Regulation of Respiration and Fermentation to Control the Plant Internal Oxygen Concentration

Abstract

Plant internal oxygen concentrations can drop well below ambient even when the plant grows under optimal conditions. Using pea (Pisum sativum) roots, we show how amenable respiration adapts to hypoxia to save oxygen when the oxygen availability decreases. The data cannot simply be explained by oxygen being limiting as substrate but indicate the existence of a regulatory mechanism, because the oxygen concentration at which the adaptive response is initiated is independent of the actual respiratory rate. Two phases can be discerned during the adaptive reaction: an initial linear decline of respiration is followed by a nonlinear inhibition in which the respiratory rate decreased progressively faster upon decreasing oxygen availability. In contrast to the cytochrome c pathway, the inhibition of the alternative oxidase pathway shows only the linear component of the adaptive response. Feeding pyruvate to the roots led to an increase of the oxygen consumption rate, which ultimately led to anoxia. The importance of balancing the in vivo pyruvate availability in the tissue was further investigated. Using various alcohol dehydrogenase knockout lines of Arabidopsis (Arabidopsis thaliana), it was shown that even under aerobic conditions, alcohol fermentation plays an important role in the control of the level of pyruvate in the tissue. Interestingly, alcohol fermentation appeared to be primarily induced by a drop in the energy status of the tissue rather than by a low oxygen concentration, indicating that sensing the energy status is an important component of optimizing plant metabolism to changes in the oxygen availability.

Oxygen Sensing via the Ethylene Response Transcription Factor RAP2.12 Affects Plant Metabolism and Performance under Both Normoxia and Hypoxia

“…These alterations in respiratory metabolism resemble the metabolic changes that have been found to occur in response to a decrease in oxygen concentrations in previous work (Geigenberger et al, 2000;van Dongen et al, 2009;Narsai et al, 2011;António et al, 2016). As shown in previous studies, a decrease in internal oxygen concentration in roots, tubers, and other plant tissues leads to an adaptive inhibition of respiration as a proactive response to decrease oxygen consumption and prevent the tissue to drive into anoxia (Geigenberger et al, 2000;Zabalza et al, 2009;Geigenberger, 2014). Because inhibition of respiration occurs at oxygen concentrations well above the K m (oxygen) of cytochrome oxidase, an oxygen-sensing mechanism has been suggested to be involved (Geigenberger et al, 2000;Zabalza et al, 2009;Gupta et al, 2009).…”

“…As shown in previous studies, a decrease in internal oxygen concentration in roots, tubers, and other plant tissues leads to an adaptive inhibition of respiration as a proactive response to decrease oxygen consumption and prevent the tissue to drive into anoxia (Geigenberger et al, 2000;Zabalza et al, 2009;Geigenberger, 2014). Because inhibition of respiration occurs at oxygen concentrations well above the K m (oxygen) of cytochrome oxidase, an oxygen-sensing mechanism has been suggested to be involved (Geigenberger et al, 2000;Zabalza et al, 2009;Gupta et al, 2009). While the nature of this oxygen-sensing mechanism is unclear, decreased respiration rates and associated changes in the levels of TCA cycle intermediates in response to 35S::D13RAP2.12 overexpression implies a possible link between RAP2.12-mediated oxygen sensing and the regulation of respiration, although it cannot be excluded that this is due to indirect effects.…”

Waterlogging-induced changes in fermentative metabolism in roots and nodules of soybean genotypes

“…Enzymes of two important pathways are induced under anaerobic conditions: lactic fermentation is a one-step reaction from pyruvate to lactate, catalyzed by lactate dehydrogenase (LDH) with the regeneration of NAD + . Ethanolic fermentation is a two-step process regenerating NAD + in which pyruvate is first decarboxylated to acetaldehyde by pyruvate decarboxylase (PDC), and acetaldehyde is subsequently converted to ethanol by alcohol dehydrogenase (ADH) (Tadege et al, 1999;Zabalza et al, 2009).Although many studies have been carried out to clarify the effects of oxygen deficiency in plants, few studies are related to nodulated plants, especially soybean. This study aimed to characterize anaerobic metabolism through alterations of lactic and alcoholic fermentation enzymes, anaerobic metabolites and carbohydrate allocation in roots and nodules of two genotypes of soybean under hypoxia and post-hypoxic conditions.…”

A Mutant in theADH1Gene ofChlamydomonas reinhardtiiElicits Metabolic Restructuring during Anaerobiosis

“…1). The pfl1 mutant cells also accumulate elevated intracellular levels of amino acids, which may help recycle NADH and limit the potentially damaging consequences of pyruvate accumulation Zabalza et al, 2009). Aspects of electron rerouting observed in the Chlamydomonas pfl1 strain are similar to those observed for analogous E. coli mutants (Clark, 1989;Zhu and Shimizu, 2005), suggesting that the pathways and potentially some of the compensatory mechanisms are conserved between bacteria and eukaryotic green algae.…”