Plant Life with and without Oxygen: A Metabolomics Approach

Abstract

Oxygen deficiency is an environmental challenge which affects plant growth, the development and distribution in land and aquatic ecosystems, as well as crop yield losses worldwide. The capacity to exist in the conditions of deficiency or the complete lack of oxygen depends on a number of anatomic, developmental and molecular adaptations. The lack of molecular oxygen leads to an inhibition of aerobic respiration, which causes energy starvation and the acceleration of glycolysis passing into fermentations. We focus on systemic metabolic alterations revealed with the different approaches of metabolomics. Oxygen deprivation stimulates the accumulation of glucose, pyruvate and lactate, indicating the acceleration of the sugar metabolism, glycolysis and lactic fermentation, respectively. Among the Krebs-cycle metabolites, only the succinate level increases. Amino acids related to glycolysis, including the phosphoglycerate family (Ser and Gly), shikimate family (Phe, Tyr and Trp) and pyruvate family (Ala, Leu and Val), are greatly elevated. Members of the Asp family (Asn, Lys, Met, Thr and Ile), as well as the Glu family (Glu, Pro, Arg and GABA), accumulate as well. These metabolites are important members of the metabolic signature of oxygen deficiency in plants, linking glycolysis with an altered Krebs cycle and allowing alternative pathways of NAD(P)H reoxidation to avoid the excessive accumulation of toxic fermentation products (lactate, acetaldehyde, ethanol). Reoxygenation induces the downregulation of the levels of major anaerobically induced metabolites, including lactate, succinate and amino acids, especially members of the pyruvate family (Ala, Leu and Val), Tyr and Glu family (GABA and Glu) and Asp family (Asn, Met, Thr and Ile). The metabolic profiles during native and environmental hypoxia are rather similar, consisting in the accumulation of fermentation products, succinate, fumarate and amino acids, particularly Ala, Gly and GABA. The most intriguing fact is that metabolic alterations during oxidative stress are very much similar, with plant response to oxygen deprivation but not to reoxygenation.

Keywords: adaptation; anoxia; desubmergence; flooding; hypoxia; metabolomics; reoxygenation; submergence; tolerance; waterlogging.

Figure 1

Impact of oxygen deficiency/reoxygenation stress of different origins on plants. Based on [1,2,5,6,7,8,9,10,11,12,13,14].

Figure 2

Oxygen deficiency/reoxygenation stress-specific alteration of the central metabolism in plants. Schematic representation of the major metabolic pathways of the central metabolism: glycolysis and fermentations, the Krebs cycle, the GABA shunt and the metabolism of amino acids. The scheme is based on the results of multiple studies summarized in Table S1. The frequencies of the directions in the metabolite abundance alteration after the treatments were calculated and are shown in Table S2, allowing one to choose the significantly changed metabolites (p < 0.1). Metabolites are indicated in different boxes corresponding to the metabolite class. Red color denotes increased abundance, yellow denotes being unchanged and blue is the decreased one. Color filling in the left part of the box designates changes due to oxygen deprivation, and in the right part, due to reoxygenation. The absence of filling reflects that the individual metabolites may display different patterns in various studies, or were not detected/measured.

Figure 3

The possible importance of primary metabolism alterations in plant adaptation to oxygen deficiency.