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Theoretical and Applied Genetics

, Volume 128, Issue 10, pp 1893–1916 | Cite as

AGPase: its role in crop productivity with emphasis on heat tolerance in cereals

  • Gautam Saripalli
  • Pushpendra Kumar Gupta
Review

Abstract

Key message

AGPase, a key enzyme of starch biosynthetic pathway, has a significant role in crop productivity. Thermotolerant variants of AGPase in cereals may be used for developing cultivars, which may enhance productivity under heat stress.

Abstract

Improvement of crop productivity has always been the major goal of plant breeders to meet the global demand for food. However, crop productivity itself is influenced in a large measure by a number of abiotic stresses including heat, which causes major losses in crop productivity. In cereals, crop productivity in terms of grain yield mainly depends upon the seed starch content so that starch biosynthesis and the enzymes involved in this process have been a major area of investigation for plant physiologists and plant breeders alike. Considerable work has been done on AGPase and its role in crop productivity, particularly under heat stress, because this enzyme is one of the major enzymes, which catalyses the rate-limiting first committed key enzymatic step of starch biosynthesis. Keeping the above in view, this review focuses on the basic features of AGPase including its structure, regulatory mechanisms involving allosteric regulators, its sub-cellular localization and its genetics. Major emphasis, however, has been laid on the genetics of AGPases and its manipulation for developing high yielding cultivars that will have comparable productivity under heat stress. Some important thermotolerant variants of AGPase, which mainly involve specific amino acid substitutions, have been highlighted, and the prospects of using these thermotolerant variants of AGPase in developing cultivars for heat prone areas have been discussed. The review also includes a brief account on transgenics for AGPase, which have been developed for basic studies and crop improvement.

Keywords

Heat Stress Large Subunit Starch Synthesis Disulphide Bridge Starch Biosynthesis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

National Academy of Science India (NASI) and Indian National Science Academy (INSA), New Delhi, India, awarded Senior Scientist Fellowships to PKG, during the tenures of which this review was written. SG is thankful to Department of Biotechnology, Government of India, New Delhi, for the award of a Senior Research Fellowship. Authors are also thankful to Professor L.C.Hannah, University of Florida, for his comments and suggestions which helped in improving the manuscript.

Conflict of interest

No conflict of interest declared.

References

  1. Ahmadi A, Baker DA (2001) The effect of water stress on the activities of key regulatory enzymes of the sucrose to starch pathway in wheat. Plant Growth Regul 35:81–91CrossRefGoogle Scholar
  2. Ahmed N, Maekawa M, Tetlow IJ (2008) Effects of low temperature on grain filling, amylose content, and activity of starch biosynthesis enzymes in endosperm of basmati rice. Aust J Agric Res 59:599–604CrossRefGoogle Scholar
  3. Ainsworth C, Tarvis M, Clark J (1993) Isolation and analysis of cDNA clone encoding small subunit of Adp-glucose pyrophosphorylase from wheat. Plant Mol Biol 23:23–33PubMedCrossRefGoogle Scholar
  4. Ainsworth C, Hosein F, Tarvis M, Weir F, Burrell MM, Devos KM, Gale MD (1995) Adenosine diphosphate glucose pyrophosphorylase genes in wheat: differential expression and gene mapping. Planta 197:1–10PubMedCrossRefGoogle Scholar
  5. 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
  6. Anderson JM, Hnllo J, Raymond L, Oklta TW, Morell M, Preiss J (1989) The encoded primary sequence of a rice seed ADP-glucose pyrophosphorylase subunit and its homology to the bacterial enzyme. J Biol Chem 264:12238–12242PubMedGoogle Scholar
  7. Bae JM, Giroux M, Hannah LC (1990) Cloning and characterization of the brittle-2 gene of maize. Maydica 35:317–322Google Scholar
  8. Ball S, Marianne T, Dirick L, Fresnoy M, Delrue B, Decq A (1991) A Chlamydomonas reinhardtii low-starch mutant is defective for 3-phosphoglycerate activation and orthophosphate inhibition of ADP-glucose pyrophosphorylase. Planta 185:17–26PubMedCrossRefGoogle Scholar
  9. 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 109:245–251PubMedCentralPubMedCrossRefGoogle Scholar
  10. Ballicora MA, Iglesias AA, Preiss J (2004) ADP-glucose pyrophosphorylase: a regulatory enzyme for plant starch synthesis. Photosynth Res 79:1–24PubMedCrossRefGoogle Scholar
  11. Bansal K, Munjal R, Madan S, Arora V (2012) Influence of high temperature stress on starch metabolism in two durum wheat varieties differing in heat tolerance. J Wheat Res 4(1):43–48Google Scholar
  12. Bao JS, Corke H, Sun M (2006) Microsatellites, single nucleotide polymorphisms and a sequence tagged site in starch-synthesizing genes in relation to starch physicochemical properties in non-waxy rice (Oryza sativa L.). Theor Appl Genet 113:1185–1196PubMedCrossRefGoogle Scholar
  13. Bao J, Lu Y, Yang F, Zhang G, Shao Y, Corke H, Sun M (2012) Nucleotide polymorphisms in OsAGP genes and their possible association with grain weight in rice. J Cereal Sci 55:312–317CrossRefGoogle Scholar
  14. Beckles DM, Craig J, Smith AM (2001a) ADP-glucose pyrophosphorylase is located in the plastid in developing tomato fruit. Plant Physiol 126(1):261–266PubMedCentralPubMedCrossRefGoogle Scholar
  15. Beckles DM, Smith AM, Rees T (2001b) A cytosolic ADP-glucose pyrophosphorylase is a feature of graminaceous endosperms, but not of other starch-storing organs. Plant Physiol 125(2):818–827PubMedCentralPubMedCrossRefGoogle Scholar
  16. Bhave MR, Lawrence S, Barton C, Hannah LC (1990) Identification and molecular characterization of shrunken-2 cDNA clones of maize. Plant Cell 2:581–588PubMedCentralPubMedCrossRefGoogle Scholar
  17. Boehlein SK, Shaw JR, Stewart JD, Hannah C (2008) Heat stability and allosteric properties of the maize endosperm ADP-glucose pyrophosphorylase are intimately intertwined. Plant Physiol 146:289–299PubMedCentralPubMedCrossRefGoogle Scholar
  18. Boehlein SK, Shaw JR, Stewart JD, Hannah CL (2010) Studies of the kinetic mechanism of maize endosperm Adp-glucose pyrophosphorylase uncovered complex regulatory properties. Plant Physiol 152:1056–1064PubMedCentralPubMedCrossRefGoogle Scholar
  19. Boehlein SK, Shaw JR, Georgelis N, Sullivan B, Hannah LC (2014) Enhancing the heat stability and kinetic parameters of the maize endosperm ADP-glucose pyrophosphorylase using iterative saturation mutagenesis. Arch Biochem Biophys 543:1–9PubMedCrossRefGoogle Scholar
  20. Boehlein SK, Shaw JR, Stewart JD, Sullivan B, Hannah LC (2015) Enhancing the heat stability and kinetic parameters of the maize endosperm ADP-glucose pyrophosphorylase using iterative saturation mutagenesis. Arch Biochem Biophys 568:28–37PubMedCrossRefGoogle Scholar
  21. Burger BT (2001) Thermotolerant variants of maize endosperm Adenosine diphosphate glucose pyrophosphorylase. A thesis submitted to graduate school of University of FloridaGoogle Scholar
  22. Burger BT, Cross JM, Shaw JR, Caren JR, Greene TW, Okita TW, Hannah LC (2003) Relative turnover numbers of maize endosperm and potato tuber ADP-glucose pyrophosphorylases in the absence and presence of 3-phosphoglyceric acid. Planta 217:449–456PubMedCrossRefGoogle Scholar
  23. 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 ADPglucose pyrophosphorylase in wheat endosperm. Plant Physiol 130:1464–1475PubMedCentralPubMedCrossRefGoogle Scholar
  24. Caley CY, Duffus CM, Jeffcoat B (1990) Effects of elevated temperature and reduced water uptake on enzymes of starch synthesis in developing wheat grains. Aust J Plant Physiol 17:431–439CrossRefGoogle Scholar
  25. Causse M, Santoni S, Damerwal C, Maurice A, Charcosset A, Deatric J, Vienne D (1996) A composite map of expressed sequences in maize. Genome 39(2):418–432PubMedCrossRefGoogle Scholar
  26. Chen X, Wang Z, Wang J, Wang M, Zhao L, Wang G (2007) Isolation and characterization of Brittle2 promoter from Zea mays and its comparison with Ze19 promoter in transgenic tobacco plants. Plant Cell Tiss Organ Cult 88(1):11–20CrossRefGoogle Scholar
  27. Cook FR (2011) Control of the size and composition of the embryo in cereals. A thesis submitted to University of East AngliaGoogle Scholar
  28. Corbi J, Debieu M, Rousselet A, Montalent P, Le Guilloux M, Manicacci D, Tenaillon MI (2011) Contrasted patterns of selection since maize domestication on duplicated genes encoding a starch pathway enzyme. Theor Appl Genet 122(4):705–722PubMedCrossRefGoogle Scholar
  29. Corbi J, Duthiel JY, Damerval C, Tennailon MI, Manicacci D (2012) Accelerated evolution and coevolution drove the evolutionary history of AGPase sub-units during angiosperm radiation. Ann Bot 1:6Google Scholar
  30. Cossegal M, Chambrier P, Mbelo S, Balzergue S, Martin-Magniette ML, Moing A, Deborde C, Guyon V, Perez P, Rogowsky P (2008) Transcriptional and metabolic adjustments in ADP-glucose pyrophosphorylase-deficient bt2 maize kernels. Plant Physiol 146:1553–1570PubMedCentralPubMedCrossRefGoogle Scholar
  31. Cross JM, Clancy M, Shaw JR, Greene TW, Schmidt RR, Okita TW, Hannah LC (2004) Both subunits of ADP-glucose pyrophosphorylase are regulatory. Plant Physiol 135:137–144PubMedCentralPubMedCrossRefGoogle Scholar
  32. Danishuddin M, Chatrath R, Singh R (2011) Insights of interaction between small and large subunits of ADP-glucose pyrophosphorylase from bread wheat (Triticum aestivum L.). Bioinformation 6(4):144–148PubMedCentralPubMedCrossRefGoogle Scholar
  33. Dawar C, Jain S, Kumar S (2013) Insight into the 3D structure of ADP-glucose pyrophosphorylase from rice (Oryza sativa L.). J Mol Model 19(8):3351–3367PubMedCrossRefGoogle Scholar
  34. Denyer K, Dunlap F, Thorbjornsen T, Keeling PL, Smith AM (1996) The major form of ADP-glucose pyrophosphorylase in maize endosperm is extra-plastidial. Plant Physiol 112:779–785PubMedCentralPubMedCrossRefGoogle Scholar
  35. Dickinson DB, Preiss J (1969) ADP glucose pyrophosphorylase from maize endosperm. Arch Biochem Biophys 130:119–128PubMedCrossRefGoogle Scholar
  36. Doan DNP, Rudy 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(3):965–975PubMedCentralPubMedCrossRefGoogle Scholar
  37. Duke ER, Doelhert DC (1996) Effects of heat stress on enzyme activities and transcript levels in developing maize kernels grown in culture. Environ Exp Bot 36:199–208CrossRefGoogle Scholar
  38. Eimert K, Luo C, Dejardin A, Villand P, Thorbjornsen T, Kleczkowski LA (1997) Molecular cloning and expression of the large subunit of ADP-glucose pyrophosphorylase from barley (Hordeum vulgare) leaves. Gene 189(1):79–82PubMedCrossRefGoogle Scholar
  39. Geigenberger P (2011) Regulation of starch biosynthesis in response to a fluctuating environment. Plant Physiol 155:1566–1577PubMedCentralPubMedCrossRefGoogle Scholar
  40. Geigenberger P, Geiger M, Stitt M (1998) High-temperature perturbation of starch synthesis is attributable to inhibition of ADP-glucose pyrophosphorylase by decreased levels of glycerate-3-phosphate in growing potato tubers. Plant Physiol 117:1307–1316PubMedCentralPubMedCrossRefGoogle Scholar
  41. 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
  42. Georgelis N, Hannah CL (2008) Isolation of a heat-stable maize endosperm Adp-glucose pyrophosphorylase variant. Plant Sci 175:247–254CrossRefGoogle Scholar
  43. Georgelis N, Braun EL, Shaw JR, Hannah CL (2007) The two AGPase subunits evolve at different rates in angiosperms, yet they are equally sensitive to activity-altering amino acid changes when expressed in bacteria. Plant Cell 19(5):1458–1472PubMedCentralPubMedCrossRefGoogle Scholar
  44. Georgelis N, Braun EL, Hannah CL (2008) Duplications and functional divergence of ADP-glucose pyrophosphorylase genes in plants. BMC Evol Biol 8:1–17CrossRefGoogle Scholar
  45. Georgelis N, Shaw JR, Hannah CL (2009a) Phylogenetic analysis of ADP-glucose pyrophosphorylase subunits reveals a role of subunit interfaces in the allosteric properties of the enzyme. Plant Physiol 151:67–77PubMedCentralPubMedCrossRefGoogle Scholar
  46. Georgelis N, Shaw JR, Hannah CL (2009b) Phylogenetic analysis of ADP-glucose pyrophosphorylase subunits reveals a role of subunit interfaces in the allosteric properties of the enzyme. Plant Physiol 151:67–77PubMedCentralPubMedCrossRefGoogle Scholar
  47. Ghosh HP, Preiss J (1966) Adenosine diphosphate glucose pyrophosphorylase: a regulatory enzyme in the biosynthesis of starch in spinach leaf chloroplasts. J Biol Chem 241:4491–4504PubMedGoogle Scholar
  48. Giroux MJ, Hannah LC (1994) ADP-glucose pyrophosphorylase in shrunken-2 and brittle-2 mutants of maize. Mol Gen Genet 243:400–408PubMedGoogle Scholar
  49. Giroux M, Smith-White B, Gilmore V, Hannah LC, Preiss J (1995) The large subunit of the embryo isoform of ADP glucose pyrophosphorylase from maize. Plant Physiol 108:1333–1334PubMedCentralPubMedCrossRefGoogle Scholar
  50. 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 93:5824–5829PubMedCentralPubMedCrossRefGoogle Scholar
  51. Goldman IL, Rocheford TR, Dudley JW (1993) Quantitative trait loci influencing protein and starch concentration in the Illinois long term selection maize strains. Theor Appl Genet 87:217–224PubMedCrossRefGoogle Scholar
  52. Gomez-Casati DF, Iglesias AA (2002) ADP-glucose pyrophosphorylase from wheat endosperm. Purification and characterization of an enzyme with novel regulatory properties. Planta 214:428–434PubMedCrossRefGoogle Scholar
  53. Greene TW, Hannah LC (1998a) Enhanced stability of maize endosperm ADP-glucose pyrophosphorylase is gained through mutants that alter subunit interactions. Proc Natl Acad Sci USA 95:13342–13347PubMedCentralPubMedCrossRefGoogle Scholar
  54. Greene TW, Hannah LC (1998b) Adenosine diphosphate glucose pyrophosphorylase, a rate limiting step in starch biosynthesis. Physiol Plant 103:574–580CrossRefGoogle Scholar
  55. 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 95:10322–10327PubMedCentralPubMedCrossRefGoogle Scholar
  56. Hadrich N, Hendriks JHM, Kotting O, Arrivault S, Feil R, Zeeman SC, Gibon Y, Schulze WX, Stitt M, Lunn JE (2012) Mutagenesis of cysteine 81 prevents dimerization of the APS1 subunit of Adp-glucose pyrophosphorylase and alters diurnal starch turnover in Arabidopsis thaliana leaves. Plant J 70:231–242PubMedCrossRefGoogle Scholar
  57. Hannah LC, Greene T (2009) The complexities of starch biosynthesis in cereal endosperms. In: AL Kriz, BA Larkins, eds, Molecular genetic approaches to maize improvement. Springer-Verlag, Berlin, pp 287–301Google Scholar
  58. 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 127:173–183PubMedCentralPubMedCrossRefGoogle Scholar
  59. Hannah CL, Futch B, Bing J, Shaw JR, Boehlein S, Stewart JD, Beiriger R, Georgelis N, Greene T (2012) A shrunken-2 transgene increases maize yield by acting in maternal tissues to increase the frequency of seed development. Plant Cell 24(6):2352–2363PubMedCentralPubMedCrossRefGoogle Scholar
  60. Hawker JS, Jenner CJ (1993) High temperature affects the activity of enzymes in the committed pathway of starch synthesis in developing wheat endosperm. Aust J Plant Physiol 20:197–209CrossRefGoogle Scholar
  61. Hendriks JHM, 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 133:838–849PubMedCentralPubMedCrossRefGoogle Scholar
  62. Huang B, Chen J, Zhang J, Liu H, Tian M, Gu Y, Hu Y, Li Y, Liu Y, Huang Y (2010) Characterization of ADP-glucose pyrophosphorylase encoding genes in source and sink organs of maize. Plant Mol Biol Rep 29:563–572CrossRefGoogle Scholar
  63. Huang B, Hennen-Bierwagen TA, Myers AM (2014) Functions of multiple genes encoding Adp-glucose pyrophosphorylase subunits in maize endosperm, embryo, and leaf. Plant Physiol 164:596–611PubMedCentralPubMedCrossRefGoogle Scholar
  64. Hurkman WJ, McCue KF, Altenbach SB, Korn A, Tanaka CK, Kotharia KM, Johnson EL, Bechtel DB, Wilson JD, Anderson OD, DuPont FM (2003) Effect of temperature on expression of genes encoding enzymes for starch biosynthesis in developing wheat endosperm. Plant Sci 164:873–881CrossRefGoogle Scholar
  65. HyltonC Smith AM (1992) The rb mutation of peas causes structural and regulatory changes in ADP-glucose pyrophosphorylase from developing embryos. Plant Physiol 99:1626–1634CrossRefGoogle Scholar
  66. Iglesias AA, Barry GF, Meyer C, Bloksberg L, Nakata PA, Greene T, Laughlin MJ, Okita TW, Kishore GM, Preiss J (1993) Expression of the potato tuber ADP-glucose pyrophosphorylase in Escherichia coli. J Biol Chem 268:1081–1086PubMedGoogle Scholar
  67. Jin X, Ballicora MA, Preiss J, Geiger JH (2005) Crystal structure of potato tuber ADP-Glc pyrophosphorylase. EMBO J 24:694–704PubMedCentralPubMedCrossRefGoogle Scholar
  68. Johnson PE, Patron NJ, Bottrill AR, Dinges JR, Fahy BF, Parker ML, Waite DN, Denyer K (2003) A low-starch barley mutant, risø 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(2):684–696PubMedCentralPubMedCrossRefGoogle Scholar
  69. Kaneko T, Zhang W, Takahashi H, Ito K, Takedo K (2001) QTL mapping for enzyme assay and thermostability of B-amylase in barley (Hordeum vulgare). Breed Sci 51:99–105CrossRefGoogle Scholar
  70. Kang GZ, Wang YH, Liu C, Shen BQ, Zheng BB, Feng W, Guo TC (2010) Difference in AGPase subunits could be associated with starch accumulation in grains between two wheat cultivars. Plant Growth Regul 61:61–66CrossRefGoogle Scholar
  71. Kang G, Liu G, Peng X, Wei L, Wang C, Zhu Y, Ying M, Yumei J, Tiancai G (2013) Increasing the starch content and grain weight of common wheat by overexpression of the cytosolic AGPase large subunit gene. Plant Physiol Biochem 73:93–98PubMedCrossRefGoogle Scholar
  72. Kato T, Taniguchi A, Horibata A (2010) Effects of the alleles at OsAGPS2 and OsSUT1 on the grain filling in extra-heavy panicle type of rice. Crop Sci 50:2448–2456CrossRefGoogle Scholar
  73. Keeling PL, Bacon PJ, Holt DC (1993) Elevated temperature reduces starch deposition in wheat endosperm by reducing the activity of soluble starch synthase. Planta 191:342–348CrossRefGoogle Scholar
  74. Kim D, Hwang SK, Okita TW (2007) Subunit interactions specify the allosteric regulatory properties of the potato tuber ADP-glucose pyrophosphorylase. Biochem Biophys Res Commun 362:301–306PubMedCrossRefGoogle Scholar
  75. Koehler P, Weiser H (2013) Chapter 2: Chemistry of cereal grains. In: M. Gobbetti and M. Ganzle (eds.), Handbook on Sourdough Biotechnology, Springer Science + Business Media, New York, pp 11–45Google Scholar
  76. 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 102:11118–11123PubMedCentralPubMedCrossRefGoogle Scholar
  77. Kossmann J, Lloyd J (2000) Understanding and influencing starch biochemistry. Crit Rev Biochem Mol Biol 35:141–196PubMedGoogle Scholar
  78. La Cognata U, Willmitzer L, Muller-Rober B (1995) Molecular cloning and characterization of novel isoforms of potato ADP-glucose pyrophosphorylase. Mol Gen Genet 246:538–548PubMedCrossRefGoogle Scholar
  79. Lee SK, Hwang SK, Han M, Eom JS, Kang HG, Han Y, Choi SB, Cho MH, Bhoo SH, An G, Hahn TR, Okita TW, Jeon JS (2007) Identification of the ADP-glucose pyrophosphorylase isoforms essential for starch synthesis in the leaf and seed endosperm of rice (Oryza sativa L.). Plant Mol Biol 65:531–546PubMedCrossRefGoogle Scholar
  80. Li HM, Sullivan TD, Keegstra K (1992) Information for targeting to the chloroplastic inner envelope membrane is contained in the mature region of the maize Bt1-encoded protein. J Biol Chem 267:18999–19004PubMedGoogle Scholar
  81. Li N, Zhang S, Zhao Y, Li B, Zhang J (2011) Over-expression of AGPase genes enhances seed weight and starch content in transgenic maize. Planta 233:241–250PubMedCrossRefGoogle Scholar
  82. Lin TP, Caspar T, Somerville CR, Preiss J (1988) A starch deficient mutant of Arabidopsis thaliana with low ADPglucose pyrophosphorylase activity lacks one of the two subunits of the enzyme. Plant Physiol 88:1175–1181PubMedCentralPubMedCrossRefGoogle Scholar
  83. Linebarger CR, Boehlein SK, Sewell AK, Shaw J, Hannah LC (2005) Heat stability of maize endosperm ADP-glucose pyrophosphorylase is enhanced by insertion of a cysteine in the N terminus of the small subunit. Plant Physiol 139(4):1625–1634PubMedCrossRefGoogle Scholar
  84. Lohot VD, Sharma-Natu P, Pandey R, Ghildiyal MC (2010) ADP-glucose pyrophosphorylase activity in relation to starch accumulation and grain growth in wheat cultivars. Curr Sci 98(3):426–430Google Scholar
  85. Lu Fh, Park YJ (2012) Sequence variations in OsAGPase significantly associated with amylase content and viscosity properties in rice. Genet Res 94(4):179–189CrossRefGoogle Scholar
  86. Lunn JE, Feil R, Hendriks JHM, Gibon Y, Morcuende R, Osuna D, Scheible WR, Carillo P, Hajirezaei MR, Stitt M (2006) Sugar-induced increases in trehalose 6-phosphate are correlated with redox activation of ADPglucose pyrophosphorylase and higher rates of starch synthesis in Arabidopsis thaliana. Biochem J 397(1):139–148PubMedCentralPubMedCrossRefGoogle Scholar
  87. Maniacci D, Falque M, Le Guillou S, Piegu B, Henry AM, Le Guilloux M, Damerval C, De Vienne D (2007) Maize Sh2 gene is constrained by natural selection but escaped domestication. J Evol Biol 20:503–516CrossRefGoogle Scholar
  88. Meyer FD, Smidansky ED, Beecher B, Greene TW, Giroux MJ (2004) The maize Sh2r6hs ADP-glucose pyrophosphorylase (AGP) large subunit confers enhanced AGP properties in transgenic wheat (Triticum aestivum). Plant Sci 167(4):899–911CrossRefGoogle Scholar
  89. Meyer RC, Steinfath M, Lisec J, Becher M, Witucka Wall H, Torjek O, Fiehn O, Eckardt A, Willmitzer L, Selbig J, Altmann T (2007) The metabolic signature related to high plant growth rate in Arabidopsis thaliana. Proc Natl Acad Sci USA 104:4759–4764PubMedCentralPubMedCrossRefGoogle Scholar
  90. Morell M, Bloom M, Preiss J (1988) Affinity labeling of the allosteric activator sites of spinach leaf. J Biol Chem 263:633–637PubMedGoogle Scholar
  91. Moss SC, Denyer K (2009) The evolution of the starch biosynthetic pathway in cereals and other grasses. J Exp Bot 60(9):2481–2492CrossRefGoogle Scholar
  92. Muller-Rober B, Sonnewald U, Willmitzer L (1992) Inhibition of the ADP-glucose pyrophosphorylase in transgenic potatoes leads to sugar-storing tubers and influences tuber formation and expression of tuber storage protein genes. The EMBO Journal 11(4):1229–1238PubMedCentralPubMedGoogle Scholar
  93. Nakamura Y, Kawaguchi K (1992) Multiple forms of ADP glucose pyrophosphorylase of rice endosperm. Physiol Plant 84:336–342CrossRefGoogle Scholar
  94. Obana Y, Omoto D, Kato C, Matsumoto K, Nagai Y, Kavakli IH, Hamada S, Edwards GE, Okita TW, Matsui H, Ito H (2006) Enhanced turnover of transitory starch by expression of up-regulated ADP-glucose pyrophosphorylases in Arabidopsis thaliana. Plant Sci 170:1–11CrossRefGoogle Scholar
  95. 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(422):3229–3244PubMedCrossRefGoogle Scholar
  96. Okita T, Nakata P, Anderson J, Sowokinos J, Morell M, Preiss J (1990) The subunit structure of potato tuber ADP-glucose pyrophosphorylase. Plant Physiol 93:785–790PubMedCentralPubMedCrossRefGoogle Scholar
  97. Patron NJ, Keeling PJ (2005) Common evolutionary origin of starch biosynthetic enzymes in green and red algae. J Phycol 41:1131–1141CrossRefGoogle Scholar
  98. 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 135:2088–2097PubMedCentralPubMedCrossRefGoogle Scholar
  99. Plaxton WC, Preiss J (1987) Purification and properties of non-proteolytic degraded ADP-glucose pyrophosphorylase from maize endosperm. Plant Physiol 83:105–112PubMedCentralPubMedCrossRefGoogle Scholar
  100. Preiss J (1991) Biology and molecular biology of starch synthesis and its regulation. In: Miflin BJ (ed) Oxford surveys of cellular and molecular biology, vol 7. Oxford University Press, Oxford, pp 59–114Google Scholar
  101. Preiss J (2004) Plant starch synthesis. In: Eliasson AC (ed) Starch in food :Structire, function and applications. CRC Press, USA, pp 3–56CrossRefGoogle Scholar
  102. Preiss J, Danner S, Summers PS, Morell M, Barton CR, Yang L, Nieder M (1990) Molecular characterization of the brittle-2 gene effect on maize endosperm ADP-glucose pyrophosphorylase subunits. Plant Physiol 92:881–885PubMedCentralPubMedCrossRefGoogle Scholar
  103. Prioul JL, Jeannette E, Reyss A, Gregory N, Giroux M, Hannah LC, Causse M (1994) Expression of ADP-glucose pyrophosphorylase in maize (Zea mays L.) grain and source leaf during grain filling. Plant Physiol 104:179–187PubMedCentralPubMedCrossRefGoogle Scholar
  104. Prioul JL, Pelleschi S, Sene M, Thevenot C, Causse M, de Vienne D, Leonardi A (1999) From QTLs for enzyme activity to candidate genes in maize. J Exp Bot 50:1281–1288CrossRefGoogle Scholar
  105. Rosti S, Denyer K (2007) Two paralogous genes encoding small subunits of ADP-glucose pyrophosphorylase in maize, Bt2 and L2, replace the single alternatively spliced gene found in other cereal species. J Mol Evol 65:316–327PubMedCrossRefGoogle Scholar
  106. Rosti S, Rudi H, Rudi K, Opsahl-Sortberg 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
  107. Rosti S, Fahy B, Denyer K (2007) A mutant of rice lacking the leaf large subunit of ADP-glucose pyrophosphorylase has drastically reduced leaf starch content but grows normally. Funct Plant Biol 34:480–489CrossRefGoogle Scholar
  108. Sakulsingharoj C, Choi SB, Hwang SK, Edwards GE, Bork J, Meyer CR, Preiss J, Okita TW (2004) Engineering starch biosynthesis for increasing rice seed weight: the role of the cytoplasmic ADP glucose pyrophosphorylase. Plant Sci 167:1323–1333CrossRefGoogle Scholar
  109. Salamone PR, Kavakli IH, Slattery CJ, Okita TW (2002) Directed molecular evolution of ADP-glucose pyrophosphorylase. Proc Natl Acad Sci USA 99:1070–1075PubMedCentralPubMedCrossRefGoogle Scholar
  110. Schlossar AJ, Martin JM, Beecher BS, Giroux MJ (2014) Enhanced rice growth is conferred by increased leaf Adp-glucose pyrophosphorylase activity. J Plant Physiol Pathol 2(4):2. doi: 10.4172/2329-955X.1000136 Google Scholar
  111. Sene M, Causse M, Damerval C, Thevenot C, Prioul J (2000) Quantitative trait loci affecting amylase, amylopectin and starch content in maize recombinant inbred lines. Plant Physiol Biochem 38(6):459–472CrossRefGoogle Scholar
  112. 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(4):1235–1252PubMedCentralPubMedCrossRefGoogle Scholar
  113. Shaw JR, Hannah LC (1992) Genomic nucleotide sequence of a wild-type shrunken-2 allele of Zea mays. Plant Physiol 98:1214–1216PubMedCentralPubMedCrossRefGoogle Scholar
  114. Sikka VK, Choi S, Kavakli IH, Sakulsingharoj C, Gupta S, Ito H, Okita TW (2001) Subcellular compartmentation and allosteric regulation of the rice endosperm ADP glucose pyrophosphorylase. Plant Sci 161:461–468CrossRefGoogle Scholar
  115. Singletary GW, Banisadr R, Keeling PL (1994) Heat stress during grain filling in maize: effects on carbohydrate storage and metabolism. Aust J Plant Physiol 21:829–841CrossRefGoogle Scholar
  116. Slewinski TL, Ma Y, Baker RF, Huang M, Meeley R, Braun DM (2008) Determining the role of Tie-dyed1 in starch metabolism: epistasis analysis with a maize ADP-glucose pyrophosphorylase mutant lacking leaf starch. J Hered 99:661–666PubMedCrossRefGoogle Scholar
  117. 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 99:1724–1729PubMedCentralPubMedCrossRefGoogle Scholar
  118. 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
  119. Smidansky ED, Meyer FD, Blakeslee B, Weglarz TE, Greene TW, Giroux MJ (2007) Expression of a modified ADP-glucose pyrophosphorylase large subunit in wheat seeds stimulates photosynthesis and carbon metabolism. Planta 225(4):965–976PubMedCrossRefGoogle Scholar
  120. Smith AM, Denyer K, Martin CR (1995) What controls the amount and structure of starch in storage organs? Plant Physiol 107:673–677PubMedCentralPubMedGoogle Scholar
  121. Smith-White BJ, Preiss J (1992) Comparison of proteins of ADP-glucose pyrophosphorylase from diverse sources. J Mol Evol 34:449–464PubMedCrossRefGoogle Scholar
  122. Stark DM, Timmerman 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
  123. Teas HJ, Teas AN (1953) Heritable characters in maize. Description and linkage of brittle endosperm-2. J Hered 44:156–158Google Scholar
  124. Tester RF, Morrison WR, Schulman AH (1993) Swelling and gelatinization of cereal starches: V. Risø mutants of Bomi and Carlsberg II barley cultivars. J Cereal Sci 17:1–9CrossRefGoogle Scholar
  125. Tetlow IJ, Davies EJ, Vardy KA, Bowsher CG, Burrell MM, Emes MJ (2003) Subcellular localization of ADPglucose pyrophosphorylase in developing wheat endosperm and analysis of theproperties of a plastidial isoform. J Exp Bot 54(383):715–725PubMedCrossRefGoogle Scholar
  126. Thevenot C, Simond-Cote E, Reyss A, Manicacci D, Trouverie J, Guilloux ML, Ginhoux V, Sidicina F, Priou L (2005) QTLs for enzyme activities and soluble carbohydrates involved in starch accumulation during grain filling in maize. J Exp Bot 56(413):945–958PubMedCrossRefGoogle Scholar
  127. Thitisaksakul M, Jimenez RC, Arias MC, Beckles DM (2012) Effects of environmental factors on cereal starch biosynthesis and composition. J Cereal Sci 56:67–80CrossRefGoogle Scholar
  128. Thorbjornsen T, Villand P, Kleczkowski LA, Olsen OA (1996a) A single gene encodes two different transcripts for the ADP-glucose pyrophosphorylase small subunit from barley (Hordeum vulgare). Biochem J 313(1):149–154PubMedCentralPubMedCrossRefGoogle Scholar
  129. Thorbjornsen T, Villand P, Denyer K, Olsen OA, Smith A (1996b) Distinct isoforms of ADP glucose pyrophosphorylase occur inside and outside the amyloplasts in barley endosperm. Plant J 10:243–250CrossRefGoogle Scholar
  130. Thorneycroft D, Hosein F, Thangavelu M, Clark J, Vizir L, Burrell M, Ainsworth C (2003) Characterization of a gene from chromosome 1B encoding the large subunit of ADP glucose pyrophosphorylase from wheat: evolutionary divergence and differential expression of Agp2 genes between leaves and developing endosperm. Plant Biotech J 1:259–270CrossRefGoogle Scholar
  131. Tiana Z, Qianb Q, Liuc Q, Yanb M, Liua X, Yanc C, Liua G, Gaob Z, Tangc S, Zengb D, Wanga Y, Yud J, Guc M, Lia J (2009) Allelic diversities in rice starch biosynthesis lead to a diverse array of rice eating and cooking qualities. Pros Natl Acad Sci USA 106(51):21760–21765CrossRefGoogle Scholar
  132. Tiessen A, Hendriks JHM, 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 14:2191–2213PubMedCentralPubMedCrossRefGoogle Scholar
  133. Tsai CY, Nelson OE (1966) Starch-deficient maize mutants lacking adenosine diphosphate glucose pyrophosphorylase activity. Science 151:341–343PubMedCrossRefGoogle Scholar
  134. Tuncel A, Okita TW (2013) Improving starch yield in cereals by over-expression of ADP glucose pyrophosphorylase: expectations and unanticipated outcomes. Plant Sci 211:52–60PubMedCrossRefGoogle Scholar
  135. Tuncel A, Kavakli IH, Keskin O (2008) Insights into subunit interactions in the heterotetrameric structure of potato ADP glucose pyrophosphorylase. Biophys J 95:3628–3639PubMedCentralPubMedCrossRefGoogle Scholar
  136. Tuncel A, Kawaguchi J, Ihara Y, Matsusaka H, Nishi A, Nakamura T, Kuhara S, Hirakawa H, Nakamura Y, Cakir B, Nagamine A, Okita TW, Hwang SK, Satoh H (2014) The rice endosperm ADP-glucose pyrophosphorylase large subunit is essential for optimal catalysis and allosteric regulation of the heterotetrameric enzyme. Plant Cell Physiol 55(6):1169–1183PubMedCrossRefGoogle Scholar
  137. Umemoto T, Horibata T, Aoki N, Hiratsuka M, Yano M, Inouchi N (2008) Effects of variation in starch synthase on starch properties and eating quality of rice. Plant Prod Sci 11(4):472–480CrossRefGoogle Scholar
  138. Villand P, Kleczkowski LA (1994) Is there an alternative pathway for starch biosynthesis in cereal seeds? Zeitschrift für Naturforschung C 49:215–219Google Scholar
  139. Villand P, Aalen R, Olsen O-A, Lüthi E, Lonneborg A, Kleckowski LA (1992) PCR amplification and sequences of cDNA clones for the small and LS of ADP-glucose pyrophosphorylase from barley tissues. Plant Mol Biol 19:381–389PubMedCrossRefGoogle Scholar
  140. Viswanathan C, Khanna-Chopra R (2001) Effect of heat stress on grain growth, starch synthesis and protein synthesis in grains of wheat (Triticum aestivum L.) varieties differing in grain weight stability. J Agron Crop Sci 186:1–7CrossRefGoogle Scholar
  141. Wang Z, Chen X, Wang J, Liu T, Liu Y, Zhao L, Wang G (2007) Increasing maize seed weight by enhancing the cytoplasmic ADP-glucose pyrophosphorylase activity in transgenic plants. Plant Cell Tiss Organ Cult 88:83–92CrossRefGoogle Scholar
  142. Weber H, Heim U, Borisjuk L, Wobus U (1995) Cell-type specific, coordinate expression of two ADPglucose pyrophosphorylase genes in relation to starch biosynthesis during seed development in Vicia faba L. Planta 195:352–361PubMedCrossRefGoogle Scholar
  143. Wilhelm EP, Mullen RE, Keeling PL, Singletary GW (1999) Heat stress during grain filling in maize: effects on kernel growth and metabolism. Crop Sci 39:1733–1741CrossRefGoogle Scholar
  144. Yan HB, Pan XX, Jiang HW, Wu GJ (2009) Comparison of the starch synthesis genes between maize and rice: copies, chromosome location and expression divergence. Theor Appl Genet 119:815–825PubMedCrossRefGoogle Scholar
  145. Yu G, Olsen KM, Schaal BA (2011) Molecular evolution of the endosperm starch synthesis pathway genes in rice (Oryza sativa L.) and its wild ancestor, O. rufipogon L. Mol Biol Evol 28(1):659–671PubMedCrossRefGoogle Scholar
  146. Zhang N, Gibon Y, Gur A, Chen C, Lepak N, Hohne M, Zhang Z, Kroon D, Tschoep H, Stitt M, Edward B (2010) Fine quantitative trait loci mapping of carbon and nitrogen metabolism enzyme activities and seedling biomass in the maize IBM mapping population. Plant Physiol 154(1753):1765Google Scholar

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© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Molecular Biology Laboratory, Department of Genetics and Plant BreedingCh.Charan Singh UniversityMeerutIndia

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