The role of ethylene in metabolic acclimations to low oxygen

Abstract

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.

Keywords: ERFVII; anaerobic metabolism; autophagy; ethylene; hypoxia; oxygen sensing; reactive oxygen species (ROS); submergence.

Figure 1

The role of ethylene in known and proposed metabolic adjustments during flooding‐induced hypoxia. Key: green arrows, increase; red arrows, decrease; dashed lines, hypothesized and requires experimental confirmation. (a) In Arabidopsis, entrapped ethylene upon submergence enhances messenger RNA (mRNA) and protein levels of nitric oxide (NO)‐scavenger PHYTOGLOBIN1 (PGB1), limiting NO‐dependent class VII ethylene response factor (ERFVII) proteolysis and enhancing ERFVII accumulation in the nucleus. In addition, ERFVII transcription is under direct control of ethylene signalling in Arabidopsis and rice. (b) When oxygen (O₂) levels decline, oxidative phosphorylation is reduced and limits ATP production. This drop in in O₂ (and ATP) activates the ethylene‐enhanced ERFVII pool and initiates hypoxia‐adaptive gene expression and stimulates anaerobic metabolism through processes like ethanolic fermentation. (c) When carbohydrates are depleted, a feedback loop downregulates fermentation genes downstream of ERFVII action. Under prolonged hypoxia and carbohydrate starvation, autophagy can be induced to supply the cell with alternative energy‐rich substrates. Ethylene is suggested to mediate autophagy through the induction of ATG genes and altered reactive oxygen species (ROS) levels, but only under carbohydrates‐limited conditions. (d) Upon reoxygenation, high light and O₂ levels lead to excess ROS levels. Ethylene was shown to strongly reduce ROS levels and confer tolerance under a variety of abiotic stresses through direct production of ROS scavenging compounds, but a role for ethylene in ROS detoxification under flooding stress remains to be revealed. ADH, alcohol dehydrogenase; ALAAT, alanine aminotransferase; APX, ascorbate peroxidase; CAT, catalase; EIN3, Ethylene Insensitive 3; GPX, glutathione peroxidase; HRU1, Hypoxia Responsive Universal Stress Protein 1; PDC, pyruvate decarboxylase; POD, peroxidase; RBOHD, Respiratory Burst Oxidase Homologue Protein D; SRO5, SIMILAR TO RCD ONE5; SUS, sucrose synthase; TF, transcription factor; Ub, ubiquitin.