Abstract
Ethanol fermentation is considered as one of the main metabolic adaptations to ensure energy production in higher plants under anaerobic conditions. Following this pathway, pyruvate is decarboxylated and reduced to ethanol with the concomitant oxidation of NADH to NAD+. Despite its acknowledgement as an essential metabolic strategy, the conservation of this pathway and its regulation throughout plant evolution have not been assessed so far. To address this question, we compared ethanol fermentation in species representing subsequent steps in plant evolution and related it to the structural features and transcriptional regulation of the two enzymes involved: pyruvate decarboxylase (PDC) and alcohol dehydrogenase (ADH). We observed that, despite the conserved ability to produce ethanol upon hypoxia in distant phyla, transcriptional regulation of the enzymes involved is not conserved in ancient plant lineages, whose ADH homologues do not share structural features distinctive for acetaldehyde/ethanol-processing enzymes. Moreover, Arabidopsis mutants devoid of ADH expression exhibited enhanced PDC activity and retained substantial ethanol production under hypoxic conditions. Therefore, we concluded that, whereas ethanol production is a highly conserved adaptation to low oxygen, its catalysis and regulation in land plants probably involve components that will be identified in the future.
Highlights
Being aerobic organisms, plants rely on oxygen as the final electron acceptor in the mitochondrial electron transport chain dedicated to energy production
Lactic acid rapidly dissociates, contributing to the cytoplasmic acidification, which is initiated by the inactivation of vacuolar H+ ATPases (Gibbs and Greenway, 2003).The drop in cytoplasmic pH, in turn, inhibits lactate dehydrogenase (LDH) activity and stimulates that of pyruvate decarboxylase (PDC; 4.1.1.1), the first enzyme involved in ethanol fermentation (O’Carra and Mulcahy, 1997)
Arabidopsis thaliana Col-0 (Columbia-0) ecotype was used as the wild type in all experiments.The T-DNA insertion mutants adh1 (N552699) and adh2 (N430191) were obtained from the Nottingham Arabidopsis Stock Centre (NASC), and the pdc1pdc2 double mutant was obtained by crossing N660027 and N862662
Summary
Plants rely on oxygen as the final electron acceptor in the mitochondrial electron transport chain dedicated to energy production. Falls below the affinity of terminal oxidases, the electron movement is interrupted with an accumulation of TCA intermediates such as succinate and a drop in ATP production (António et al, 2016) In such conditions, minimal energy production is maintained by coupling glycolysis with ancillary reactions that prevent the organism from arresting glycolysis due to NAD+ shortage. Common to several kingdoms of life is the anaerobic activation of fermentative pathways.These reactions constitute an efficient solution to restore the pool of oxidized NAD+ while, at the same time, avoiding pyruvate and succinate accumulation These metabolites have been proposed to stimulate respiratory rates and, thereby, rapidly deplete the already scarce oxygen pool to nearly anoxic conditions (Zabalza et al, 2009). In Arabidopsis, four PDC-coding genes have been identified, two of which are hypoxia inducible (Mithran et al, 2014)
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