Plant Molecular Biology

, Volume 65, Issue 4, pp 531–546 | Cite as

Identification of the ADP-glucose pyrophosphorylase isoforms essential for starch synthesis in the leaf and seed endosperm of rice (Oryza sativa L.)

  • Sang-Kyu Lee
  • Seon-Kap Hwang
  • Muho Han
  • Joon-Seob Eom
  • Hong-Gyu Kang
  • Yulyi Han
  • Sang-Bong Choi
  • Man-Ho Cho
  • Seong Hee Bhoo
  • Gynheung An
  • Tae-Ryong Hahn
  • Thomas W. Okita
  • Jong-Seong Jeon
Article

Abstract

ADP-glucose pyrophosphorylase (AGP) catalyzes the first committed step of starch biosynthesis in higher plants. To identify AGP isoforms essential for this biosynthetic process in sink and source tissues of rice plants, we analyzed the rice AGP gene family which consists of two genes, OsAGPS1 and OsAGPS2, encoding small subunits (SSU) and four genes, OsAGPL1, OsAGPL2, OsAGPL3 and OsAGPL4, encoding large subunits (LSU) of this enzyme heterotetrameric complex. Subcellular localization studies using green fluorescent protein (GFP) fusion constructs indicate that OsAGPS2a, the product of the leaf-preferential transcript of OsAGPS2, and OsAGPS1, OsAGPL1, OsAGPL3, and OsAGPL4 are plastid-targeted isoforms. In contrast, two isoforms, SSU OsAGPS2b which is a product of a seed-specific transcript of OsAGPS2, and LSU OsAGPL2, are localized in the cytosol. Analysis of osagps2 and osagpl2 mutants revealed that a lesion of one of the two cytosolic isoforms, OsAGPL2 and OsAGPS2b, causes a shrunken endosperm due to a remarkable reduction in starch synthesis. In leaves, however, only the osagps2 mutant appears to severely reduce the transitory starch content. Interestingly, the osagps2 mutant was indistinguishable from wild type during vegetative plant growth. Western blot analysis of the osagp mutants and wild type plants demonstrated that OsAGPS2a is an SSU isoform mainly present in leaves, and that OsAGPS2b and OsAGPL2 are the major SSU and LSU isoforms, respectively, in the endosperm. Finally, we propose a spatiotemporal complex model of OsAGP SSU and LSU isoforms in leaves and in developing endosperm of rice plants.

Keywords

ADP-glucose pyrophosphorylase Endosperm Mutant Rice Starch Subcellular localization 

Notes

Acknowledgements

We thank Dr. Pieter Ouwerkerk (Institute of Biology, Leiden University, The Netherlands) for the binary vector pC1300intC. This work was supported, in part, by grants from SRC for the Plant Metabolism Research Center (PMRC), Korea Science and Engineering Foundation (KOSEF) Program; from the Biogreen 21 Program, Rural Development Administration; from the Crop Functional Genomic Center (CG1422 and CG1111), the 21 Century Frontier Program; and from the BK21 Program, Ministry of Education and Human Resources Development. S.-K. H. and T.W.O. gratefully acknowledge support by the U.S. Department of Energy Grant No. DE-FG02-96ER20216.

References

  1. Akihiro T, Mizuno K, Fujimura T (2005) Gene expression of ADP-glucose pyrophosphorylase and starch contents in rice cultured cells are cooperatively regulated by sucrose and ABA. Plant Cell Physiol 46:937–946PubMedCrossRefGoogle Scholar
  2. Ballicora MA, Dubay JR, Devillers CH, Preiss J (2005) Resurrecting the ancestral enzymatic role of a modulatory subunit. J Biol Chem 280:10189–10195PubMedCrossRefGoogle Scholar
  3. Ballicora MA, Laughlin MJ, Fu Y, Okita TW, Barry GF, Preiss J (1995) Adenosine 5′-diphosphate-glucose pyrophosphorylase from potato tuber. Significance of the N terminus of the small subunit for catalytic properties and heat stability. Plant Physiol 109:245–251PubMedCrossRefGoogle Scholar
  4. Banks W, Greenwood CT (1975) Starch and its components. Edinburgh University Press, Edinburgh, ScotlandGoogle Scholar
  5. Baroja-Fernández E, Muñoz FJ, Akazawa T, Pozueta-Romero J (2001) Reappraisal of the currently prevailing model of starch biosynthesis in photosynthetic tissues: A proposal involving the cytosolic production of ADP-glucose by sucrose synthase and occurrence of cyclic turnover of starch in the chloroplast. Plant Cell Physiol 42:1311–1320PubMedCrossRefGoogle Scholar
  6. Baroja-Fernández E, Muñoz FJ, Zandueta-Criado A, Morán-Zorzano MT, Viale AM, Alonso-Casajús N, Pozueta-Romero J (2004) Most of ADP glucose linked to starch biosynthesis occurs outside the chloroplast in source leaves. Proc Natl Acad Sci USA 101:13080–13085PubMedCrossRefGoogle Scholar
  7. Beckles DM, Smith AM, ap Rees T (2001a) A cytosolic ADP-glucose pyrophosphorylase is a feature of graminaceous endosperms, but not of other starch-storing organs. Plant Physiol 125:818–827CrossRefGoogle Scholar
  8. Beckles DM, Craig J, Smith AM (2001b) ADP-glucose pyrophosphorylase is located in the plastid in developing tomato fruit. Plant Physiol 126:261–266CrossRefGoogle Scholar
  9. Bhave MR, Lawrence S, Barton C, Hannah LC (1990) Identification and molecular characterization of shrunken-2 cDNA clones of maize. Plant Cell 2:581–588PubMedCrossRefGoogle Scholar
  10. Burger B, Cross J, Okita TW, Hannah LC (2003) Relative turnover numbers of maize endosperm and potato tuber ADPglucose pyrophosphorylases in the absence and presence of 3-PGA. Planta 217:449–456PubMedCrossRefGoogle Scholar
  11. Burton RA, Johnson PE, Beckles DM, Fincher GB, Jenner HL, Naldrett MJ, Denyer K (2002) Characterization of the genes encoding the cytosolic and plastidial forms of ADP-glucose pyrophosphorylase in wheat endosperm. Plant Physiol 130:1464–1475PubMedCrossRefGoogle Scholar
  12. Choi SB, Kim KH, Kavakli IH, Lee SK, Okita TW (2001) Transcriptional expression characteristics and subcellular localization of ADP-glucose pyrophosphorylase in the oil plant Perilla frutescens. Plant Cell Physiol 42:146–153PubMedCrossRefGoogle Scholar
  13. Choi SB, Zhang Y, Ito H, Stephens K, Winder T, Edwards GE, Okita TW (1998) Increasing rice productivity by manipulation of starch biosynthesis during seed development. In: Armstrong DG, Riley R, Waterlow JC (eds) Feeding a world population of more than eight billion people: a challenge to science. Oxford University Press, New York, pp 137–149Google Scholar
  14. Crevillén P, Ballicora MA, Mérida A, Preiss J, Romero JM (2003) The different large subunit isoforms of Arabidopsis thaliana ADP-glucose pyrophosphorylase confer distinct kinetic and regulatory properties to the heterotetrameric enzyme. J Biol Chem 278:28508–28515PubMedCrossRefGoogle Scholar
  15. Denyer K, Dunlap F, Thorbjornsen T, Keeling P, Smith AM (1996) The major form of ADP-glucose pyrophosphorylase in maize endosperm is extra-plastidial. Plant Physiol 112:779–785PubMedCrossRefGoogle Scholar
  16. Doan DN, Rudi H, Olsen OA (1999) The allosterically unregulated isoform of ADP-glucose pyrophosphorylase from barley endosperm is the most likely source of ADP-glucose incorporated into endosperm starch. Plant Physiol 121:965–975PubMedCrossRefGoogle Scholar
  17. Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300:1005–1016PubMedCrossRefGoogle Scholar
  18. Geigenberger P, Kolbe A, Tiessen A (2005) Redox regulation of carbon storage and partitioning in response to light and sugars. J Exp Bot 56:1469–1479PubMedCrossRefGoogle Scholar
  19. Giroux MJ, Boyer C, Feix G, Hannah LC (1994) Coordinated transcriptional regulation of storage product genes in the maize endosperm. Plant Physiol 106:713–722PubMedGoogle Scholar
  20. Giroux MJ, Hannah LC (1994) ADP-glucose pyrophosphorylase in shrunken-2 and brittle-2 mutants of maize. Mol Gen Genet 243:400–408PubMedGoogle Scholar
  21. Giroux MJ, Shaw J, Barry G, Cobb BG, Greene T, Okita T Hannah LC (1996) A single mutation that increases maize seed weight. Proc Natl Acad Sci USA 93:5824–5829PubMedCrossRefGoogle Scholar
  22. Greene TW, Hannah LC (1998) Maize endosperm ADP-glucose pyrophosphorylase SHRUNKEN2 and BRITTLE2 subunit interactions. Plant Cell 10:1295–1306PubMedCrossRefGoogle Scholar
  23. Greene TW, Kavakli IH, Kahn ML, Okita TW (1998) Generation of up-regulated allosteric variants of potato ADP-glucose pyrophosphorylase by reversion genetics. Proc Natl Acad Sci USA 95:10322–10327PubMedCrossRefGoogle Scholar
  24. Hannah LC, Shaw JR, Giroux MJ, Reyss A, Prioul JL, Bae JM, Lee JY (2001) Maize genes encoding the small subunit of ADP-glucose pyrophosphorylase. Plant Physiol 127:173–183PubMedCrossRefGoogle Scholar
  25. Haugen TH, Ishaque A, Preiss J (1976) Biosynthesis of bacterial glycogen. characterization of the subunit structure of Escherichia coli B glucose-1-phosphate adenylyltransferase (EC 2.7.7.27). J Biol Chem 251:7880–7885PubMedGoogle Scholar
  26. Hendriks JH, Kolbe A, Gibon Y, Stitt M, Geigenberger P (2003) ADP-glucose pyrophosphorylase is activated by posttranslational redox-modification in response to light and to sugars in leaves of Arabidopsis and other plant species. Plant Physiol 133:838–849PubMedCrossRefGoogle Scholar
  27. Hirose T, Ohdan T, Nakamurac Y, Teraoa T (2006) Expression profiling of genes related to starch synthesis in rice leaf sheaths during the heading period. Physiol Plant 128:425–435CrossRefGoogle Scholar
  28. Hwang SK, Hamada S, Okita TW (2006) ATP binding site in the plant ADP-glucose pyrophosphorylase large subunit. FEBS Lett 580:6741–6748PubMedCrossRefGoogle Scholar
  29. Hwang SK, Hamada S, Okita TW (2007) Catalytic implications of the higher plant ADP-glucose pyrophosphorylase large subunit. Phytochemistry doi:10.1016/j.phytochem. 2006.11.027Google Scholar
  30. Hwang SK, Salamone PR, Okita TW (2005) Allosteric regulation of the higher plant ADP-glucose pyrophosphorylase is a product of synergy between the two subunits. FEBS Lett 579:983–990PubMedCrossRefGoogle Scholar
  31. International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800CrossRefGoogle Scholar
  32. James MG, Denyer K, Myers AM (2003) Starch synthesis in the cereal endosperm. Curr Opin Plant Biol 6:215–222PubMedCrossRefGoogle Scholar
  33. Jang JC, Sheen J (1994) Sugar sensing in higher plants. Plant Cell 6:1665–1679PubMedCrossRefGoogle Scholar
  34. Jelitto T, Sonnewald U, Willmitzer L, Hajirezaei M, Stitt M (1992) Inorganic pyrophosphate content and metabolites in leaves and tubers of potato and tobacco plants expressing E. coli pyrophosphatase in the cytosol: biochemical evidence that sucrose metabolism has been manipulated. Planta 188:238–244CrossRefGoogle Scholar
  35. Jeon J, An G (2001) Gene tagging in rice: A high throughput system for functional genomics. Plant Sci 161:211–219PubMedCrossRefGoogle Scholar
  36. Jeon JS, Lee S, Jung KH, Jun SH, Jeong DH, Lee J, Kim C, Jang S, Yang K, Nam J, An K, Han MJ, Sung RJ, Choi HS, Yu JH, Choi JH, Cho SY, Cha SS, Kim SI, An G (2000) T-DNA insertional mutagenesis for functional genomics in rice. Plant J 22:561–570PubMedCrossRefGoogle Scholar
  37. Johnson PE, Patron NJ, Bottrill AR, Dinges JR, Fahy BF, Parker ML, Waite DN, 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 131:684–696PubMedCrossRefGoogle Scholar
  38. Kavakli IH, Kato C, Choi SB, Kim KH, Salamone PR, Ito H, Okita TW (2002) Generation, characterization, and heterologous expression of wild-type and up-regulated forms of Arabidopsis thaliana leaf ADP-glucose pyrophosphorylase. Planta 215:430–439PubMedCrossRefGoogle Scholar
  39. Kawagoe Y, Kubo A, Satoh H, Takaiwa F, Nakamura Y (2005) Roles of isoamylase and ADP-glucose pyrophosphorylase in starch granule synthesis in rice endosperm. Plant J 42:164–174PubMedCrossRefGoogle Scholar
  40. Kolbe A, Tiessen A, Schluepmann H, Paul M, Ulrich S, Geigenberger P (2005) Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase. Proc Natl Acad Sci USA 102:11118–11123PubMedCrossRefGoogle Scholar
  41. Lee JW, Lee DS, Bhoo SH, Jeon JS, Lee YH, Hahn TR (2005) Transgenic Arabidopsis plants expressing Escherichia coli pyrophosphatase display both altered carbon partitioning in their source leaves and reduced photosynthetic activity. Plant Cell Rep 24:374–382PubMedCrossRefGoogle Scholar
  42. Lee S, Kim J, Son JS, Nam J, Jeong DH, Lee K, Jang S, Yoo J, Lee J, Lee DY, Kang HG, An G (2003) Systematic reverse genetic screening of T-DNA tagged genes in rice for functional genomic analyses: MADS-box genes as a test case. Plant Cell Physiol 44:1403–1411PubMedCrossRefGoogle Scholar
  43. Lin TP, Caspar T, Somerville CR, Preiss J (1988a) Isolation and characterization of a starchless mutant of Arabidopsis thaliana (L.) Heynh lacking ADPglucose pyrophosphorylase activity. Plant Physiol 86:1131–1135Google Scholar
  44. Lin TP, Caspar T, Somerville CR, Preiss J (1988b) A starch deficient mutant of Arabidopsis thaliana with low ADPglucose pyrophosphorylase activity lacks one of the two subunits of the enzyme. Plant Physiol 88:1175–1181Google Scholar
  45. Lu Y, Sharkey TD (2006) The importance of maltose in transitory starch breakdown. Plant Cell Environ 29:353–366PubMedCrossRefGoogle Scholar
  46. Luo C, Dejardin A, Villand P, Doan DN, Kleczkowski LA (1997) Differential processing of homologues of the small subunit of ADP-glucose pyrophosphorylase from barley (Hordeum vulgare) tissues. Z Naturforsch [C] 52:807–811Google Scholar
  47. Morell MK, Myers AM (2005) Towards the rational design of cereal starches. Curr Opin Plant Biol 8:204–210PubMedCrossRefGoogle Scholar
  48. Murchie EH, Yang J, Hubbart S, Horton P, Peng S (2002) Are there associations between grain-filling rate and photosynthesis in the flag leaves of field-grown rice? J Exp Bot 53:2217–2224PubMedCrossRefGoogle Scholar
  49. Müller-Röber BT, Kossmann J, Hannah LC, Willmitzer L, Sonnewald U (1990) One of two different ADP-glucose pyrophosphorylase genes from potato responds strongly to elevated levels of sucrose. Mol Gen Genet 224:136–146PubMedCrossRefGoogle Scholar
  50. Muñoz FJ, Baroja-Fernández E, Morán-Zorzano MT, Viale AM, Etxeberria E, Alonso-Casajús N, Pozueta-Romero J (2005) Sucrose synthase controls both intracellular ADP glucose levels and transitory starch biosynthesis in source leaves. Plant Cell Physiol 46:1366–1376PubMedCrossRefGoogle Scholar
  51. Nakano H, Makino A, Mae T (1995) Effects of panicle removal on the photosynthetic characteristics of the flag leaf of rice plants during the ripening stage. Plant cell Physiol 36:653–659Google Scholar
  52. Nakano H, Makino A, Mae T (1997) The effect of elevated partial pressures of CO2 on the relationship between photosynthetic capacity and N content in rice leaves. Plant Physiol 115:191–198PubMedGoogle Scholar
  53. Nakata PA, Anderson JM, Okita TW (1994) Structure and expression of the potato ADP-glucose pyrophosphorylase small subunit. J Biol Chem 269:30798–30807PubMedGoogle Scholar
  54. Nakata PA, Greene TW, Anderson JM, Smith-White BJ, Okita TW, Preiss J (1991) Comparison of the primary sequences of two potato tuber ADP-glucose pyrophosphorylase subunits. Plant Mol Biol 17:1089–1093PubMedCrossRefGoogle Scholar
  55. Nelson OE (1982) Genetic control of polysaccharide and storage protein synthesis in endosperms of barley, maize and sorghum. In: Pomeranz Y (ed) Advances in cereal science and technology, vol III. American Association of Cereal Chemists, St. Paul, pp 41–71Google Scholar
  56. Niittylä T, Messerli G, Trevisan M, Chen J, Smith AM, Zeeman SC (2004) A previously unknown maltose transporter essential for starch degradation in leaves. Science 303:87–89PubMedCrossRefGoogle Scholar
  57. Ohdan T, Francisco PB Jr, Sawada T, Hirose T, Terao T, Satoh H, Nakamura Y (2005) Expression profiling of genes involved in starch synthesis in sink and source organs of rice. J Exp Bot 56:3229–3244PubMedCrossRefGoogle Scholar
  58. Okita TW (1992) Is there an alternative pathway for starch synthesis? Plant Physiol 100:560–564PubMedCrossRefGoogle Scholar
  59. Okita TW, Nakata PA, Anderson JM, Sowokinos J, Morell M, Preiss J (1990) The subunit structure of potato tuber ADPglucose pyrophosphorylase. Plant Physiol 93:785–790PubMedGoogle Scholar
  60. Ouwerkerk PB, de Kam RJ, Hoge JH, Meijer AH (2001) Glucocorticoid-inducible gene expression in rice. Planta 213:370–378PubMedCrossRefGoogle Scholar
  61. Patron NJ, Greber B, Fahy BF, Laurie DA, Parker ML, Denyer K (2004) The lys5 mutations of barley reveal the nature and importance of plastidial ADP-glc transporters for starch synthesis in cereal endosperm. Plant Physiol 135:2088–2097PubMedCrossRefGoogle Scholar
  62. Rösti S, Rudi H, Rudi K, Opsahl-Sorteberg HG, Fahy B, Denyer K (2006) The gene encoding the cytosolic small subunit of ADP-glucose pyrophosphorylase in barley endosperm also encodes the major plastidial small subunit in the leaves. J Exp Bot 57:3619–3626PubMedCrossRefGoogle Scholar
  63. Sakulsingharoj C, Choi SB, Ogawa M, Singh S, Bork J, Meyer CR, Edwards GE, Preiss J, Okita TW (2003) Manipulating starch and storage protein biosynthesis during endosperm development to increase rice yield. In: Mew TW, DS Brar DS, S Peng S, Dawe D, Hardy B (eds) Rice science: innovations and impact for livelihood. International Rice Research Institute, Makati City, Philippines, pp 345–359Google Scholar
  64. Salamone PR, Kavakli IH, Slattery CJ, Okita TW (2002) Directed molecular evolution of ADP-glucose pyrophosphorylase. Proc Natl Acad Sci USA 99:1070–1075PubMedCrossRefGoogle Scholar
  65. Schneider A, Hausler RE, Kolukisaoglu U, Kunze R, van der Graaff E, Schwacke R, Catoni E, Desimone M, Flugge UI (2002) An Arabidopsis thaliana knock-out mutant of the chloroplast triose phosphate/phosphate translocator is severely compromised only when starch synthesis, but not starch mobilisation is abolished. Plant J 32:685–699PubMedCrossRefGoogle Scholar
  66. Shannon JC, Pien FM, Cao H, Liu KC (1998) Brittle-1, an adenylate translocator, facilitates transfer of extraplastidial synthesized ADP-glucose into amyloplasts of maize endosperms. Plant Physiol 117:1235–1252PubMedCrossRefGoogle Scholar
  67. Sikka VK, Choi SB, Kavakli IH, Sakulsingharoj C, Gupta S, Ito H, Okita TW (2001) Subcellular compartmentation and allosteric regulation of the rice endosperm ADPglucose pyrophosphorylase. Plant Sci 161:461–468CrossRefGoogle Scholar
  68. Singh S, Choi SB, Modi MK, Okita TW (2002) Isolation and characterization of cDNA clones encoding ADP-glucose pyrophosphorylase (AGPase) large and small subunits from chickpea (Cicer arietinum L.). Phytochemistry 59:261–268PubMedCrossRefGoogle Scholar
  69. Smidansky ED, Clancy M, Meyer FD, Lanning SP, Blake NK, Talbert LE, Giroux MJ (2002) Enhanced ADP-glucose pyrophosphorylase activity in wheat endosperm increases seed yield. Proc Natl Acad Sci USA 99:1724–1729PubMedCrossRefGoogle Scholar
  70. Smidansky ED, Martin JM, Hannah LC, Fischer AM, Giroux MJ (2003) Seed yield and plant biomass increases in rice are conferred by deregulation of endosperm ADP-glucose pyrophosphorylase. Planta 216:656–664PubMedGoogle Scholar
  71. Smidansky ED, Meyer FD, Blakeslee B, Weglarz TE, Greene TW, Giroux MJ (2006) Expression of a modified ADP-glucose pyrophosphorylase large subunit in wheat seeds stimulates photosynthesis and carbon metabolism. Planta DOI 10.1007/s00425-006-0400-3Google Scholar
  72. Smith AM, Denyer K, Martin CR (1995) What controls the amount and structure of starch in storage organs? Plant Physiol 107:673–677PubMedCrossRefGoogle Scholar
  73. Smith AM, Zeeman SC, Smith SM (2005) Starch degradation. Annu Rev Plant Biol 56:73–98PubMedCrossRefGoogle Scholar
  74. Smith-White BJ, Preiss J (1992) Comparison of proteins of ADP-glucose pyrophosphorylase from diverse sources. J Mol Evol 34:449–464PubMedCrossRefGoogle Scholar
  75. Stark DM, Timmermann KP, Barry GF, Preiss J, Kishore GM (1992) Regulation of the amount of starch in plant tissues by ADP-glucose pyrophosphorylase. Science 258:287–292PubMedCrossRefGoogle Scholar
  76. Sun J, Okita TW, Edwards GE (1999) Feedback inhibition of photosynthesis in rice measured by O2 dependent transients. Photosynth Res 59:187–200CrossRefGoogle Scholar
  77. Tetlow IJ, Morell MK, Emes MJ (2004) Recent developments in understanding the regulation of starch metabolism in higher plants. J Exp Bot 55:2131–2145PubMedCrossRefGoogle Scholar
  78. Thorbjørnsen T, Villand P, Denyer K, Olsen OA, Smith AM (1996a) Distinct isoforms of ADPglucose pyrophosphorylase occur inside and outside the amyloplasts in barley endosperm. Plant J 10:243–250CrossRefGoogle Scholar
  79. Thorbjørnsen T, Villand P, Kleczkowski LA, Olsen OA (1996b) A single gene encodes two different transcripts for the ADP-glucose pyrophosphorylase small subunit from barley (Hordeum vulgare). Biochem J 313:149–154Google Scholar
  80. Tiessen A, Hendriks JH, Stitt M, Branscheid A, Gibon Y, Farre EM, Geigenberger P (2002) Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase: A novel regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell 14:2191–2213PubMedCrossRefGoogle Scholar
  81. Vain P, Afolabi AS, Worland B, Snape JW (2003) Transgene behaviour in populations of rice plants transformed using a new dual binary vector system: PGreen/pSoup. Theor Appl Genet 107:210–217PubMedCrossRefGoogle Scholar
  82. Van Camp W (2005) Yield enhancement genes: seeds for growth. Curr Opin Biotechnol 16:147–153PubMedCrossRefGoogle Scholar
  83. Villand P, Olsen OA, Kleczkowski LA (1993) Molecular characterization of multiple cDNA clones for ADP-glucose pyrophosphorylase from Arabidopsis thaliana. Plant Mol Biol 23:1279–1284PubMedCrossRefGoogle Scholar
  84. Walters RG, Ibrahim DG, Horton P, Kruger NJ (2004) A mutant of Arabidopsis lacking the triose-phosphate/phosphate translocator reveals metabolic regulation of starch breakdown in the light. Plant Physiol 135:891–906PubMedCrossRefGoogle Scholar
  85. Wang SM, Chu B, Lue WL, Yu TS, Eimert K, Chen J (1997) adg2-1 represents a missense mutation in the ADPG pyrophosphorylase large subunit gene of Arabidopsis thaliana. Plant J 11:1121–1126PubMedCrossRefGoogle Scholar
  86. Winder TL, Sun J, Okita TW, Edwards GE (1998) Evidence for the occurrence of feedback inhibition of photosynthesis in rice. Plant Cell Physiol 39:813–820Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Sang-Kyu Lee
    • 1
  • Seon-Kap Hwang
    • 2
  • Muho Han
    • 1
  • Joon-Seob Eom
    • 1
  • Hong-Gyu Kang
    • 3
  • Yulyi Han
    • 4
  • Sang-Bong Choi
    • 4
  • Man-Ho Cho
    • 1
  • Seong Hee Bhoo
    • 1
  • Gynheung An
    • 5
  • Tae-Ryong Hahn
    • 1
  • Thomas W. Okita
    • 2
  • Jong-Seong Jeon
    • 1
  1. 1.Graduate School of Biotechnology & Plant Metabolism Research CenterKyung Hee UniversityYonginKorea
  2. 2.Institute of Biological ChemistryWashington State UniversityPullmanUSA
  3. 3.BK21 Life Sciences and BiotechnologyKyungpook National UniversityDaeguKorea
  4. 4.Department of Biological SciencesMyongji UniversityYonginKorea
  5. 5.National Research Laboratory of Plant Functional Genomics, Division of Molecular and Life SciencesPohang University of Science and TechnologyPohangKorea

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