Production and organ distribution of succinate in rice seedlings during anoxia

Menegus, Faustino; Cattaruzza, Liliana; Chersi, Alberto; Selva, Antonio; Fronza, Giovanni

doi:10.1111/j.1399-3054.1988.tb02001.x

Cited by 30 publications

(27 citation statements)

References 26 publications

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“…2) showing its role as a fermentation product in this alga. Others have recently reported succinate as a fermentative end-product in higher plants (25,26). The present study is, to our knowledge, the first report of such a finding in a green alga.…”

Section: 04supporting

confidence: 56%

“…In higher plants, anaerobiosis has been shown to lead to an accumulation of succinate (9,25,26), and Ala (9,20,25,26,30,36) and a decline in Asp (9,36 …”

Section: Introductionmentioning

confidence: 99%

“…In the green alga Selenastrum minutum, there is no PFP (5, 38), but a cytosolic FBPase does exist and is strongly inhibited by Fru-2,6-P2 (6, 38). The absence of PFP in this alga means that a role of Fru-2,6-P2 in regulating cytosolic FBPase during changes in glycolytic flux can be tested unambiguously.In higher plants, anaerobiosis has been shown to lead to an accumulation of succinate (9,25,26), and Ala (9,20,25,26,30,36) and a decline in Asp (9,36 …”

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confidence: 99%

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Anaerobic Metabolism in the N-Limited Green Alga Selenastrum minutum

Vanlerberghe

Feil²,

Turpin³

1990

Plant Physiol.

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The onset of anaerobiosis in darkened, N-limited cells of the green alga Selenastrum minutum (Naeg.) Collins elicited the following metabolic responses. There was a rapid decrease in energy charge from 0.85 to a stable lower value of 0.6 accompanied by rapid increases in pyruvate/phosphoenolpyruvate and fructose-1,6-bisphosphate/fructose-6-phosphate ratios indicating activation of pyruvate kinase and 6-phosphofructokinase, respectively. There was also a large increase in fructose-2,6-bisphosphate, which, since this alga lacks pyrophosphate dependent 6-phosphofructokinase, can be inferred to inhibit gluconeogenic fructose-1,6-bisphosphatase activity. flux during anoxia (the Pasteur effect) is accompanied by large increases in FBP/F6P and pyr/PEP ratios (37). A Pasteur effect also has been shown to occur in green algae (13, 28) but these observations have not been accompanied by a detailed analysis of changes in glycolytic intermediates. There has been speculation that PFK is also important in regulating anaerobic carbon metabolism in green algae (13).Fru-2,6-P2 is an important effector ofplant PFP and FBPase and therefore a key regulator of plant respiration (2). Studies have reported increases in Fru-2,6-P2 in response to anoxia in higher plants (22,27) yet it is unclear how Fru-2,6-P2 contributes to increased glycolytic flux under these conditions. One possibility is that by inhibiting the cytosolic FBPase it stops gluconeogenic carbon flow. A second possibility is that by stimulating PFP, the forward (glycolytic) reaction may provide FBP for glycolysis or conversely, the reverse (gluconeogenic) reaction may provide PPi for use in sucrose mobilization (1, 2, 33, 34). In the green alga Selenastrum minutum, there is no PFP (5, 38), but a cytosolic FBPase does exist and is strongly inhibited by Fru-2,6-P2 (6, 38). The absence of PFP in this alga means that a role of Fru-2,6-P2 in regulating cytosolic FBPase during changes in glycolytic flux can be tested unambiguously.In higher plants, anaerobiosis has been shown to lead to an accumulation of succinate (9,25,26), and Ala (9,20,25,26,30,36) and a decline in Asp (9,36

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Section: 04supporting

confidence: 56%

“…In higher plants, anaerobiosis has been shown to lead to an accumulation of succinate (9,25,26), and Ala (9,20,25,26,30,36) and a decline in Asp (9,36 …”

Section: Introductionmentioning

confidence: 99%

mentioning

confidence: 99%

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Anaerobic Metabolism in the N-Limited Green Alga Selenastrum minutum

Vanlerberghe

Feil²,

Turpin³

1990

Plant Physiol.

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“…Although it has been argued that succinate accumulation plays a role in resistance to hypoxia (Menegus et al, 1988(Menegus et al, , 1989, Roberts et al (1992) found that succinate does not accumulate in corn root tips. We found a similar pattern, with succinate showing a short-term increase in levels followed by a long-term decline.…”

Section: Fermentation Productsmentioning

confidence: 99%

Long-Term Anaerobic Metabolism in Root Tissue (Metabolic Products of Pyruvate Metabolism)

1993

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Vanlerberghe et al. (1990) have recently shown that the green alga Selenastrum minutum accumulates succinate under anaerobic conditions. They demonstrate that the OAA required for reduction to succinate is initially provided by transferring the amino group of aspartate to pymvate to provide a 2-fold increase in ATP yield per hexose as com- One of the difficulties with most of the studies on anaerobic metabolism in plants is that they are restricted to short time intervals, usually a maximum of 12 to 24 h Ranson, 1967% 1967b;Hoffman et al., 1986;Vanlerberghe et al., 1990;Roberts et al., 1992). However, since barley (Hordeum vulgare L.) and maize can usually survive 3 to 5 d of anaerobic stress (Harberd and Edwards, 1982;Lemke-Keyes and Sachs, 1989), it may be the long-term adaptations to anaerobic stress that are more important in determining sensitivity to flooding.In this study, we looked at the long-tem effects of anaeroshort-term effects. We show that although a number of metabolic products, lactate, Ala, malate, and succinate, accumulate during short-term anaerobiosis, they do not continue to increase during long-term anaerobiosis. We also examined the effect on the accumulation of metabolites of reducing both the leve1 of available nitrogen and the accumulation of ethanol by using an ADH-mutant. Finally, we 'Ooked at 'Ome Of the enzYmes involved in and wccinate production to determine whether anY Of these enzYmes are induced der anaerobic COnditions. 1988, 1989).Under hypoxic or anaerobic conditions, there are changes in the levels of glycolytic intermediates in roots and an increased glycolytic flux (the Pasteur effect) (Faiz-ur-Rahman occur so that the cell can meet its requirements for ATP despite the much lower efficiency of ATp production by fermentation. The increase in glycolytic flux &ring hypoxia is accompanied by the accumulation of a number of glycolytic end products including ethanoI, lactate, AIa, and various organic acids and amino acids (Effer and R~~~~~, 196713;Gfeller and Gibbs, 1984;Roberts et al., 1984;Hoffman et al., 1986;Roberts et al., 1992). A number of alternative pathways to lactate and ethanol fermentation have been discovered in animals with high resistance to anoxia. These animals accumulate combinations of a number of end products including Ala, octopine, alanopine, acetate, propionate, 2-methyl-b~-tyrate, and succinate (Fields, 1983). The advantages of these alternative strategies for anaerobic fermentation are based on an increased ATP production per mo1 of substrate fermented, the production of NAD+ to provide a net sink for reductant, and the maintenance of the cellular pH. Davies, 1980

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“…Other studies have dealt with the accumulation of N containing compounds under anoxia. It has been observed that there are large fluxes of 14C to Ala from '4C-sugars in anoxic plant tissue (7,17,18) and that Ala accumulates in anoxic plant tissue (8,12,13,17,20,25). It anoxia (6).…”

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confidence: 99%

Anaerobic Metabolism in the N-Limited Green Alga Selenastrum minutum

Vanlerberghe

Turpin²

1990

Plant Physiol.

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The green alga Selenastrum minutum (Naeg.) Collins is able to assimilate NH4+ in the dark under anaerobic conditions (GC Vanlerberghe, AK Horsey, HG Weger, DH Turpin [1989] Plant Physiol 91: 1551-1557. In the present study, analysis of metabolites following addition of NH4+ to cells acclimated to anaerobic conditions has shown the following. There was a transient decline in adenylate energy charge from 0.6 to 0.4 followed by a recovery back to -0.6. This was accompanied by a rapid increase in pyruvate/phosphoenolpyruvate and fructose-1,6-bisphosphate/ fructose-6-phosphate ratios indicating activation of pyruvate kinase and 6-phosphofructokinase, respectively. There was also an increase in fructose-2,6-bisphosphate, which, since this alga lacks pyrophosphate dependent 6-phosphofructokinase can be inferred to inhibit gluconeogenic fructose-1,6-bisphosphatase.These changes resulted in an increase in the rate of anaerobic starch breakdown. Anaerobic NH4+ assimilation also resulted in a two-fold increase in the rate of production of the major fermentative end-products in this alga, D-lactate and ethanol. There was no change in the rate of accumulation of the fermentative endproduct succinate but malate accumulated under anoxia during NH4+ assimilation. A rapid increase in Gin and decline in Glu indicates that primary NH4+ assimilation under anoxia was via glutamine synthetase-glutamate synthase. Almost all N assimilated under these conditions was sequestered in alanine. These results allow us to propose a model for the regulation of carbon metabolism during anaerobic NH4+ assimilation.

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Production and organ distribution of succinate in rice seedlings during anoxia

Cited by 30 publications

References 26 publications

Anaerobic Metabolism in the N-Limited Green Alga Selenastrum minutum

Anaerobic Metabolism in the N-Limited Green Alga Selenastrum minutum

Long-Term Anaerobic Metabolism in Root Tissue (Metabolic Products of Pyruvate Metabolism)

Anaerobic Metabolism in the N-Limited Green Alga Selenastrum minutum

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