Metabolic strategies in hypoxic plants

Abstract

Complex multicellular organisms have evolved in an oxygen-enriched atmosphere. Oxygen is therefore essential for all aerobic organisms, including plants, for energy production through cellular respiration. However, plants can experience hypoxia following extreme flooding events and also under aerated conditions in proliferative organs or tissues characterized by high oxygen consumption. When oxygen availability is compromised, plants adopt different strategies to cope with hypoxia and limited aeration. A common feature among different plant species is the activation of an anaerobic fermentative metabolism to provide ATP to maintain cellular homeostasis under hypoxia. Fermentation also requires many sugar substrates, which is not always feasible, and alternative metabolic strategies are thus needed. Recent findings have also shown that the hypoxic metabolism is also active in specific organs or tissues of the plant under aerated conditions. Here, we describe the regulatory mechanisms that control the metabolic strategies of plants and how they enable them to thrive despite challenging conditions. A comprehensive mechanistic understanding of the genetic and physiological components underlying hypoxic metabolism should help to provide opportunities to improve plant resilience under the current climate change scenario.

Figure 1.

Toward an energy-efficient plant cell during hypoxia. Energy costs are strongly decreased by the inhibition of translational and a drop in H⁺-ATPase activity. Low H⁺-ATPase results in a reduction in the membrane potential which normally leads to potassium losses out of the cell through outward rectifying channels. The resulting loss of K⁺ triggers programmed cell death. Therefore, for H⁺-ATPase to operate within minimal ATP consumption, the increased GABA levels under hypoxia de-sensitize K⁺ efflux upon a drop of inner membrane potential. PPi from residual biosynthetic activity can also be leveraged in sucrose breakdown and glycolysis to maximize ATP output. Aerobic respiration in the mitochondria generates most of the energy (ATP) needed for cellular metabolism. ERFVII transcription factor genes are continuously expressed; however, their stability is undermined by the activity of PCOs. These enzymes, in an oxygen-dependent process, oxidize the N-terminal cysteine residue, directing the ERFVII proteins to the proteasome. Under normoxic conditions, oxygen activates PCOs, which are enzymes that oxidize the N-terminal cysteine residue in proteins that have a Cys residue following the removal of the N-terminal methionine. When hypoxia causes inefficient carbohydrate metabolism and reduces ATP production, the lower ATP content reduces TOR activity. This decrease in TOR activity weakens the induction efficiency of HRGs by ERF-VIIs. Created in BioRender. Triozzi et al. (2024)BioRender.com/w48h170.

Figure 2.

Molecular regulatory and metabolic pathways in rice during hypoxic germination. Low oxygen stress under submerged conditions leads to sugar starvation, which acts as a crucial upstream signal affecting metabolic regulation. Ca²⁺ functions as a secondary messenger to mediate downstream responses. CBL proteins bind to Ca²⁺ and interact with CIPK15, activating its kinase activity. This activated CIPK15 then interacts with SnRK1A, an upstream kinase of the transcription factor MYBS1, enhancing its activity and subsequently increasing αAmy activity for starch degradation in seeds. Seed imbibition triggers GA biosynthesis in the embryo. GA induces the αAmy gene. Concurrently, low oxygen-induced OsTPP7 relieves the inhibition of SnRK1A activity by T6P. OsTPP7 enhances the embryo axis–coleoptile's sink strength by converting T6P to trehalose. This lowers the T6P/sucrose ratio and promotes starch mobilization for energy production to facilitate coleoptile elongation. Low oxygen conditions shift aerobic respiration to anaerobic fermentation, inducing the expression of essential components, such as PDC and ADH. Created in BioRender. Triozzi et al. (2024)BioRender.com/g66n236.

Figure 3.

Long-term flood adaptations without a sugar supply. A) The sequential senescence phenotype of Arabidopsis completely submerged in the dark over the course of a week. The activation of the developmental program leads to death and controlled breakdown of organelles. B) Proposed metabolic route during flooding in dying leaves based on transcriptome and metabolome profiles. These findings are in line with a low abundance of sugars, which forces the cell to rely on alternative substrates. Created in BioRender. Triozzi et al. (2024)BioRender.com/z94e135.

Figure 4.

Cyclic activation of hypoxic metabolism in developing leaves. Young emerging leaves experience oxygen fluctuations under day/night cycles, which is referred to as cyclic hypoxia. This mechanism relies on ERFVII stability and activity. During the day, ERFVIIs undergo proteasomal degradation in young leaves through the N-degron pathway. However, an internal decreased in oxygen concentration occurs in young leaves at night because of the high respiration rate. Consequently, ERFVIIs are stabilized, translocate to the nucleus, and trigger the transcription of HRGs. This ERFVII-dependent cyclic mechanism creates a metabolic switch, which slows down the respiration rate in favor of the hypoxic metabolism at night. Cyclic hypoxia responses are also modulated by the activity of the energy sensor TOR complex, which depends on carbon and energy availability. Created in BioRender. Triozzi et al. (2024)BioRender.com/a44t283.