Conservation of ethanol fermentation and its regulation in land plants

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.

Arabidopsis phenotyping reveals the importance of alcohol dehydrogenase and pyruvate decarboxylase for aerobic plant growth

“…Although ADH is the crucial enzyme for NADH oxidation, mutations in ADH can also lead to the accumulation of acetaldehyde, which is much more toxic than ethanol 38 . The pdc1pdc2 is instead blocked at the level of pyruvate, and therefore, while the two mutants are both equally impaired in their ability to produce ethanol 39 , they differ in terms of the metabolic step blocked and the possible detrimental effects of acetaldehyde accumulating in the adh1 mutant could be revealed by differences in the phenotypes of the two mutants.…”

Ethylene Differentially Modulates Hypoxia Responses and Tolerance across Solanum Species

“…It is currently unclear which hypoxia-responsive genes actually contribute to enhanced hypoxia tolerance. For instance, several studies suggest transcriptional SUS1 or ADH1 induction may not be required for anaerobic fermentation, maintenance of glycolysis and subsequent hypoxia tolerance in potato tubers and Arabidopsis, respectively [40,52]. Previous research showed that protein levels of ADH1 in tomato roots increased only 1.7-fold after 24 h of waterlogging, whereas PDC1 levels were even down-regulated [53].…”

Detection and characterization of quantitative trait loci for coleoptile elongation under anaerobic conditions in rice

“…In this regard, a recent study in Arabidopsis revealed that ADH activity was up-regulated in a PDC-inactivated mutant (Bui et al, 2019). Given that the authors observed that gene expression levels in mutant and wild-type plants were essentially the same, they concluded that inactivation of PDC activity promotes the accumulation of ADH protein (Bui et al, 2019). We suspect that similar, as yet undetermined, mechanisms may suppress gene expression of ADH in rice during germination.…”

“…At present, however, we are unable to explain why SL2111 shows lower ADH1 expression, even though this line was characterized by a longer coleoptile under anaerobic conditions. In this regard, a recent study in Arabidopsis revealed that ADH activity was up-regulated in a PDC-inactivated mutant (Bui et al, 2019). Given that the authors observed that gene expression levels in mutant and wild-type plants were essentially the same, they concluded that inactivation of PDC activity promotes the accumulation of ADH protein (Bui et al, 2019).…”