ADP-Glucose Transport by the Chloroplast Adenylate Translocator Is Linked to Starch Biosynthesis

Overview

Journal Plant Physiol

Specialty Physiology

Date 1991 Dec 1

PMID 16668585

Citations 13

Authors

J Pozueta-Romero

F Ardila

T Akazawa

Affiliations

Soon will be listed here.

Abstract

In organello starch biosynthesis was studied using intact chloroplasts isolated from spinach leaves (Spinacia oleracea). Immunoblot analysis using a specific antiserum against the mitochondrial adenylate (ADP/ATP) translocator of Neurospora crassa shows the presence of an adenylate translocator protein in the chloroplast envelope membranes, similar to that existing in mitochondria and amyloplasts from cultured cells of sycamore (Acer pseudoplatanus). The double silicone oil layer-filtering centrifugation technique was employed to study the kinetic properties of adenylate transport in the purified chloroplasts; ATP, ADP, AMP, and most importantly ADP-Glc were shown to be recognized by the adenylate translocator. Similar to the situation with sycamore amyloplasts, only ATP and ADP-Glc uptake was inhibited by carboxyatractyloside, an inhibitor of the mitochondrial adenylate translocator. Evidence is presented to show that the ADP-Glc transported into the chloroplast stroma is utilized for starch synthesis catalyzed by starch synthase (ADP-Glc:1,4-alpha-d-glucan 4-alpha-d-glucosyltransferase). The high activity of sucrose synthase producing ADP-Glc observed in the extrachloroplastic fractions suggests that starch biosynthesis in chloroplasts may be coupled with the direct import of ADP-Glc from the cytosol.

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References

Fliege R, Flugge U, Werdan K, Heldt H . Specific transport of inorganic phosphate, 3-phosphoglycerate and triosephosphates across the inner membrane of the envelope in spinach chloroplasts. Biochim Biophys Acta. 1978; 502(2):232-47. DOI: 10.1016/0005-2728(78)90045-2. View

Heldt H . Adenine nucleotide translocation in spinach chloroplasts. FEBS Lett. 1969; 5(1):11-14. DOI: 10.1016/0014-5793(69)80280-2. View

Giaquinta R . Source and sink leaf metabolism in relation to Phloem translocation: carbon partitioning and enzymology. Plant Physiol. 1978; 61(3):380-5. PMC: 1091872. DOI: 10.1104/pp.61.3.380. View

Erdelt H, Weidemann M, Buchholz M, Klingenberg M . Some principle effects of bongkrekic acid on the binding of adenine nucleotides to mitochondrial membranes. Eur J Biochem. 1972; 30(1):107-22. DOI: 10.1111/j.1432-1033.1972.tb02077.x. View

Gibbs M, Kandler O . ASYMMETRIC DISTRIBUTION OF C IN SUGARS FORMED DURING PHOTOSYNTHESIS. Proc Natl Acad Sci U S A. 1957; 43(6):446-51. PMC: 528478. DOI: 10.1073/pnas.43.6.446. View

Stitt M, Kurzel B, Heldt H . Control of Photosynthetic Sucrose Synthesis by Fructose 2,6-Bisphosphate : II. Partitioning between Sucrose and Starch. Plant Physiol. 1984; 75(3):554-60. PMC: 1066954. DOI: 10.1104/pp.75.3.554. View

Huber S, Akazawa T . A novel sucrose synthase pathway for sucrose degradation in cultured sycamore cells. Plant Physiol. 1986; 81(4):1008-13. PMC: 1075476. DOI: 10.1104/pp.81.4.1008. View

Heldt H, Chon C, Maronde D . Role of orthophosphate and other factors in the regulation of starch formation in leaves and isolated chloroplasts. Plant Physiol. 1977; 59(6):1146-55. PMC: 542524. DOI: 10.1104/pp.59.6.1146. View

Heber U, Santarius K . Direct and indirect transfer of ATP and ADP across the chloroplast envelope. Z Naturforsch B. 1970; 25(7):718-28. DOI: 10.1515/znb-1970-0714. View

10.

Wintermans J, DE MOTS A . Spectrophotometric characteristics of chlorophylls a and b and their pheophytins in ethanol. Biochim Biophys Acta. 1965; 109(2):448-53. DOI: 10.1016/0926-6585(65)90170-6. View

11.

Pozueta-Romero J, Frehner M, Akazawa T . Filtering centrifugation through two layers of silicone oil: a method for the kinetic analysis of rapid metabolite transport in organelles. Cell Struct Funct. 1991; 16(5):357-63. DOI: 10.1247/csf.16.357. View

12.

Frehner M, Pozueta-Romero J, Akazawa T . Enzyme Sets of Glycolysis, Gluconeogenesis, and Oxidative Pentose Phosphate Pathway Are Not Complete in Nongreen Highly Purified Amyloplasts of Sycamore (Acer pseudoplatanus L.) Cell Suspension Cultures. Plant Physiol. 1990; 94(2):538-44. PMC: 1077266. DOI: 10.1104/pp.94.2.538. View

13.

Silvius J, Snyder F . Comparative Enzymic Studies of Sucrose Metabolism in the Taproots and Fibrous Roots of Beta vulgaris L. Plant Physiol. 1979; 64(6):1070-3. PMC: 543193. DOI: 10.1104/pp.64.6.1070. View

14.

Kandler O, Gibbs M . [Studies on effect of photosynthesis on exchange processes within the hexose molecule]. Z Naturforsch B. 1959; 14B(1):8-13. View

15.

Stitt M, Bulpin P, Ap Rees T . Pathway of starch breakdown in photosynthetic tissues of Pisum sativum. Biochim Biophys Acta. 1978; 544(1):200-14. DOI: 10.1016/0304-4165(78)90223-4. View

16.

Havir E, Gibbs M . STUDIES ON THE REDUCTIVE PENTOSE PHOSPHATE CYCLE IN INTACT AND RECONSTITUTED CHLOROPLAST SYSTEMS. J Biol Chem. 1963; 238:3183-7. View

17.

Maclachlan G, Porter H . Replacement of oxidation by light as the energy source for glucose metabolism in tobacco leaf. Proc R Soc Lond B Biol Sci. 1959; 150:460-73. DOI: 10.1098/rspb.1959.0035. View

18.

Pozueta-Romero J, Frehner M, Viale A, Akazawa T . Direct transport of ADPglucose by an adenylate translocator is linked to starch biosynthesis in amyloplasts. Proc Natl Acad Sci U S A. 1991; 88(13):5769-73. PMC: 51959. DOI: 10.1073/pnas.88.13.5769. View

19.

Vignais P, Douce R, Lauquin G, Vignais P . Binding of radioactively labeled carboxyatractyloside, atractyloside and bongkrekic acid to the ADP translocator of potato mitochondria. Biochim Biophys Acta. 1976; 440(3):688-96. DOI: 10.1016/0005-2728(76)90051-7. View

20.

Schafer G, Heber U . Glucose transport into spinach chloroplasts. Plant Physiol. 1977; 60(2):286-9. PMC: 542597. DOI: 10.1104/pp.60.2.286. View