Direct Transport of ADPglucose by an Adenylate Translocator is Linked to Starch Biosynthesis in Amyloplasts

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1991 Jul 1

PMID 11607196

Citations 21

Authors

J Pozueta-Romero

M Frehner

A M Viale

T Akazawa

Affiliations

Soon will be listed here.

Abstract

Starch biosynthesis has been studied by using amyloplasts isolated from cultured cells of sycamore trees (Acer pseudoplatanus L.). Highly purified intact amyloplasts, free from mitochondria and starch granules derived from broken amyloplasts, were isolated from a Percoll step gradient. Subsequently, the double silicone oil layer centrifugation technique was used to study adenylate transport in the amyloplasts. An adenylate-specific carrier was found to be active in the uptake of ATP, ADP, AMP, and most importantly, ADPglucose (ADP-Glc). Kinetic analyses showed that the uptake of these adenylates was mutually competitive with each other. In contrast to the mitochondrial adenylate carrier, in amyloplasts only ATP and ADP-Glc uptake were inhibited by carboxyatractyloside. Evidence is presented that the ADP-Glc transported into the amyloplast stroma can be used in starch synthesis catalyzed by starch synthase (ADP-Glc:1,4-alpha-D-glucan 4-alpha-D-glucosyltransferase, EC 2.4.1.21). We propose that starch biosynthesis in amyloplasts is tightly coupled with the direct transport of ADP-Glc synthesized in the cytosol by sucrose synthase (ADP-Glc:D-fructose 2-alpha-D-glucosyltransferase, EC 2.4.1.13)

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References

Lizotte P, Henson C, Duke S . Purification and Characterization of Pea Epicotyl beta-Amylase. Plant Physiol. 1990; 92(3):615-21. PMC: 1062343. DOI: 10.1104/pp.92.3.615. View

Ngernprasirtsiri J, Harinasut P, Macherel D, Strzalka K, Takabe T, Akazawa T . Isolation and Characterization of the Amyloplast Envelope-Membrane from Cultured White-Wild Cells of Sycamore (Acer pseudoplatanus L.). Plant Physiol. 1988; 87(2):371-8. PMC: 1054759. DOI: 10.1104/pp.87.2.371. View

Keeling P, Wood J, Tyson R, Bridges I . Starch Biosynthesis in Developing Wheat Grain : Evidence against the Direct Involvement of Triose Phosphates in the Metabolic Pathway. Plant Physiol. 1988; 87(2):311-9. PMC: 1054750. DOI: 10.1104/pp.87.2.311. 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

Echeverria E, Boyer C, Thomas P, Liu K, Shannon J . Enzyme activities associated with maize kernel amyloplasts. Plant Physiol. 1988; 86(3):786-92. PMC: 1054571. DOI: 10.1104/pp.86.3.786. View

Doehlert D, Kuo T . Sugar metabolism in developing kernels of starch-deficient endosperm mutants of maize. Plant Physiol. 1990; 92(4):990-4. PMC: 1062406. DOI: 10.1104/pp.92.4.990. View

Ngernprasirtsiri J, Takabe T, Akazawa T . Immunochemical Analysis Shows That an ATP/ADP-Translocator Is Associated with the Inner-Envelope Membranes of Amyloplasts from Acer pseudoplatanus L. Plant Physiol. 1989; 89(4):1024-7. PMC: 1055967. DOI: 10.1104/pp.89.4.1024. View

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

Liu T, Shannon J . Measurement of Metabolites Associated with Nonaqueously Isolated Starch Granules from Immature Zea mays L. Endosperm. Plant Physiol. 1981; 67(3):525-9. PMC: 425718. DOI: 10.1104/pp.67.3.525. View

10.

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

11.

Entwistle G, Rees T . Enzymic capacities of amyloplasts from wheat (Triticum aestivum) endosperm. Biochem J. 1988; 255(2):391-6. PMC: 1135240. DOI: 10.1042/bj2550391. View

12.

Macherel D, Kobayashi H, Akazawa T, Kawano S, Kuroiwa T . Amyloplast nucleoids in sycamore cells and presence in amyloplast DNA of homologous sequences to chloroplast genes. Biochem Biophys Res Commun. 1985; 133(1):140-6. DOI: 10.1016/0006-291x(85)91852-2. View

13.

Chourey P, Nelson O . The enzymatic deficiency conditioned by the shrunken-1 mutations in maize. Biochem Genet. 1976; 14(11-12):1041-55. DOI: 10.1007/BF00485135. View

14.

Vignais P, Vignais P, Defaye G . Adenosine diphosphate translocation in mitochondria. Nature of the receptor site for carboxyatractyloside (gummiferin). Biochemistry. 1973; 12(8):1508-19. DOI: 10.1021/bi00732a007. View

15.

Pfaff E, Klingenberg M . Adenine nucleotide translocation of mitochondria. 1. Specificity and control. Eur J Biochem. 1968; 6(1):66-79. DOI: 10.1111/j.1432-1033.1968.tb00420.x. View

16.

Murata T, Sugiyama T, Minamikawa T, Akazawa T . Enzymic mechanism of starch synthesis in ripening rice grains. 3. Mechanism of the sucrose-starch conversion. Arch Biochem Biophys. 1966; 113(1):34-44. DOI: 10.1016/0003-9861(66)90153-6. View