Phosphoenolpyruvate Carboxykinase is Involved in the Decarboxylation of Aspartate in the Bundle Sheath of Maize

Overview

Journal Plant Physiol

Specialty Physiology

Date 1999 Jun 11

PMID 10364405

Citations 60

Authors

Wingler

Walker

Chen

Leegood

Affiliations

Soon will be listed here.

Abstract

We recently showed that maize (Zea mays L.) leaves contain appreciable amounts of phosphoenolpyruvate carboxykinase (PEPCK; R.P. Walker, R.M. Acheson, L.I. Tecsi, R.C. Leegood [1997] Aust J Plant Physiol 24: 459-468). In the present study, we investigated the role of PEPCK in C4 photosynthesis in maize. PEPCK activity and protein were enriched in extracts from bundle-sheath (BS) strands compared with whole-leaf extracts. Decarboxylation of [4-14C]aspartate (Asp) by BS strands was dependent on the presence of 2-oxoglutarate and Mn2+, 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 [4-14C]malate was stimulated severalfold by Asp and 3-phosphoglycerate, was only slightly reduced in the absence of Mn2+ 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 NADP-malic enzyme, decarboxylation of Asp is dependent on the activity of PEPCK.

Citing Articles

Biochemical and Structural Diversification of C Photosynthesis in Tribe Zoysieae (Poaceae).

Koteyeva N, Voznesenskaya E, Pathare V, Borisenko T, Zhurbenko P, Morozov G Plants (Basel). 2023; 12(23).

PMID: 38068683 PMC: 10798372. DOI: 10.3390/plants12234049.

Integrating multiple regulations on enzyme activity: the case of phosphopyruvate carboxykinases.

Rojas B, Iglesias A AoB Plants. 2023; 15(4):plad053.

PMID: 37608926 PMC: 10441589. DOI: 10.1093/aobpla/plad053.

Overexpression of chloroplastic Zea mays NADP-malic enzyme (ZmNADP-ME) confers tolerance to salt stress in Arabidopsis thaliana.

Kandoi D, Tripathy B Photosynth Res. 2023; 158(1):57-76.

PMID: 37561272 DOI: 10.1007/s11120-023-01041-x.

Two cyclic electron flows around photosystem I differentially participate in C4 photosynthesis.

Ogawa T, Kobayashi K, Taniguchi Y, Shikanai T, Nakamura N, Yokota A Plant Physiol. 2023; 191(4):2288-2300.

PMID: 36703198 PMC: 10069883. DOI: 10.1093/plphys/kiad032.

Distinct C sub-types and C bundle sheath isolation in the Paniceae grasses.

Washburn J, Strable J, Dickinson P, Kothapalli S, Brose J, Covshoff S Plant Direct. 2022; 5(12):e373.

PMID: 34988355 PMC: 8711749. DOI: 10.1002/pld3.373.

References

Numazawa T, Yamada S, Hase T, Sugiyama T . Aspartate aminotransferase from Panicum maximum Jacq. var. trichoglume Eyles, a C4 plant: purification, molecular properties, and preparation of antibody. Arch Biochem Biophys. 1989; 270(1):313-9. DOI: 10.1016/0003-9861(89)90033-7. View

Langdale J, Rothermel B, Nelson T . Cellular pattern of photosynthetic gene expression in developing maize leaves. Genes Dev. 1988; 2(1):106-15. DOI: 10.1101/gad.2.1.106. View

Hatch M, Kagawa T . Photosynthetic activities of isolated bundle sheath cells in relation to differing mechanisms of C-4 pathway photosynthesis. Arch Biochem Biophys. 1976; 175(1):39-53. DOI: 10.1016/0003-9861(76)90483-5. View

Hatch M . The C 4 -pathway of photosynthesis. Evidence for an intermediate pool of carbon dioxide and the identity of the donor C 4 -dicarboxylic acid. Biochem J. 1971; 125(2):425-32. PMC: 1178076. DOI: 10.1042/bj1250425. View

Walker R, Leegood R . Phosphorylation of phosphoenolpyruvate carboxykinase in plants. Studies in plants with C4 photosynthesis and Crassulacean acid metabolism and in germinating seeds. Biochem J. 1996; 317 ( Pt 3):653-8. PMC: 1217536. DOI: 10.1042/bj3170653. View

Chapman K, Berry J, Hatch M . Photosynthetic metabolism in bundle sheath cells of the C4 species Zea mays: Sources of ATP and NADPH and the contribution of photosystem II. Arch Biochem Biophys. 1980; 202(2):330-41. DOI: 10.1016/0003-9861(80)90435-x. View

Creach E, Michel J, Thibault P . Aspartic acid as an internal CO2 reservoir in Zea mays: Effect of oxygen concentration and of far-red illumination. Planta. 2014; 118(2):91-100. DOI: 10.1007/BF00388386. View

Stokes D, Walker D . Photosynthesis by isolated chloroplasts. Inhibition by DL-glyceraldehyde of carbon dioxide assimilation. Biochem J. 1972; 128(5):1147-57. PMC: 1174003. DOI: 10.1042/bj1281147. View

Walker R, Leegood R . Purification, and phosphorylation in vivo and in vitro, of phosphoenolpyruvate carboxykinase from cucumber cotyledons. FEBS Lett. 1995; 362(1):70-4. DOI: 10.1016/0014-5793(95)00212-r. View

10.

Schramm V, Hanson R . Mechanism of 3-mercaptopicolinic acid inhibition of hepatic phosphoenolpyruvate carboxykinase (GTP). J Biol Chem. 1976; 251(1):37-44. View

11.

Hatch M . Synthesis of L-malate-4- 14 C and determination of label in the C-4 carboxyl of L-malate. Anal Biochem. 1972; 47(1):174-83. DOI: 10.1016/0003-2697(72)90290-4. View

12.

Boag S, Jenkins C . The Involvement of Aspartate and Glutamate in the Decarboxylation of Malate by Isolated Bundle Sheath Chloroplasts from Zea mays. Plant Physiol. 1986; 81(1):115-9. PMC: 1075292. DOI: 10.1104/pp.81.1.115. View

13.

Rathnam C, Edwards G . C4-Dicarboxylic acid metabolism in bundle-sheath chloroplasts, mitochondria and strands of Eriochloa borumensis Hack., a phosphoenolpyruvate-carboxykinase type C4 species. Planta. 2014; 133(2):135-44. DOI: 10.1007/BF00391911. View

14.

Muench D, Good A . Hypoxically inducible barley alanine aminotransferase: cDNA cloning and expression analysis. Plant Mol Biol. 1994; 24(3):417-27. DOI: 10.1007/BF00024110. View

15.

Smith A, Woolhouse H . Metabolism of phosphoenolpyruvate in the C4 cycle during photosynthesis in the phosphoenolpyruvate-carboxykinase C4 grass Spartina anglica Hubb. Planta. 2013; 159(6):570-8. DOI: 10.1007/BF00409147. View

16.

Valle E, Heldt H . Alanine synthesis by bundle sheath cells of maize. Plant Physiol. 1991; 95(3):839-45. PMC: 1077614. DOI: 10.1104/pp.95.3.839. View

17.

Gutierrez M, Gracen V, Edwards G . Biochemical and cytological relationships in C4 plants. Planta. 2014; 119(4):279-300. DOI: 10.1007/BF00388331. View

18.

Baysdorfer C, Bassham J . Spinach pyruvate kinase isoforms : partial purification and regulatory properties. Plant Physiol. 1984; 74(2):374-9. PMC: 1066685. DOI: 10.1104/pp.74.2.374. View

19.

Chapman K, Hatch M . Aspartate stimulation of malate decarboxylation in Zea mays bundle sheath cells: possible role in regulation of C4 photosynthesis. Biochem Biophys Res Commun. 1979; 86(4):1274-80. DOI: 10.1016/0006-291x(79)90254-7. View