Roles of isoamylase and ADP-glucose pyrophosphorylase in starch granule synthesis in rice endosperm

Plant Journal

Volumn 42, Issue 2, 2005, Pages 164-174

  Kawagoe, Yasushi ^a   Kubo, Akiko ^b   Satoh, Hikaru ^c   Takaiwa, Fumio ^a   Nakamura, Yasunori ^b  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b AKITA PREFECTURAL UNIVERSITY   (Japan)

^c KYUSHU UNIVERSITY   (Japan)

Author keywords

ADP glucose pyrophosphorylase; Amyloplast; GFP; Isoamylase; Rice endosperm; Starch biosynthesis

Indexed keywords

GRANULAR MATERIALS; MUTAGENESIS; PROTEINS; RANDOM PROCESSES; STARCH;

GREEN FLUORESCENT PROTEIN (GFP); ISOAMYLASE1 (ISA1); PHYTOGLYCOGENS; PLEOMORPHIC AMYLOPLASTS;

ENZYME KINETICS;

GLUCAN; GLUCOSE 1 PHOSPHATE ADENYLYLTRANSFERASE; ISOAMYLASE; NUCLEOTIDYLTRANSFERASE; STARCH;

ARTICLE; BIOSYNTHESIS; ENZYMOLOGY; GENETICS; METABOLISM; PHYSIOLOGY; PLANT SEED; PLASTID; RICE; TRANSGENIC PLANT; ULTRASTRUCTURE;

GLUCANS; GLUCOSE-1-PHOSPHATE ADENYLYLTRANSFERASE; ISOAMYLASE; NUCLEOTIDYLTRANSFERASES; ORYZA SATIVA; PLANTS, GENETICALLY MODIFIED; PLASTIDS; SEEDS; STARCH;

ENZYMATIC ACTIVITY; GRANULES; MUTAGENS; PROTEINS; RANDOM PROCESSES; STARCH;

EID: 17844364648     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2005.02367.x     Document Type: Article

References (51)

1. Arimura, S.-I., Hirai, A. and Tsutsumi, N. (2001) Numerous and highly developed tubular projections from plastids observed in tobacco epidermal cells. Plant Sci. 160, 449-454.
2. Ball, S., Guan, H.P., James, M., Myers, A., Keeling, P., Mouille, G., Buleon, A., Colonna, P. and Preiss, J. (1996) From glycogen to amylopectin: a model for the biogenesis of the plant starch granule. Cell, 86, 349-352.
3. Beckles, D.M., Smith, A.M. and ap Rees, T. (2001) A cytosolic ADP-glucose pyrophosphorylase is a feature of graminaceous endosperms, but not of other starch-storing organs. Plant Physiol. 125, 818-827.
4. Bhave, M.R., Lawrence, S., Barton, C. and Hannah, L.C. (1990) Identification and molecular characterization of shrunken-2cDNA clones of maize. Plant Cell, 2, 581-588.
5. Burton, R.A., Johnson, P.E., Beckles, D.M., Fincher, G.B., Jenner, H.L., Naldrett, M.J. and Denyer, K. (2002a) Characterization of the genes encoding the cytosolic and plastidial forms of ADP-glucose pyrophosphorylase in wheat endosperm. Plant Physiol. 130, 1464-1475.
6. Burton, R.A., Jenner, H., Carrangis, L. et al. (2002b) Starch granule initiation and growth are altered in barley mutants that lack isoamylase activity. Plant J. 31, 97-112.
7. Cameron, J.W. and Teas, H.J. (1954) Carbohydrate relationships in developing and mature endosperms of brittle and related maize genotypes. Am. J. Bot. 41, 50-55.
8. Choi, S.B., Wang, C.L., Muench, D.G., Ozawa, K., Franceschi, V.R., Wu, Y.J. and Okita, T.W. (2000) Messenger RNA targeting of rice seed storage proteins to specific ER subdomains. Nature, 407, 765-767.
9. Chourey, P.S., Taliercio, E.W., Carlson, S.J. and Ruan, Y.L. (1998) Genetic evidence that the two isozymes of sucrose synthase present in developing maize endosperm are critical, one for cell wall integrity and the other for starch biosynthesis. Mol. Gen. Genet. 259, 88-96.
10. Creech, R.G. (1965) Genetic control of carbohydrate synthesis in maize endosperm. Genetics, 52, 1175-1186.
11. Denyer, K., Dunlap, F., Thorbjornsen, T., Keeling, P. and Smith, A.M. (1996) The major form of ADP-glucose pyrophosphorylase in maize endosperm is extra-plastidial. Plant Physiol. 112, 779-785.
12. Dickinson, D.B. and Preiss, J. (1969) Presence of ADP-glucose pyrophosphorylase in shrunken-2 and brittle-2 mutants in maize endosperm. Plant Physiol. 44, 1058-1062.
13. Dinges, J.R., Colleoni, C., Myers, A.M. and James, M.G. (2001) Molecular structure of three mutations at the maize sugaryl locus and their allele-specific phenotypic effects. Plant Physiol. 125, 1406-1418.
14. Dinges, J.R., Colleoni, C., James, M.G. and Myers, A.M. (2003) Mutational analysis of the pullulanase-type debranching enzyme of maize indicates multiple functions in starch metabolism. Plant Cell, 15, 666-680.
15. Fujita, N., Kubo, A., Francisco, P.B., Nakakita, M., Harada, K., Minaka, N. and Nakamura, Y. (1999) Purification, characterization, and cDNA structure of isoamylase from developing endosperm of rice. Planta, 208, 283-293.
16. Fujita, N., Kubo, A., Suh, D.S., Wong, K.S., Jane, J.L., Ozawa, K., Takaiwa, F., Inaba, Y. and Nakamura, Y. (2003) Antisense inhibition of isoamylase alters the structure of amylopectin and the physicochemical properties of starch in rice endosperm. Plant Cell Physiol. 44, 607-618.
17. Gibson, S.I. (2004) Sugar and phytohormone response pathways: navigating a signalling network. J. Exp. Bot. 55, 253-264.
18. Goto, F., Yoshihara, T., Shigemoto, N., Toki, S. and Takaiwa, F. (1999) Iron fortification of rice seed by the soybean ferritin gene. Nat. Biotechnol. 17, 282-286.
19. Haigler, C.H., Ivanova-Datcheva, M., Hogan, P.S., Salnikov, V.V., Hwang, S., Martin, K. and Delmer, D.P. (2001) Carbon partitioning to cellulose synthesis. Plant Mol. Biol. 47, 29-51.
20. Hannah, L.C., Shaw, J.R., Giroux, M.J., Reyss, A., Prioul, J.-L., Bae, J.-M. and Lee, J.-Y. (2001) Maize genes encoding the small subunit of ADP-glucose pyrophosphorylase. Plant Physiol. 127, 173-183.
21. Hashimoto, H. (2003) Plastid division: its origins and evolution. Intern. Rev. Cytol. 222, 63-98.
22. Hoshikawa, K. (1967) Studies on the development of endosperm in rice. I. Process of endosperm tissue formation. Proc. Crop Sci. Soc. Japan, 36, 151-161.
23. Hoshikawa, K. (1968) Studies on the development of endosperm in rice. 11. Development of starch granules in endosperm tissue. Proc. Crop Sci. Soc. Japan, 37, 207-216.
24. Jane, J.L., Kasemsuwan, T., Leas, S., Zobel, H. and Robyt, J.F. (1994) Anthology of starch granule morphology by scanning electronmicroscopy. Starch-Starke, 46, 121-129.
25. Johnson, P.E., Patron, N.J., Bottrill, A.R., Dinges, J.R., Fahy, B.F., Parker, M.L., Waite, D.N. and Denyer, K. (2003) A low-starch barley mutant, riso 16, lacking the cytosolic small subunit of ADP-glucose pyrophosphorylase, reveals the importance of the cytosolic isoform and the identity of the plastidial small subunit. Plant Physiol. 131, 684-696.
26. Kohler, R.H. and Hanson, M.R. (2000) Plastid tubules of higher plants are tissue-specific and developmentally regulated. J. Cell Sci. 113, 81-89.
27. Kohler, R.H., Cao, J., Zipfel, W.R., Webb, W.W. and Hanson, M.R. (1997) Exchange of protein molecules through connections between higher plant plastids. Science, 276, 2039-2042.
28. Kubo, A., Fujita, N., Harada, K., Matsuda, T., Satoh, H. and Nakamura, Y. (1999) The starch-debranching enzymes isoamylase and pullulanase are both involved in amylopectin biosynthesis in rice endosperm. Plant Physiol. 121, 399-409.
29. Kwok, E.Y. and Hanson, M.R. (2004) GFP-labelled rubisco and aspartate aminotransferase are present in plastid stromules and traffic between plastids. J. Exp. Bot. 55, 595-604.
30. Langeveld, S.M.J., van Wijk, R., Stuurman, N., Kijne, J.W. and de Pater, S. (2000) B-type granule containing protrusions and interconnections between amyloplasts in developing wheat endosperm revealed by transmission electron microscopy and GFP expression. J. Exp. Bot. 51, 1357-1361.
31. Laughnan, J.R. (1953) The effect of the sh2 factor on carbohydrate reserves in the mature endosperm of maize. Genetics, 38, 485-499.
32. Matsuo, T., Yano, M., Satoh, H. and Omura, T. (1987) Effects of sugary and shrunken mutant genes on carbohydrates in rice endosperm during ripening period. Jpn J. Breed. 37, 17-21.
33. Miyagishima, S.Y., Nishida, K. and Kuroiwa, T. (2003) An evolutionary puzzle: chloroplast and mitochondrial division rings. Trends Plant Sci. 8, 432-438.
34. Myers, A.M., Morell, M.K., James, M.G. and Ball, S.G. (2000) Recent progress toward understanding biosynthesis of the amylopectin crystal. Plant Physiol. 122, 989-998.
35. Nakamura, Y. (2002) Towards a better understanding of the metabolic system for amylopectin biosynthesis in plants: rice endosperm as a model tissue. Plant Cell Physiol. 43, 718-725.
36. Nakamura, Y. and Kawaguchi, K. (1992) Multiple forms of ADPglucose pyrophosphorylase of rice endosperm. Physiol. Plant. 84, 336-342.
37. Nakamura, Y., Yuki, K., Park, S.-Y. and Ohya, T. (1989) Carbohydrate metabolism in the developing endosperm of rice grains. Plant Cell Physiol. 30, 833-839.
38. Nakamura, Y., Umemoto, T., Takahata, Y., Komae, K., Amano, E. and Satoh, H. (1996a) Changes in structure of starch and enzyme activities affected by sugary mutations in developing rice endosperm. Possible role of starch debranching enzyme (R-enzyme) in amylopectin biosynthesis. Physiol. Plant, 97, 491-498.
39. Nakamura, Y., Umemoto, T., Ogata, N., Kuboki, Y., Yano, M. and Sasaki, T. (1996b) Starch debranching enzyme (R-enzyme or pullulanase) from developing rice endosperm: purification, cDNA and chromosomal localization of the gene. Planta, 199, 209-218.
40. Nakamura, Y., Kubo, A., Shimamune, T., Matsuda, T., Harada, K. and Satoh, H. (1997) Correlation between activities of starch debranching enzyme and alpha-polyglucan structure in endosperms of sugary-1 mutants of rice. Plant J. 12, 143-153.
41. Osteryoung, K.W. and Nunnari, J. (2003) The division of endosymbiotic organelles. Science, 302, 1698-1704.
42. Satoh, H. and Omura, T. (1981) New endosperm mutations induced by chemical mutagens in rice, Oryza sativa L. Jpn J. Breed. 31, 316-326.
43. Satoh, H., Nishi, A., Fujita, N., Kubo, A., Nakamura, Y., Kawasaki, T. and Okita, T.W. (2003) Isolation and characterization of starch mutants in rice. J. Appl. Glycosci. 50, 225-230.
44. Soll, J. and Schleiff, E. (2004) Protein import into chloroplasts. Nat. Rev. Mol. Cell Biol. 5, 198-208.
45. Tetlow, I.J., Davies, E.J., Vardy, K.A., Bowsher, C.G., Burrell, M.M. and Emes, M.J. (2003) Subcellular localization of ADPglucose pyrophosphorylase in developing wheat endosperm and analysis of the properties of a plastidial isoform. J. Exp. Bot. 54, 715-725.
46. Thorbjornsen, T., Villand, P., Denyer, K., Olsen, O.A. and Smith, A.M. (1996) Distinct isoforms of ADPglucose pyrophosphorylase occur inside and outside the amyloplasts in barley endosperm. Plant J. 10, 243-250.
47. Weber, H., Rolletschek, H., Heim, U., Golombek, S., Gubatz, S. and Wobus, U. (2000) Antisense-inhibition of ADP-glucose pyrophosphorylase in developing seeds of Vicia narbonensis moderately decreases starch but increases protein content and affects seed maturation. Plant J. 24, 33-43.
48. Wong, K.S., Kubo, A., Jane, J.L., Harada, K., Satoh, H. and Nakamura, Y. (2003) Structures and properties of amylopectin and phytoglycogen in the endosperm of sugary-1 mutants of rice. J. Cereal Sci. 37, 139-149.
49. Wu, C.Y., Adachi, T., Hatano, T., Washida, H., Suzuki, A. and Takaiwa, F. (1998) Promoters of rice seed storage protein genes direct endosperm-specific gene expression in transgenic rice. Plant Cell Physiol. 39, 885-889.
50. Yano, M., Isono, Y., Satoh, H. and Omura, T. (1984) Gene analysis of sugary and shrunken mutants of rice, Oryza sativa L. Jpn J. Breed. 34, 43-49.
51. Zeeman, S.C., Umemoto, T., Lue, W.L., Au-Yeung, P., Martin, C., Smith, A.M. and Chen, J. (1998) A mutant of Arabidopsis lacking a chloroplastic isoamylase accumulates both starch and phytoglycogen. Plant Cell, 10, 1699-1711.