Photosynthetica 2006, 44(1):1-10 | DOI: 10.1007/s11099-005-0151-6

Developmental regulation of photosynthate distribution in leaves of rice

T. Shinano1, K. Nakajima2, J. Wasaki1, H. Mori2, T. Zheng2, M. Osaki2
1 Creative Research Initiative "Sousei" (CRIS), Hokkaido University, Sapporo, Japan
2 Graduate School of Agriculture, Hokkaido University, Sapporo, Japan

mRNA expression patterns of genes for metabolic key enzymes sucrose phosphate synthase (SPS), phosphoenolpyruvate carboxylase (PEPC), pyruvate kinase, ribulose 1,5-bisphosphate carboxylase/oxygenase, glutamine synthetase 1, and glutamine synthetase 2 were investigated in leaves of rice plants grown at two nitrogen (N) supplies (N0.5, N3.0). The relative gene expression patterns were similar in all leaves except for 9th leaf, in which mRNA levels were generally depressed. Though increased N supply prolonged the expression period of each mRNA, it did not affect the relative expression intensity of any mRNA in a given leaf. SPS Vmax, SPS limiting and PEPC activities, and carbon flow were examined. The ratio between PEPC activity and SPS Vmax was higher in leaves developed at the vegetative growth stage (vegetative leaves: 5th and 7th leaves) than in leaves developed after the ear primordia formation stage (reproductive leaves: 9th and flag leaves). PEPC activity and SPS Vmax decreased with declining leaf N content. After using 14CO2 the 14C photosynthate distribution in the amino acid fraction was higher in vegetative than in reproductive leaves when compared for the same leaf N status. Thus, at high PEPC/SPS activities ratio, more 14C photosynthate was distributed to the amino acid pool, whereas at higher SPS activity more 14C was channelled into the saccharide fraction. Thus, leaf ontogeny was an important factor controlling photosynthate distribution to the N- or C-pool, respectively, regardless of the leaf N status.

Additional key words: glutamine synthetases; leaf development; mRNA expression; Oryza; phosphoenolpyruvate carboxylase; pyruvate kinase; ribulose-1,5-bisphosphate carboxylase, oxygenase; sucrose phosphate synthase

Received: January 3, 2005; Accepted: April 26, 2005; Published: March 1, 2006  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Shinano, T., Nakajima, K., Wasaki, J., Mori, H., Zheng, T., & Osaki, M. (2006). Developmental regulation of photosynthate distribution in leaves of rice. Photosynthetica, 44(1), 1-10. doi: 10.1007/s11099-005-0151-6
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Bakrim, N., Brulfert, J., Vidal, J., Chollet, R.: Phosphoenolpyruvate carboxylase kinase is controlled by a similar signaling cascade in CAM and C4 plants. - Biochem. biophys. Res. Commun. 286: 1158-1162, 2001. Go to original source...
    2. Buchanan-Wollaston, V., Ainsworth, C.: Leaf senescence in Brassica napus: cloning of senescence related genes by subtractive hybridization. - Plant mol. Biol. 33: 821-834, 1997. Go to original source...
    3. Champigny, M.-L., Foyer, C.: Nitrate activation of cytosolic protein kinases diverts photosynthetic carbon from sucrose to amino acid biosynthesis. Basis for a new concept. - Plant Physiol. 100: 7-12, 1992. Go to original source...
    4. Copeland, L., Turner, J.F.: The regulation of glycolysis and the pentose phosphate pathway. - In: Stumpf, P.K., Conn, E.E. (ed.): The Biochemistry of Plants. Pp. 107-128. Academic Press, New York 1987. Go to original source...
    5. Duff, S.M.G., Chollet, R.: In vivo regulation of wheat-leaf phosphoenolpyruvate carboxylase by reversible phosphorylation. - Plant Physiol. 107: 775-782, 1995. Go to original source...
    6. Fellows, R.J., Geiger, D.R.: Structural and physiological changes in sugar beet leaves during sink to source conversion. - Plant Physiol. 54: 877-885, 1974. Go to original source...
    7. Foyer, C.H., Noctor, G., Lelandais, M., Lescure, J.C., Valadier, M.H., Boutin, J.P., Horton, P.: Short-term effects of nitrate, nitrite and ammonium assimilation on photosynthesis, carbon partitioning and protein phosphorylation in maize. - Planta 192: 211-220, 1994. Go to original source...
    8. Foyer, C.H., Valadier, M.H., Ferrario, S.: Co-regulation of nitrogen and carbon assimilation in leaves. - In: Smirnoff, N. (ed.): Environment and Plant Metabolism. Flexibility and Acclimation. Pp. 17-33. BIOS Scientific Publishers, Oxford 1995.
    9. Galtier, N., Foyer, C.H., Huber, J., Voelker, T.A., Huber, S.C.: Effects of elevated sucrose-phosphate synthase activity on photosynthesis, assimilate partitioning, and growth in tomato (Lycopersicon esculentum var. UC82B). - Plant Physiol. 101: 535-543, 1993. Go to original source...
    10. Galtier, N., Foyer, C.H., Murchie, E., Alred, R., Quick, P., Voelker, T.A., Thepenier, C., Lasceve, G., Betsche, T.: Effects of light and atmospheric carbon dioxide enrichment on photosynthesis and carbon partitioning in the leaves of tomato (Lycopersicon esculentum L.) plants over-expressing sucrose phosphate synthase. - J. exp. Bot. 46: 1335-1344, 1995. Go to original source...
    11. Huber, J.L., Redinbaugh, M.G., Huber, S.C., Campbell, W.H.: Regulation of maize leaf nitrate reductase activity involves both gene expression and protein phosphorylation. - Plant Physiol. 106: 1667-1674, 1994. Go to original source...
    12. Huber, S.C., Huber, J.L.: Role of sucrose synthase in sucrose metabolism in leaves. - Plant Physiol. 99: 673-678, 1992. Go to original source...
    13. Huber, S.C., Huber, J.L.: Role and regulation of sucrose-phosphate-synthase in higher plants. - Annu. Rev. Plant Physiol. Plant mol. Biol. 47: 431-444, 1996. Go to original source...
    14. Huppe, H.C., Turpin, D.H.: Integration of carbon and nitrogen metabolism in plant and algal cells. - Annu. Rev. Plant Physiol. Plant mol. Biol. 45: 577-607, 1994. Go to original source...
    15. Kamachi, K., Yamaya, T., Mae, T., Ojima, K.: A role for glutamine synthetase in the remobilization of leaf nitrogen during natural senescence in rice leaves. - Plant Physiol. 96: 411-417, 1991. Go to original source...
    16. Kawakami, N., Watanabe, A.: Senescence-specific increase in cytosolic gutamine synthetase and its mRNA in radish cotyledons. - Plant Physiol. 88: 1430-1434, 1988. Go to original source...
    17. Koga, N., Ikeda, M.: Responses to nitrogen sources and regulatory properties of root phosphoenolpyruvate carboxylase. - Soil Sci. Plant Nutr. 43: 643-650, 1997. Go to original source...
    18. Kozaki, A., Takeba, G.: Photorespiration protects C3 plants from photooxidation. - Nature 384: 557-560, 1996. Go to original source...
    19. Laporte, M.M., Galagan, J.A., Prasch, A.L., Vanderveer, P.J., Hanson, D.T., Shewmaker, C.K., Sharkey, T.D.: Promoter strength and tissue specificity effects on growth of tomato plants transformed with maize sucrose-phosphate synthase. - Planta 212: 817-22, 2001. Go to original source...
    20. MacKintosh, C.: Regulation of plant nitrate assimilation: from ecophysiology to brain proteins. - New Phytol. 139: 153-159, 1998. Go to original source...
    21. Micallef, B.J., Haskins, K.A., Vanderveer, P.J., Roh, K.S., Shewmaker, C.K., Sharkey, T.D.: Altered photosynthesis, flowering, and fruiting in transgenic tomato plants that have an increased capacity for sucrose synthesis. - Planta 196: 327-334, 1995. Go to original source...
    22. Murchie, E.H., Sarrobert, C., Contard, P., Betsche, T., Foyer, C., Galtier, N.: Overexpression of sucrose-phosphate synthase in tomato plants grown with CO2 enrichment leads to decreased controls. - Plant Physiol. Biochem. 37: 251-260, 1999. Go to original source...
    23. Nakamura, T., Osaki, M., Shinano, T., Tadano, T.: Difference in system of current photosynthesized carbon distribution to carbon and nitrogen compounds between rice and soybean. - Soil Sci. Plant Nutr. 43: 777-788, 1997. Go to original source...
    24. Osaki, M., Hada, K., Tanaka, A.: [Reconstruction of the leaf-proteins into grain-proteins during ripening in the rice plant.] - Jap. J. Soil Sci. Plant Nutr. 59: 272-278, 1988. [In Jap.]
    25. Osaki, M., Shinano, T., Tadano, T.: Carbon-nitrogen interaction in field crop production. - Soil Sci. Plant Nutr. 38: 553-564, 1992. Go to original source...
    26. Palmiter, R.D.: Magnesium precipitation of ribonucleoprotein complexes: expedient techniques for the isolation of undegraded polysomes and messenger ribonucleic acid. - Biochemistry 13: 3606-3615, 1974. Go to original source...
    27. Plaxton, W.C.: The organization and regulation of plant glycolysis. - Annu. Rev. Plant Physiol. Plant mol. Biol. 47: 185-214, 1996. Go to original source...
    28. Plaxton, W.C., Sangwan, R.S., Singh, N., Gauthier, D.A., Turpin, D.H.: Phosphoenolpyruvate metabolism of developing oil seeds. - In: MacKenzie, S.L., Taylor, D.C. (ed.): Seed Oils for the Future. Pp. 35-43. AOCS Press, Champaign 1993.
    29. Plumley, F.G., Schmidt, G.W.: Nitrogen-dependent regulation of photosynthetic gene expression. - Proc. nat. Acad. Sci. USA 86: 2678-2682, 1989. Go to original source...
    30. Quy, L.V., Champigny, M.-L.: NO3 - enhances the kinase activity for phosphorylation of phosphoenolpyruvate carboxylase and sucrose phosphate synthase proteins in wheat leaves. - Plant Physiol. 99: 344-347, 1992. Go to original source...
    31. Quy, L.V., Foyer, C.H., Champigny, M.-L.: Effect of light and NO3 - on wheat leaf phosphoenolpyruvate carboxylase activity. Evidence for covalent modulation of the C3 enzyme. - Plant Physiol. 97: 1476-1482, 1991. Go to original source...
    32. Rademacher, T., Hausler, R.E., Hirsch, H.J., Zhang, L., Lipka, V., Weier, D., Kreuzaler, F., Peterhansel, C.: An engineered phosphoenolpyruvate carboxylase redirects carbon and nitrogen flow in transgenic potato plants. - Plant J. 32: 25-39, 2002. Go to original source...
    33. Sagi, M., Dovrat, A., Kipnis, T., Lips, H.: Nitrate reductase, phosphoenolpyruvate carboxylase, and glutamine synthetase in annual ryegrass as affected by salinity and nitrogen. - J. Plant Nutr. 21: 707-723, 1998. Go to original source...
    34. Sakakibara, H., Kawabata, S., Hase, T., Sugiyama, T.: Differential effects of nitrate and light on the expression of glutamine synthetases and ferredoxin-dependent glutamate synthase in maize. - Plant Cell Physiol. 33: 1193-1198, 1992.
    35. Shinano, T., Osaki, M., Tadano, T.: 14C-allocation of 14C-compounds introduced to a leaf to carbon and nitrogen components in rice and soybean during ripening. - Soil Sci. Plant Nutr. 40: 199-210, 1994. Go to original source...
    36. Shinano, T., Osaki, M., Tadano, T.: Problems in the methods of estimation of growth and maintenance respiration. - Soil Sci. Plant Nutr. 42: 773-784, 1996. Go to original source...
    37. Signora, L., Galtier, N., Skot, L., Lucas, H., Foyer, C.H.: Overexpression of sucrose phosphate synthase in Arabidopsis thaliana results in increased foliar sucrose/starch ratios and favours decreased foliar carbohydrate accumulation in plants after prolonged growth with CO2 enrichment. - J. exp. Bot. 49: 669-680, 1998. Go to original source...
    38. Stitt, M.: Nitrate regulation of metabolism and growth. - Curr. Opin. Plant Biol. 2: 178-186, 1999. Go to original source...
    39. Stitt, M., Gerhardt, R., Wilke, I., Heldt, H.W.: The contribution of fructose 2,6-bisphosphate to the regulation of sucrose synthesis during photosynthesis. - Physiol. Plant. 69: 377-386, 1987. Go to original source...
    40. Stitt, M., Wilke, I., Feil, R., Heldt, H.W.: Coarse control of sucrose-phosphate synthase in leaves: Alterations of the kinetic properties in response to the rate of photosynthesis and the accumulation of sucrose. - Planta 174: 217-230, 1988. Go to original source...
    41. Sugiharto, B., Sugiyama, T.: Effects of nitrate and ammonium on gene expression of phosphoenolpyruvate carboxylase and nitrogen metabolism in maize leaf tissue during recovery from nitrogen stress. - Plant Physiol. 98: 1403-1408, 1992. Go to original source...
    42. Sugiharto, B., Suzuki, I., Burnell, J.N., Sugiyama, T.: Glutamine induces the N-dependent accumulation of mRNAs encoding phosphoenolpyruvate carboxylase and carbonic anhydrase in detached maize leaf tissue. - Plant Physiol. 100: 2066-2070, 1992. Go to original source...
    43. Suzuki, I., Cretin, C., Omata, T., Sugiyama, T.: Transcriptional and posttranscriptional regulation of nitrogen-responding expression of phosphoenolpyruvate carboxylase gene in maize. - Plant Physiol. 105: 1223-1229, 1994. Go to original source...
    44. Tanaka, A., Osaki, M.: Growth and behavior of photosynthesized 14C in various crops in relation to productivity. - Soil Sci. Plant Nutr. 29: 147-158, 1983. Go to original source...
    45. Taybi, T., Patil, S., Chollet, R., Cushman, J.C.: A minimal serine/threonine protein kinase circadianly regulates phosphoenolpyruvate carboxylase in Crassulacean acid metabolism-induced leaves of the common ice plants. - Plant Physiol. 123: 1471-1481, 2000. Go to original source...
    46. Turgeon, R.: The sink-source transition in leaves. - Annu. Rev. Plant Physiol. Plant mol. Biol. 40: 119-138, 1989. Go to original source...
    47. Vanlerberghe, G.C., Schuller, K.A., Smith, R.G., Feil, R., Plaxton, W.C., Turpin, D.H.: Relationship between NH4 + assimilation rate and in vivo phosphoenolpyruvate carboxylase activity. Regulation of anaplerotic carbon flow in the green alga Selenastrum minutum. - Plant Physiol. 94: 284-290, 1990. Go to original source...
    48. Vidal, J., Chollet, R.: Regulatory phosphorylation of C4 PEP carboxylase. - Trends Plant Sci. 2: 230-237, 1997. Go to original source...
    49. Wallenda, T., Schaefeer, C., Einig, W., Wingler, A., Hampp, U., Seith, B., George, E., Marshner, H.: Effects of varied soil nitrogen supply on Norway spruce (Picea abies (L.) Karst.). - Plant Soil 186: 361-369, 1996. Go to original source...
    50. Worrel, A.C., Bruneau, J.-M., Summerfelt, K., Boersig, M., Voelker, T.A.: Expression of a maize sucrose phosphate synthase in tomato alters leaf carbohydrate partitioning. - Plant Cell 3: 1121-1130, 1991. Go to original source...

    Return to the content