Evaluation of Metabolite Alteration under Flooding Stress in Soybeans

Nakamura, Takuji; Yamamoto, Ryō; Hiraga, Susumu; Nakayama, Naofumi; Okazaki, Keiichi; Takahashi, Hideyuki; Uchimiya, Hirofumi; Komatsu, Setsuko

doi:10.6090/jarq.46.237

Cited by 26 publications

(37 citation statements)

References 62 publications

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“…It is well established that Ala and GABA accumulate in different plant organs as a consequence of oxygen deficiency of different grades imposed by either waterlogging or submergence (Branco-Price et al, 2008;Mustroph et al, 2009Mustroph et al, , 2010Narsai et al, 2009Narsai et al, , 2011van Dongen et al, 2009;Rocha et al, 2010a;Nakamura et al, 2012;Barding et al, 2013). In line with these reports, we observed an accumulation of Ala and GABA in roots of wild-type Arabidopsis under long-term hypoxia.…”

Section: Loss Of Function Of Gox3 Induces Metabolic Rearrangements Insupporting

confidence: 80%

GLYCOLATE OXIDASE3, a Glycolate Oxidase Homolog of Yeast l-Lactate Cytochrome c Oxidoreductase, Supports l-Lactate Oxidation in Roots of Arabidopsis

et al. 2015

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In roots of Arabidopsis (Arabidopsis thaliana), L-lactate is generated by the reduction of pyruvate via L-lactate dehydrogenase, but this enzyme does not efficiently catalyze the reverse reaction. Here, we identify the Arabidopsis glycolate oxidase (GOX) paralogs GOX1, GOX2, and GOX3 as putative L-lactate-metabolizing enzymes based on their homology to CYB2, the L-lactate cytochrome c oxidoreductase from the yeast Saccharomyces cerevisiae. We found that GOX3 uses L-lactate with a similar efficiency to glycolate; in contrast, the photorespiratory isoforms GOX1 and GOX2, which share similar enzymatic properties, use glycolate with much higher efficiencies than L-lactate. The key factor making GOX3 more efficient with L-lactate than GOX1 and GOX2 is a 5-to 10-fold lower K m for the substrate. Consequently, only GOX3 can efficiently metabolize L-lactate at low intracellular concentrations. Isotope tracer experiments as well as substrate toxicity tests using GOX3 loss-offunction and overexpressor plants indicate that L-lactate is metabolized in vivo by GOX3. Moreover, GOX3 rescues the lethal growth phenotype of a yeast strain lacking CYB2, which cannot grow on L-lactate as a sole carbon source. GOX3 is predominantly present in roots and mature to aging leaves but is largely absent from young photosynthetic leaves, indicating that it plays a role predominantly in heterotrophic rather than autotrophic tissues, at least under standard growth conditions. In roots of plants grown under normoxic conditions, loss of function of GOX3 induces metabolic rearrangements that mirror wild-type responses under hypoxia. Thus, we identified GOX3 as the enzyme that metabolizes L-lactate to pyruvate in vivo and hypothesize that it may ensure the sustainment of low levels of L-lactate after its formation under normoxia.

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Section: Loss Of Function Of Gox3 Induces Metabolic Rearrangements Insupporting

confidence: 80%

GLYCOLATE OXIDASE3, a Glycolate Oxidase Homolog of Yeast l-Lactate Cytochrome c Oxidoreductase, Supports l-Lactate Oxidation in Roots of Arabidopsis

et al. 2015

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“…Irrespective of morphotypes, three sugar metabolic pathways were enhanced in the root system of L. grandiflora grown in the terrestrial condition (starch and sugar metabolism, galactose metabolism, and amino sugar and nucleotide sugar metabolic pathways). In organs of wetland plant species, reserves of carbohydrates and ethanol fermentation are equally important in maintaining glycolysis and energetic metabolism in general (reviewed in Nakamura et al., ). In our study, the significant decrease in glucose‐6‐phosphate and fructose‐6‐phosphate levels measured in both morphotypes, and the concomitant increase in fructose and mannose concentrations pinpointed the enhanced glycolytic activities and energetic needs of plants developing in terrestrial condition.…”

Section: Discussionmentioning

confidence: 99%

Aquatic and terrestrial morphotypes of the aquatic invasive plant, Ludwigia grandiflora, show distinct morphological and metabolomic responses

Billet

Genitoni

Bozec

et al. 2018

Ecology and Evolution

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In the context of expansion of invasive species, survival of invasive plants is conditioned by their ability to adapt. In France, the water primrose Ludwigia grandiflora, an aquatic invasive species, invades yet wet meadows, leading to a depreciation of their fodder value. Understanding its potential adaption is necessary to its management, strong differences between both morphotypes were expected. So morphological and metabolic responses to terrestrial environment were analyzed for aquatic and terrestrial morphotypes. All morphological and biomass variables were greater in the terrestrial morphotype than the aquatic morphotype, independent of conditions. In terrestrial condition, both morphotypes showed a high production of sugars in root tissues, especially in the terrestrial morphotype and both morphotypes produced a low level of amino acids in shoot tissues. All results demonstrate that the terrestrial condition seems a stressful situation for both morphotypes, which activates glycolysis and fermentation pathways to improve their survival under hypoxic stress. But, only the terrestrial morphotype has been able to adjust its metabolism and maintain efficient growth. In the future, a differential transcriptomic analysis will be carried out to confirm this result.

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“…Some enzymatic changes also occur in the tricarboxylic acid (TCA) cycle leading to important changes favoring plant survival of anaerobic conditions (Fox and Kennedy, 1991; Fox et al, 1994; Fan et al, 2003; Howell et al, 2006; Nakamura et al, 2012). Fox and Kennedy (1991) reported that 2-oxoglutarate dehydrogenase activity decreased under anoxia and the conversion of 2-oxoglutarate to succinate was identified as the limiting step in the TCA cycle under these conditions.…”

Section: Adjustments Of Carbohydrate Metabolism Under Low Oxygenmentioning

confidence: 99%

Tolerance of anaerobic conditions caused by flooding during germination and early growth in rice (Oryza sativa L.)

Miró¹,

Ismail²

2013

Front. Plant Sci.

159

134

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Rice is semi-aquatic, adapted to a wide range of hydrologies, from aerobic soils in uplands to anaerobic and flooded fields in waterlogged lowlands, to even deeply submerged soils in flood-prone areas. Considerable diversity is present in native rice landraces selected by farmers over centuries. Our understanding of the adaptive features of these landraces to native ecosystems has improved considerably over the recent past. In some cases, major genes associated with tolerance have been cloned, such as SUB1A that confers tolerance of complete submergence and SNORKEL genes that control plant elongation to escape deepwater. Modern rice varieties are sensitive to flooding during germination and early growth, a problem commonly encountered in rainfed areas, but few landraces capable of germination under these conditions have recently been identified, enabling research into tolerance mechanisms. Major QTLs were also identified, and are being targeted for molecular breeding and for cloning. Nevertheless, limited progress has been made in identifying regulatory processes for traits that are unique to tolerant genotypes, including faster germination and coleoptile elongation, formation of roots and leaves under hypoxia, ability to catabolize starch into simple sugars for subsequent use in glycolysis and fermentative pathways to generate energy. Here we discuss the state of knowledge on the role of the PDC-ALDH-ACS bypass and the ALDH enzyme as the likely candidates effective in tolerant rice genotypes. Potential involvement of factors such as cytoplasmic pH regulation, phytohormones, reactive oxygen species scavenging and other metabolites is also discussed. Further characterization of contrasting genotypes would help in elucidating the genetic and biochemical regulatory and signaling mechanisms associated with tolerance. This could facilitate breeding rice varieties suitable for direct seeding systems and guide efforts for improving waterlogging tolerance in other crops.

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Evaluation of Metabolite Alteration under Flooding Stress in Soybeans

Cited by 26 publications

References 62 publications

GLYCOLATE OXIDASE3, a Glycolate Oxidase Homolog of Yeast l-Lactate Cytochrome c Oxidoreductase, Supports l-Lactate Oxidation in Roots of Arabidopsis

GLYCOLATE OXIDASE3, a Glycolate Oxidase Homolog of Yeast l-Lactate Cytochrome c Oxidoreductase, Supports l-Lactate Oxidation in Roots of Arabidopsis

Aquatic and terrestrial morphotypes of the aquatic invasive plant, Ludwigia grandiflora, show distinct morphological and metabolomic responses

Tolerance of anaerobic conditions caused by flooding during germination and early growth in rice (Oryza sativa L.)

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