gene OsYUC8. Mutants lacking OsYUC8 are better able to penetrate compacted soil. The auxin influx transporter OsAUX1 is also required to mobilize auxin from the root tip to the elongation zone during a root compaction response. Moreover, osaux1 mutants penetrate compacted soil better than the wild-type roots and do not exhibit cortical cell radial expansion. We conclude that ethylene uses auxin and ABA as downstream signals to modify rice root cell elongation and radial expansion, causing root tips to swell and reducing their ability to penetrate compacted soil.

How plant roots respond to waterlogging.

Plant submergence is a major abiotic stress that impairs plant performance. Under water, 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 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.

Ethylene augments root hypoxia tolerance via growth cessation and reactive oxygen species amelioration.

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 pretreatment 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 pretreatments reduced this damage. Ethylene pretreatment 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.

Cation transporters in cell fate determination and plant adaptive responses to a low-oxygen environment.

Soil flooding creates low-oxygen environments in root zones and thus severely affects plant growth and productivity. Plants adapt to low-oxygen environments by a suite of orchestrated metabolic and anatomical alterations. Of these, formation of aerenchyma and development of adventitious roots are considered very critical to enable plant performance in waterlogged soils. Both traits have been firmly associated with stress-induced increases in ethylene levels in root tissues that operate upstream of signalling pathways. Recently, we used a bioinformatic approach to demonstrate that several Ca2+ and K+ -permeable channels from KCO, AKT, and TPC families could also operate in low oxygen sensing in Arabidopsis. Here we argue that low-oxygen-induced changes to cellular ion homeostasis and operation of membrane transporters may be critical for cell fate determination and formation of the lysigenous aerenchyma in plant roots and shaping the root architecture and adventitious root development in grasses. We summarize the existing evidence for a causal link between tissue-specific changes in oxygen concentration, intracellular Ca2+ and K+ homeostasis, and reactive oxygen species levels, and their role in conferring those two major traits enabling plant adaptation to a low-oxygen environment. We conclude that, for efficient operation, plants may rely on several complementary signalling pathway mechanisms that operate in concert and 'fine-tune' each other. A better understanding of this interaction may create additional and previously unexplored opportunities to crop breeders to improve cereal crop yield losses to soil flooding.

The role of ethylene in metabolic acclimations to low oxygen.

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.

Signal Dynamics and Interactions during Flooding Stress.

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.

Transcriptomes of Eight Arabidopsis thaliana Accessions Reveal Core Conserved, Genotype- and Organ-Specific Responses to Flooding Stress.

Climate change has increased the frequency and severity of flooding events, with significant negative impact on agricultural productivity. These events often submerge plant aerial organs and roots, limiting growth and survival due to a severe reduction in light reactions and gas exchange necessary for photosynthesis and respiration, respectively. To distinguish molecular responses to the compound stress imposed by submergence, we investigated transcriptomic adjustments to darkness in air and under submerged conditions using eight Arabidopsis (Arabidopsis thaliana) accessions differing significantly in sensitivity to submergence. Evaluation of root and rosette transcriptomes revealed an early transcriptional and posttranscriptional response signature that was conserved primarily across genotypes, although flooding susceptibility-associated and genotype-specific responses also were uncovered. Posttranscriptional regulation encompassed darkness- and submergence-induced alternative splicing of transcripts from pathways involved in the alternative mobilization of energy reserves. The organ-specific transcriptome adjustments reflected the distinct physiological status of roots and shoots. Root-specific transcriptome changes included marked up-regulation of chloroplast-encoded photosynthesis and redox-related genes, whereas those of the rosette were related to the regulation of development and growth processes. We identified a novel set of tolerance genes, recognized mainly by quantitative differences. These included a transcriptome signature of more pronounced gluconeogenesis in tolerant accessions, a response that included stress-induced alternative splicing. This study provides organ-specific molecular resolution of genetic variation in submergence responses involving interactions between darkness and low-oxygen constraints of flooding stress and demonstrates that early transcriptome plasticity, including alternative splicing, is associated with the ability to cope with a compound environmental stress.

Plant roots sense soil compaction through restricted ethylene diffusion.

Soil compaction represents a major challenge for modern agriculture. Compaction is intuitively thought to reduce root growth by limiting the ability of roots to penetrate harder soils. We report that root growth in compacted soil is instead actively suppressed by the volatile hormone ethylene. We found that mutant Arabidopsis and rice roots that were insensitive to ethylene penetrated compacted soil more effectively than did wild-type roots. Our results indicate that soil compaction lowers gas diffusion through a reduction in air-filled pores, thereby causing ethylene to accumulate in root tissues and trigger hormone responses that restrict growth. We propose that ethylene acts as an early warning signal for roots to avoid compacted soils, which would be relevant to research into the breeding of crops resilient to soil compaction.

Ethylene Differentially Modulates Hypoxia Responses and Tolerance across Solanum Species.

The increasing occurrence of floods hinders agricultural crop production and threatens global food security. The majority of vegetable crops are highly sensitive to flooding and it is unclear how these plants use flooding signals to acclimate to impending oxygen deprivation (hypoxia). Previous research has shown that the early flooding signal ethylene augments hypoxia responses and improves survival in Arabidopsis. To unravel how cultivated and wild Solanum species integrate ethylene signaling to control subsequent hypoxia acclimation, we studied the transcript levels of a selection of marker genes, whose upregulation is indicative of ethylene-mediated hypoxia acclimation in Arabidopsis. Our results suggest that ethylene-mediated hypoxia acclimation is conserved in both shoots and roots of the wild Solanum species bittersweet (Solanum dulcamara) and a waterlogging-tolerant potato (Solanum tuberosum) cultivar. However, ethylene did not enhance the transcriptional hypoxia response in roots of a waterlogging-sensitive potato cultivar, suggesting that waterlogging tolerance in potato could depend on ethylene-controlled hypoxia responses in the roots. Finally, we show that ethylene rarely enhances hypoxia-adaptive genes and does not improve hypoxia survival in tomato (Solanum lycopersicum). We conclude that analyzing genes indicative of ethylene-mediated hypoxia acclimation is a promising approach to identifying key signaling cascades that confer flooding tolerance in crops.

Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress.

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.

Oxygen-dependent proteolysis regulates the stability of angiosperm polycomb repressive complex 2 subunit VERNALIZATION 2.

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.