The Many Facets of Hypoxia in Plants

Abstract

Plants are aerobic organisms that require oxygen for their respiration. Hypoxia arises due to the insufficient availability of oxygen, and is sensed by plants, which adapt their growth and metabolism accordingly. Plant hypoxia can occur as a result of excessive rain and soil waterlogging, thus constraining plant growth. Increasing research on hypoxia has led to the discovery of the mechanisms that enable rice to be productive even when partly submerged. The identification of Ethylene Response Factors (ERFs) as the transcription factors that enable rice to survive submergence has paved the way to the discovery of oxygen sensing in plants. This, in turn has extended the study of hypoxia to plant development and plant-microbe interaction. In this review, we highlight the many facets of plant hypoxia, encompassing stress physiology, developmental biology and plant pathology.

Keywords: Arabidopsis; anaerobiosis; anoxia; development; flooding; hypoxia; rice; submergence; waterlogging.

Figure 1

How plants sense oxygen. Under aerobic conditions (left), aerobic respiration in the mitochondria provides most of the energy (ATP) required for the cell metabolism. The ERF-VII transcription factor genes are constitutively expressed, but their stability is compromised by the activity of PCOs, which, in a process requiring oxygen, oxidize the N-terminal Cys residue, channeling the ERF-VII proteins to the proteasome, in a process also requiring nitric oxide (NO). Under hypoxia (right), the respiration in the mitochondria is drastically reduced, and ATP production can only occur because of enhanced glycolytic activity. The ERF-VII proteins are stabilized because of the absence of oxygen and also thanks to ethylene production, which dampens the presence of NO in the cell. The stable ERF-VII proteins migrate to the nucleus where they activate the transcription of Hypoxia-Responsive Genes (HRGs), including genes encoding proteins required for alcoholic fermentation. This figure was created using BioRender [17].

Figure 2

Environmental hypoxia is generated by soil waterlogging or by plant submergence. An excess of water in the soil reduces aerobic respiration, which is replaced by anaerobic metabolism. The uptake of nutrients is reduced. A radial oxygen loss (ROL) barrier and aerenchyma eventually develops in the root system to provide oxygen to the submerged roots. The aerial part of the plant, although not submerged, is also affected by waterlogging, with reduced stomata conductance and CO₂ assimilation. Complete or partial plant submergence may trigger quiescence or escape strategies, characterized by reduced or enhanced elongation, respectively. Ethylene entrapment in the submerged plant plays an important role in defining the overall plant response to submergence. Aerenchyma develops and the metabolism is mostly anaerobic, with the exception of tissues and organs that receive sufficient oxygen through the aerenchyma. This figure was created using BioRender [17].

Figure 3

Hypoxic niches affecting developmental processes. In the roots, hypoxia in the lateral root primordia affects auxin-regulated genes through the action of ERF-VII proteins. In the anthers, hypoxia represents a developmental signal influencing meiotic fate acquisition (MSCA: male sterile converted anther 1). In the shoot apical meristem, a hypoxic niche controls the stability of ZPR2 and VRN2, affecting meristem identity and flowering, respectively. This figure was created using BioRender [17].

Figure 4

Local hypoxia establishment during plant–microbe interactions. Leaf infection by necrotrophic fungi results in enhanced respiration, which eventually leads to hypoxia. Under these conditions, ERF-VII proteins are stable and, through interaction with ORA59, they influence the efficacy of a plant’s response to the pathogen. Similarly, agrobacterium infection enhances respiration in the infected tissue, which leads to hypoxia. Stable ERF-VII activates the anaerobic response that favors tumor growth. In legumes, rhizobia requires hypoxic conditions, given that the activity of nitrogenase enzyme, which can fix N₂, is inactivated by oxygen. Nodules maintain an inner low-O₂ environment thanks to the presence of a nodule O₂ diffusion barrier and by expressing O₂-carrying symbiotic plant hemoglobins (leghemoglobin). This figure was created using BioRender [17].