Aspartate stimulation of malate decarboxylation in Zea mays bundle sheath cells: Possible role in regulation of C4 photosynthesis

Chapman, K.S.R.; Hatch, M.D.

doi:10.1016/0006-291x(79)90254-7

Cited by 22 publications

(32 citation statements)

References 8 publications

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“…ATP enhanced malate decarboxylation only in the dark, whereas Asp and 3-phosphoglycerate stimulated malate decarboxylation in the light. Since Asp facilitates the transport of malate into the chloroplasts (Chapman and Hatch, 1979;Boag and Jenkins, 1986) and 3-phosphoglycerate is important for the reoxidation of NADPH formed in the NADP-ME reaction (Hatch and Kagawa, 1976), the stimulation by Asp and 3-phosphoglycerate confirms that malate is mainly decarboxylated by NADP-ME and not by PEPCK.…”

Section: The Function Of Pepck In Maizementioning

confidence: 99%

“…Under illumination, however, the effect of ATP and NAD was smaller and malate decarboxylation was strongly stimulated by Asp and 3-phosphoglycerate. Stimulation by Asp and 3-phosphoglycerate is characteristic of malate decarboxylation catalyzed by NADP-ME (Hatch and Kagawa, 1976;Chapman and Hatch, 1979;Boag and Jenkins, 1986). The light dependence of malate decarboxylation also suggests the involvement of NADP-ME (Hatch and Kagawa, 1976).…”

Section: Decarboxylation Of [4-14 C]malatementioning

confidence: 99%

“…In maize, substantial amounts of Asp are labeled (Hatch, 1971;Créach et al, 1974;MorotGaudry and Farineau, 1978;Chapman and Hatch, 1981), more so in N-sufficient than in N-deficient maize (Khamis et al, 1992), but measurements of labeling and/or pools do not give any indication of relative fluxes. The relative capacities for Asp and malate decarboxylation would have major energetic consequences in the BS.…”

Section: Photosynthetic Metabolism In Maizementioning

confidence: 99%

“…4). Chapman and Hatch (1981) showed that the activity of Asp aminotransferase in BS cells of maize is located mainly in the mitochondria. In addition to oxaloacetate, the PEPCK reaction requires ATP.…”

Section: Photosynthetic Metabolism In Maizementioning

confidence: 99%

“…Using isolated BS strands, Chapman and Hatch (1981) showed that BS cells of maize have a significant capacity to decarboxylate Asp, and they assumed that NADP-ME was responsible. In view of the occurrence of PEPCK in maize, the involvement of PEPCK in the decarboxylation of Asp appears more likely, because PEPCK can directly catalyze the decarboxylation of oxaloacetate formed from Asp without previous reduction of oxaloacetate to malate.…”

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Phosphoenolpyruvate Carboxykinase Is Involved in the Decarboxylation of Aspartate in the Bundle Sheath of Maize1

et al. 1999

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We recently showed that maize (Zea mays L.) leaves contain appreciable amounts of phosphoenolpyruvate carboxykinase (PEPCK; R.P. Walker, R.M. Acheson, L.I. Técsi, R.C. Leegood [1997] Aust J Plant Physiol 24: 459-468). In the present study, we investigated the role of PEPCK in C 4 photosynthesis in maize. PEPCK activity and protein were enriched in extracts from bundle-sheath (BS) strands compared with whole-leaf extracts. Decarboxylation of [4-14 C]aspartate (Asp) by BS strands was dependent on the presence of 2-oxoglutarate and Mn 2؉ , was stimulated by ATP, was inhibited by the PEPCK-specific inhibitor 3-mercaptopicolinic acid, and was independent of illumination. The principal product of Asp metabolism was phosphoenolpyruvate, whereas pyruvate was a minor product. Decarboxylation of [4-14 C]malate was stimulated severalfold by Asp and 3-phosphoglycerate, was only slightly reduced in the absence of Mn 2؉ or in the presence of 3-mercaptopicolinic acid, and was light dependent. Our data show that decarboxylation of Asp and malate in BS cells of maize occurs via two different pathways: Whereas malate is mainly decarboxylated by NADPmalic enzyme, decarboxylation of Asp is dependent on the activity of PEPCK. C 4 plants have been classified as NADP-ME, NAD-ME, and PEPCK types, according to the major decarboxylase involved in the decarboxylation of C 4 acids in the BS cells Hatch et al., 1975). Maize (Zea mays) belongs to the NADP-ME subgroup of C 4 plants and possesses negligible activity of PEPCK, although suggested that some other NADP-ME species utilize PEPCK as an auxiliary decarboxylase. However, we showed previously that maize leaves contain large amounts of PEPCK (Walker et al., 1997), andFurumoto et al. (1999) identified a PEPCK gene from maize that is specifically expressed in BS cells. Other NADP-ME species such as Echinochloa colona, Echinochloa crus-galli, Digitaria sanguinalis, and Paspalum notatum also contain PEPCK, whereas PEPCK protein was not detectable in Sorghum bicolor, Saccharum officinarum, or Flaveria bidentis (Walker et al., 1997). The reason that the occurrence of PEPCK in these plants has been overlooked may be due to difficulties in measuring PEPCK activity (Walker et al., 1997) or to the lack of an antibody.PEPCK-type C 4 species mainly use Asp as the CO 2 donor and decarboxylate the oxaloacetate formed via the following reaction:In NADP-ME species such as maize, 14 CO 2 is initially incorporated into the C-4 position of malate and Asp (about 75% and 25%, respectively), and the C-4 of both is subsequently incorporated into other metabolites (Hatch, 1971; Morot-Gaudry and Farineau, 1978). Using isolated BS strands, Chapman and Hatch (1981) showed that BS cells of maize have a significant capacity to decarboxylate Asp, and they assumed that NADP-ME was responsible. In view of the occurrence of PEPCK in maize, the involvement of PEPCK in the decarboxylation of Asp appears more likely, because PEPCK can directly catalyze the decarboxylation of oxaloacetate formed from Asp without previous...

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Section: The Function Of Pepck In Maizementioning

confidence: 99%

Section: Decarboxylation Of [4-14 C]malatementioning

confidence: 99%

Section: Photosynthetic Metabolism In Maizementioning

confidence: 99%

Section: Photosynthetic Metabolism In Maizementioning

confidence: 99%

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confidence: 99%

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Phosphoenolpyruvate Carboxykinase Is Involved in the Decarboxylation of Aspartate in the Bundle Sheath of Maize1

et al. 1999

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Energy-Oriented Organelles and Activities: III The Chloroplast and Photosynthesis

Dillon

1981

Ultrastructure, Macromolecules, and Evolution

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The roles of malate and aspartate in C4 photosynthetic metabolism of Flaveria bidentis (L.)

Meister

Agostino

Hatch

1996

Planta

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Abstract. In C4 grasses belonging to the NADP-malic enzyme-type subgroup, malate is considered to be the predominant C4 acid metabolized during C4 photosynthesis, and the bundle sheath cell chloroplasts contain very little photosystem-II (PSII) activity. The present studies showed that Flaveria bidentis (L.), an NADP-malic enzyme-type C4 dicotyledon, had substantial PSII activity in bundle sheath cells and that malate and aspartate apparently contributed about equally to the transfer of CO2 to bundle sheath cells. Preparations of bundle sheath cells and chloroplasts isolated from these cells evolved O2 at rates between 1.5 and 2 gmol'min -1.mg 1 chlorophyll (Chl) in the light in response to adding either 3-phosphoglycerate plus HCO~-or aspartate plus 2-oxoglutarate. Rates of more than 2 ~tmol 02' min -1" mgChl were recorded for cells provided with both sets of these substrates. With bundle sheath cell preparations the maximum rates of light-dependent CO2 fixation and malate decarboxylation to pyruvate recorded were about 1.7 ~tmol -min-1. mg-1 Chl. Compared with NADPmalic enzyme-type grass species, F. bidends bundle sheath cells contained much higher activities of NADP-malate dehydrogenase and of aspartate and alanine aminotransferases. Time-course and pulse-chase studies following the kinetics of radiolabelling of the C-4 carboxyl of C4 acids from t4CO2 indicated that the photosynthetically active pool of malate was about twice the size of the aspartate pool. However, there was strong evidence for a rapid flux of carbon through both these pools. Possible routes of aspartate metabolism and the relationship between this metabolism and PSII activity in bundle sheath cells are considered.Abbreviations: DHAP = dihydroxyacetone phosphate; NADP-ME(-type) = NADP-malic enzyme (type); NADP-MDH = NADPmalate dehydrogenase; OAA = oxaloacetic acid; 2-OG = 2-oxoglutarate; PEP = phosphoenolpyruvate; PGA = 3-phosphoglycerate; Pi = orthophosphate; Ru5P = ribulose 5-phosphate Correspondence to: M.D. Hatch; FAX:61 (6)2465000; Tel.: 61 (6) 2465264

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Aspartate stimulation of malate decarboxylation in Zea mays bundle sheath cells: Possible role in regulation of C4 photosynthesis

Cited by 22 publications

References 8 publications

Phosphoenolpyruvate Carboxykinase Is Involved in the Decarboxylation of Aspartate in the Bundle Sheath of Maize1

Phosphoenolpyruvate Carboxykinase Is Involved in the Decarboxylation of Aspartate in the Bundle Sheath of Maize1

Energy-Oriented Organelles and Activities: III The Chloroplast and Photosynthesis

The roles of malate and aspartate in C4 photosynthetic metabolism of Flaveria bidentis (L.)

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