Barley grains, deficient in cytosolic small subunit of ADP-glucose pyrophosphorylase, reveal coordinate adjustment of C:N metabolism mediated by an overlapping metabolic-hormonal control

Plant Journal

Volumn 69, Issue 6, 2012, Pages 1077-1093

  Faix, Benjamin ^a   Radchuk, Volodymyr ^b   Nerlich, Annika ^c   Hümmer, Christine ^a   Radchuk, Ruslana ^b   Emery, R J Neil ^d   Keller, Harald ^e   Götz, Klaus Peter ^e   Weschke, Winfriede ^b   Geigenberger, Peter ^a   Weber, Hans ^b  

^a UNIVERSITY OF MUNICH   (Germany)

^b LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^c MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^d TRENT UNIVERSITY   (Canada)

^e HUMBOLDT UNIVERSITY   (Germany)

Author keywords

ADP glucose pyrophosphorylase; endosperm development; metabolic regulation; starch; storage proteins

Indexed keywords

ABSCISIC ACID; ADP-GLC; ADP-GLC PYROPHOSPHORYLASE; ADPGLUCOSE PYROPHOSPHORYLASE; CARBON FLUXES; CO-REGULATION; CYTOKININ BIOSYNTHESIS; CYTOSOLIC; DOWN-REGULATION; ENDOSPERM DEVELOPMENT; GLYCOLYTIC ENZYME; GLYCOLYTIC INTERMEDIATE; HORMONAL REGULATION; ISOCITRATE DEHYDROGENASE; METABOLIC REGULATIONS; NICOTINAMIDE ADENINE DINUCLEOTIDES; SEED SIZE; SMALL SUBUNITS; STARCH SYNTHESIS; STORAGE METABOLISM; STORAGE PROTEINS; TRANSCRIPT PROFILING; TRANSCRIPTIONAL LEVELS; TRICARBOXYLIC ACID CYCLE; WILD TYPES;

AMIDES; AMINO ACIDS; BIOCHEMISTRY; BIOSYNTHESIS; GENES; GLUCOSE; GRAIN (AGRICULTURAL PRODUCT); METABOLITES; PHYSIOLOGY; PLANTS (BOTANY); PROTEINS; STARCH; TRANSCRIPTION;

METABOLISM;

ABSCISIC ACID; AMINO ACID; AMYLASE; CARBON; CYTOKININ; GLUCOSE 1 PHOSPHATE ADENYLYLTRANSFERASE; ISOCITRATE DEHYDROGENASE; NITROGEN; PHYTOHORMONE; SEED STORAGE PROTEIN; STARCH; VEGETABLE PROTEIN;

ARTICLE; BIOSYNTHESIS; CITRIC ACID CYCLE; CYTOSOL; ENDOSPERM; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GLYCOLYSIS; HORDEUM; METABOLISM; MITOCHONDRION; MUTATION; PHYSIOLOGY; PROMOTER REGION;

ABSCISIC ACID; AMINO ACIDS; AMYLASES; CARBON; CITRIC ACID CYCLE; CYTOKININS; CYTOSOL; ENDOSPERM; GENE EXPRESSION REGULATION, PLANT; GLUCOSE-1-PHOSPHATE ADENYLYLTRANSFERASE; GLYCOLYSIS; HORDEUM; ISOCITRATE DEHYDROGENASE; MITOCHONDRIA; MUTATION; NITROGEN; PLANT GROWTH REGULATORS; PLANT PROTEINS; PROMOTER REGIONS, GENETIC; SEED STORAGE PROTEINS; STARCH;

HORDEUM;

EID: 84857456239     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2011.04857.x     Document Type: Article

References (75)

1. Beckles, D.M., Smith, A.M., and, ap Rees, T.A., (2001) Cytosolic ADP-glucose pyrophosphorylase is a feature of graminaceous endosperms, but not of other starch-storing organs. Plant Physiol. 125, 818-827.
2. Bruce, S.A., Saville, B.J., and, Emery, R.J.N., (2011) Ustilago maydis produces cytokinins and abscisic acid for potential regulation of tumor formation in maize. Journal of Plant Growth Regulation. 30, 51-63.
3. Budde, R.J., and, Randall, D.D., (1987) Regulation of pea mitochondrial pyruvate dehydrogenase complex activity: inhibition of ATP-dependent inactivation. Arch. Biochem. Biophys. 258, 600-606.
4. Casey, R., Domoney, C., Forster, C., Hedley, C., Hitchin, E., and, Wang, T., (1998) The effect of modifying carbohydrate metabolism on seed protein gene expression in peas. J. Plant Physiol. 152, 636-640.
5. Close, T.J., Wanamaker, S.I., Caldo, R.A., Turner, S.M., Ashlock, D.A., Dickerson, J.A., Wing, R.A., Muehlbauer, G.J., Kleinhofs, A., and, Wise, R.P., (2004) A new resource for cereal genomics: 22K barley GeneChip comes of age. Plant Physiol. 134, 960-968.
6. Cossegal, M., Chambrier, P., Mbelo, S., Balzergue, S., Martin-Magniette, M.L., Moing, A., Deborde, C., Guyon, V., Perez, P., and, Rogowsky, P., (2008) Transcriptional and metabolic adjustments in ADP-glucose pyrophosphorylase- deficient bt2 maize kernels. Plant Physiol. 146, 1553-1570.
7. Cox, G.F., and, Davies, D.D., (1967) Nicotinamide-adenine dinucleotide-specific isocitrate dehydrogenase from pea mitochondria. Biochem. J. 105, 729-734.
8. Dickinson, D.B., and, Preiss, J., (1969) Presence of ADP-glucose pyrophosphorylase in shrunken-2 and brittle-2 mutants of maize endosperm. Plant Physiol. 44, 1058-1062.
9. Doehlert, D.C., and, Kuo, T.M., (1994) Gene expression in developing kernels of some endosperm mutants. Plant Cell Physiol. 35, 411-418.
10. Emery, R.J.N., Leport, L., Barton, J.E., Turner, N.C., and, Atkins, C.A., (1998) cis-Isomers of cytokinins predominate in chickpea seeds throughout their development. Plant Physiol. 117, 151-1523.
11. Ezcurra, I., Ellerstrom, M., Wycliffe, P., Stalberg, K., and, Rask, L., (1999) Interaction between composite elements in the napA promoter: both the B-box ABA-responsive complex and the RY/G complex are necessary for seed-specific expression. Plant Mol. Biol. 40, 699-709.
12. Fait, A., Fromm, H., Walter, D., Galili, G., and, Fernie, A.R., (2008) Highway or byway: the metabolic role of the GABA shunt in plants. Trends Plant Sci. 13, 14-19.
13. Fernie, A.R., Tiessen, A., Stitt, M., Willmitzer, L., and, Geigenberger, P., (2002) Altered metabolic fluxes result from shifts in metabolite levels in sucrose phosphorylase expressing potato tubers. Plant Cell Environ. 25, 1219-1232.
14. Finkelstein, R.R., Gampala, S.S., and, Rock, C.D., (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell, 14 (Suppl), S15-S45.
15. Gálvez, S., Hodges, M., Decottignies, P., Bismuth, E., Lancien, M., Sangwan, R.S., Dubois, F., LeMaréchal, P., Crétin, C., and, Gadal, P., (1996) Identification of a tobacco cDNA encoding a cytosolic NADP-isocitrate dehydrogenase. Plant Mol. Biol. 30, 307-320.
16. Geigenberger, P., (2011) Regulation of starch biosynthesis in response to a fluctuating environment. Plant Physiol. 155, 1566-1577.
17. Geigenberger, P., Lerchl, J., Stitt, M., and, Sonnewald, U., (1996) Phloem-specific expression of pyrophosphatase inhibits long distance transport of carbohydrates and amino acids in tobacco plants. Plant Cell Environ. 19, 43-55.
18. Geigenberger, P., Reimholz, R., Geiger, M., Merlo, L., Canale, V., and, Stitt, M., (1997) Regulation of sucrose and starch metabolism in potato tubers in response to short-term water deficit. Planta, 201, 502-518.
19. Heinonen, J.K., and, Lahti, R.J., (1981) A new and convenient colorimetric determination of inorganic pyrophosphate and its application to the assay of inorganic pyrophosphatase. Anal. Biochem. 113, 313-317.
20. Higo, K., Ugawa, Y., Iwamoto, M., and, Korenaga, T., (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res. 27, 297-300.
21. Hodges, M., (2002) Enzyme redundancy and the importance of 2-oxoglutarate in plant ammonium assimilation. J. Exp. Bot. 53, 905-916.
22. 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, 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, 684-696.
23. Koch, K.E., (1996) Carbohydrate-modulated gene expression in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 509-540.
24. Kolbe, A., Tiessen, A., Schluepmann, H., Paul, M., Ulrich, S., and, Geigenberger, P., (2005) Trehalose-6-phosphate regulates starch synthesis via post-translational redox-activation of ADP-glucose pyrophosphorylase. Proc. Natl. Acad. Sci. USA, 102, 11118-11123.
25. Lancien, M., Gadal, P., and, Hodges, M., (1998) Molecular characterization of higher plant NAD-dependent isocitrate dehydrogenase: evidence for a heteromeric structure by the complementation of yeast mutants. Plant J. 16, 325-333.
26. Lemaitre, T., and, Hodges, M., (2006) Expression analysis of Arabidopsis thaliana NAD-dependent isocitrate dehydrogenase genes shows the presence of a functional subunit that is mainly expressed in the pollen and absent from vegetative organs. Plant Cell Physiol. 47, 634-643.
27. Lu, C.A., Lim, E.K., and, Yu, S.M., (1998) Sugar response sequence in the promoter of a rice alpha-amylase gene serves as a transcriptional enhancer. J. Biol. Chem. 273, 10120-10131.
28. Merlo, L., Geigenberger, P., Hajirezaei, M., and, Stitt, M., (1993) Changes of carbohydrates, metabolites and enzyme activities in potato tubers during development, and within a single tuber along a stolon-apex gradient. J. Plant Physiol. 142, 392-402.
29. Miyazawa, Y., Kato, H., Muranaka, T., and, Yoshida, S., (2002) Amyloplast formation in cultured tobacco BY-2 cells requires a high cytokinin content. Plant Cell Physiol. 43, 1534-1541.
30. Morita, A., Umemura, T., Kuroyanagi, M., Futsuhara, Y., Perata, P., and, Yamaguchi, J., (1998) Functional dissection of a sugar-repressed amylase gene (RAmy1A) promoter in rice embryos. FEBS Lett. 423, 81-85.
31. Müller-Röber, B., Sonnewald, U., and, 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. EMBO J. 11, 1229-1238.
32. Neuhaus, H.E., and, Emes, M.J., (2000) Nonphotosynthetic metabolism in plastids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 111-140.
33. Nunes-Nesi, A., Carrari, F., Gibon, Y., Sulpice, R., Lytovchenko, A., Fisahn, J., Graham, J., Ratcliffe, R.G., Sweetlove, L.J., and, Fernie, A.R., (2007) Deficiency of mitochondrial fumarase activity in tomato plants impairs photosynthesis via an effect on stomatal function. Plant J. 50, 1093-1106.
34. Osuna, D., Usadel, B., Morcuende, R., et al. (2007) Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings. Plant J. 49, 463-491.
35. Perata, P., Matsukura, C., Vernieri, P., and, Yamaguchi, J., (1997) Sugar repression of a gibberellin-dependent signalling pathway in barley embryos. Plant Cell, 9, 2197-2208.
36. Perez, M.D., Chambers, S.J., Bacon, J.R., Lambert, N., Hedley, C.L., and, Wang, T., (1993) Seed protein content and composition of near-isogenic and induced mutant pea lines. Seed Sci. Res. 3, 187-194.
37. Podestá, F.E., and, Plaxton, W.C., (1992) Plant cytosolic pyruvate kinase: a kinetic study. Biochim. Biophys. Acta, 1160, 213-220.
38. Preiss, J., Ball, K., Smith-White, B., Iglesias, A., Kakefuda, G., and, Li, L., (1991) Starch biosynthesis and its regulation. Biochem. Soc. Trans. 19, 539-547.
39. Price, J., Laxmi, A., St Martin, S.K., and, Jang, J.C., (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell, 16, 2128-2150.
40. Quesnelle, P.E., and, Emery, R.J.N., (2007) cis-Cytokinins that predominate in Pisum sativum during early embryogenesis will accelerate embryo growth in vitro. Can. J. Bot. 85, 91-103.
41. Radchuk, R., Radchuk, V., Weschke, W., Borisjuk, L., and, Weber, H., (2006) Repressing the expression of the sucrose nonfermenting- 1-related protein kinase gene in pea embryo causes pleiotropic defects of maturation similar to an abscisic acid-insensitive phenotype. Plant Physiol. 140, 263-278.
42. Radchuk, R., Radchuk, V., Götz, K.P., Weichert, H., Richter, A., Emery, R.J., Weschke, W., and, Weber, H., (2007) Ectopic expression of phosphoenolpyruvate carboxylase in Vicia narbonensis seeds: effects of improved nutrient status on seed maturation and transcriptional regulatory networks. Plant J. 51, 819-839.
43. Radchuk, R., Emery, R.J.N., Weier, D., Vigeolas, H., Geigenberger, P., Lunn, J.E., Feil, R., Weschke, W., and, Weber, H., (2010a) Sucrose non-fermenting kinase 1 (SnRK1) coordinates metabolic and hormonal signals during pea cotyledon growth and differentiation. Plant J. 61, 324-338.
44. Radchuk, R., Conrad, U., Saalbach, I., Giersberg, M., Emery, R.J., Küster, H., Nunes-Nesi, A., Fernie, A.R., Weschke, W., and, Weber, H., (2010b) Abscisic acid deficiency of developing pea embryos achieved by immunomodulation attenuates developmental phase transition and storage metabolism. Plant J. 64, 715-730.
45. Regierer, B., Fernie, A.R., Springer, F., Perez-Melis, A., Leisse, A., Koehl, K., Willmitzer, L., Geigenberger, P., and, Kossmann, J., (2002) Starch content and yield increase as a result of altering adenylate pools in transgenic plants. Nat. Biotechnol. 20, 1256-1260.
46. Rijavec, T., Kovac, M., Kladnik, A., Chourey, P.S., and, Dermastia, M., (2009) A comparative study on the role of cytokinins in caryopsis development in the maize miniature1 seed mutant and its wild type. J. Integr. Plant Biol. 51, 840-849.
47. Roessner-Tunali, U., Urbanczyk-Wochniak, E., Czechowski, T., Kolbe, A., Willmitzer, L., and, Fernie, A.R., (2003) De novo amino acid biosynthesis in potato tubers is regulated by sucrose levels. Plant Physiol. 133, 683-692.
48. Rolletschek, H., Hajirezaei, M., Wobus, U., and, Weber, H., (2002) Antisense-inhibition of ADP-glucose pyrophosphorylase in Vicia narbonensis seeds increases soluble sugars, causes higher uptake of water and amino acids which leads to higher protein content. Planta, 214, 954-964.
49. Rösti, S., Rudi, H., Rudi, K., Opsahl-Sorteberg, H.G., Fahy, B., and, 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, 3619-3626.
50. Sanchez, D.H., Siahpoosh, M.R., Roessner, U., Udvardi, M., and, Kopka, J., (2008) Plant metabolomics reveals conserved and divergent metabolic responses to salinity. Physiol. Plant. 132, 209-219.
51. Schoor, S., Farrow, S.C., Blaschke, H., Lee, S., Perry, G., von Schwartzenberg, K., Emery, R.J.N., and, Moffatt, B.A., (2011) Adenosine kinase contributes to cytokinin interconversion in Arabidopsis. Plant Physiol. 157, 659-672.
52. Shewry, P.R., Hill, J.M., Pratt, H.M., Leggatt, M.M., and, Miflin, B.J., (1978) An evaluation of techniques for the extraction of hordein and glutelin from barley seed and a comparison of the protein composition of Bomi and Riso 1508. J. Exp. Bot. 9, 677-686.
53. Sienkiewicz-Porzucek, A., Sulpice, R., Osorio, S., Krahnert, I., Leisse, A., Urbanczyk-Wochniak, E., Hodges, M., Fernie, A.R., and, Nunes-Nesi, A., (2010) Mild reductions in mitochondrial NAD-dependent isocitrate dehydrogenase activity result in altered nitrate assimilation and pigmentation but do not impact growth. Mol. Plant. 3, 156-173.
54. Smeekens, S., (2000) Sugar-induced signal transduction in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 49-81.
55. Smith, A.M., Bettey, M., and, Bedford, I.D., (1989) Evidence that the rb locus alters the starch content of developing pea embryos through an effect on ADP glucose pyrophosphorylase. Plant Physiol. 89, 1279-1284.
56. Sreenivasulu, N., Radchuk, V., Alawady, A., et al. (2010) De-regulation of abscisic acid contents causes abnormal endosperm development in the barley mutant seg8. Plant J. 64, 589-603.
57. Stitt, M., Lilley, R.M., Gerhardt, R., and, Heldt, H.W., (1989) Metabolite levels in specific cells and subcellular compartments of plant leaves. Meth. Enzymol. 174, 518-552.
58. Tatematsu, K., Ward, S., Leyser, O., Kamiya, Y., and, Nambara, E., (2005) Identification of cis-elements that regulate gene expression during initiation of axillary bud outgrowth in Arabidopsis. Plant Physiol. 138, 757-766.
59. Tetlow, I.J., Morell, M.K., and, Emes, M.J., (2004) Recent developments in understanding the regulation of starch metabolism in higher plants. J. Exp. Bot. 55, 2131-2145.
60. Thomas, M.S., and, Flavell, R.B., (1990) Identification of an enhancer element for the endosperm-specific expression of high molecular weight glutenin. Plant Cell, 2, 1171-1180.
61. Trethewey, R.N., Geigenberger, P., Riedel, K., Hajirezaei, M.R., Sonnewald, U., Stitt, M., Riesmeier, J.W., and, Willmitzer, L., (1998) Combined expression of glucokinase and invertase in potato tubers leads to a dramatic reduction in starch accumulation and a stimulation of glycolysis. Plant J. 15, 109-118.
62. Trethewey, R.N., Geigenberger, P., Hennig, A., Fleischer-Notter, H., Müller-Röber, B., and, Willmitzer, L., (1999) Induction of the activity of glycolytic enzymes correlates with enhanced hydrolysis of sucrose in the cytosol of transgenic potato tubers. Plant Cell Environ. 22, 71-79.
63. Urano, K., Maruyama, K., Ogata, Y., et al. (2009) Characterization of the ABA-regulated global responses to dehydration in Arabidopsis by metabolomics. Plant J. 57, 1065-1078.
64. Usadel, B., Bläsing, O.E., Gibon, Y., Retzlaff, K., Höhne, M., Günther, M., and, Stitt, M., (2008) Global transcript levels respond to small changes of the carbon status during progressive exhaustion of carbohydrates in Arabidopsis rosettes. Plant Physiol. 146, 1834-1861.
65. Vicente-Carbajosa, J., Moose, S.P., Parsons, R.L., and, Schmidt, R.J., (1997) A maize zinc-finger protein binds the prolamin box in zein gene promoters and interacts with the basic leucine zipper transcriptional activator Opaque2. Proc. Natl. Acad. Sci. USA, 94, 7685-76890.
66. Wang, T.L., and, Hedley, C.L., (1993) Genetic and developmental analysis of the seed. In Peas: Genetics, Molecular Biology and Biochemistry (, Casey, R., and, Davies, D.R., eds). Wallingford, UK: CAB International, pp. 83-120.
67. 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.
68. Weber, H., Borisjuk, L., and, Wobus, U., (2005) Molecular physiology of legume seed development. Annu. Rev. Plant Biol. 56, 253-279.
69. Weichert, N., Saalbach, I., Weichert, H., et al. (2010) Increasing sucrose uptake capacity of wheat grains stimulates storage protein synthesis. Plant Physiol. 152, 698-710.
70. Weigelt, K., Küster, H., Radchuk, R., Müller, M., Weichert, H., Fait, A., Fernie, A.R., Saalbach, I., and, Weber, H., (2008) Increasing amino acid supply in pea embryos reveals specific interactions of N and C metabolism and highlights the importance of mitochondrial metabolism. Plant J. 55, 909-926.
71. Weigelt, K., Küster, H., Rutten, T., et al. (2009) ADP-glucose pyrophosphorylase-deficient pea embryos reveal specific transcriptional and metabolic changes of carbon-nitrogen metabolism and stress responses. Plant Physiol. 149, 395-411.
72. Weiner, H., Stitt, M., and, Heldt, H.W., (1987) Subcellular compartmentation of pyrophosphate and alkaline pyrophosphatase in leaves. Biochim. Biophys. Acta, 893, 18-21.
73. Wilson, C.M., Shewry, P.R., Faulks, A.J., and, Miflin, B.J., (1981) The extraction and separation of barley glutelins and their relationship to other endosperm proteins. J. Exp. Bot. 32 (131), 1287-1293.
74. Wu, C., Washida, H., Onodera, Y., Harada, K., and, Takaiwa, F., (2000) Quantitative nature of the Prolamin-box, ACGT and AACA motifs in a rice glutelin gene promoter: minimal cis-element requirements for endosperm-specific gene expression. Plant J. 23, 415-421.
75. Yang, J., Zhang, J., Huang, Z., Wang, Z., Zhu, Q., and, Liu, L., (2002) Correlation of cytokinin levels in the endosperms and roots with cell number and cell division activity during endosperm development in rice. Ann. Bot. 90, 369-377.