Reconfiguration of N Metabolism upon Hypoxia Stress and Recovery: Roles of Alanine Aminotransferase (AlaAT) and Glutamate Dehydrogenase (GDH)

Abstract

In the context of climatic change, more heavy precipitation and more frequent flooding and waterlogging events threaten the productivity of arable farmland. Furthermore, crops were not selected to cope with flooding- and waterlogging-induced oxygen limitation. In general, low oxygen stress, unlike other abiotic stresses (e.g., cold, high temperature, drought and saline stress), received little interest from the scientific community and less financial support from stakeholders. Accordingly, breeding programs should be developed and agronomical practices should be adapted in order to save plants' growth and yield-even under conditions of low oxygen availability (e.g., submergence and waterlogging). The prerequisite to the success of such breeding programs and changes in agronomical practices is a good knowledge of how plants adapt to low oxygen stress at the cellular and the whole plant level. In the present paper, we summarized the recent knowledge on metabolic adjustment in general under low oxygen stress and highlighted thereafter the major changes pertaining to the reconfiguration of amino acids syntheses. We propose a model showing (i) how pyruvate derived from active glycolysis upon hypoxia is competitively used by the alanine aminotransferase/glutamate synthase cycle, leading to alanine accumulation and NAD⁺ regeneration. Carbon is then saved in a nitrogen store instead of being lost through ethanol fermentative pathway. (ii) During the post-hypoxia recovery period, the alanine aminotransferase/glutamate dehydrogenase cycle mobilizes this carbon from alanine store. Pyruvate produced by the reverse reaction of alanine aminotransferase is funneled to the TCA cycle, while deaminating glutamate dehydrogenase regenerates, reducing equivalent (NADH) and 2-oxoglutarate to maintain the cycle function.

Keywords: alanine; alanine aminotransferase (AlaAT); glutamate; glutamate dehydrogenase (GDH); glycolysis; hypoxia; nitrogen.

Figure 1

Schematic representation of the central role of alanine during hypoxia and post-hypoxia recovery periods. HYPOXIA: Visualization of carbon flux from carbon storage compounds to alanine through AlaAT/NADH-GOGAT cycle. (POST-HYPOXIA) Visualization of alanine mobilization through AlaAT/GDH cycle and carbon flux towards TCA cycle. Scheme drawn by integrating data from transcriptomic and metabolomic studies and studies combining ¹⁵N and ¹³C labeling in various species such as Medicago truncatula, Lotus japonicus, Glycine max and Arabidopsis thaliana. AlaAT: Alanine aminotransferase; GDH: Glutamate Dehydrogenase GOGAT: Glutamne Oxoglutarate Aminotransferase.