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Enhanced photosynthetic capacity increases nitrogen metabolism through the coordinated regulation of carbon and nitrogen assimilation in Arabidopsis thaliana

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Abstract

Plant growth and productivity depend on interactions between the metabolism of carbon and nitrogen. The sensing ability of internal carbon and nitrogen metabolites (the C/N balance) enables plants to regulate metabolism and development. In order to investigate the effects of an enhanced photosynthetic capacity on the metabolism of carbon and nitrogen in photosynthetically active tissus (source leaves), we herein generated transgenic Arabidopsis thaliana plants (ApFS) that expressed cyanobacterial fructose-1,6-/sedoheptulose-1,7-bisphosphatase in their chloroplasts. The phenotype of ApFS plants was indistinguishable from that of wild-type plants at the immature stage. However, as plants matured, the growth of ApFS plants was superior to that of wild-type plants. Starch levels were higher in ApFS plants than in wild-type plants at 2 and 5 weeks. Sucrose levels were also higher in ApFS plants than in wild-type plants, but only at 5 weeks. On the other hand, the contents of various free amino acids were lower in ApFS plants than in wild-type plants at 2 weeks, but were similar at 5 weeks. The total C/N ratio was the same in ApFS plants and wild-type plants, whereas nitrite levels increased in parallel with elevations in nitrate reductase activity at 5 weeks in ApFS plants. These results suggest that increases in the contents of photosynthetic intermediates at the early growth stage caused a temporary imbalance in the free-C/free-N ratio and, thus, the feedback inhibition of the expression of genes involved in the Calvin cycle and induction of the expression of those involved in nitrogen metabolism due to supply deficient free amino acids for maintenance of the C/N balance in source leaves of ApFS plants.

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References

  • Aronsson H, Jarvis P (2002) A simple method for isolating import-competent Arabidopsis chloroplasts. FEBS Lett 529:215–220

    Article  CAS  PubMed  Google Scholar 

  • Baroja-Fernández E, Muñoz FJ, Li J, Bahaji A, Almagro G, Montero M, Etxeberria E, Hidalgo M, Sesma MT, Pozueta-Romero J (2012) Sucrose synthase activity in the sus1/sus2/sus3/sus4 Arabidopsis mutant is sufficient to support normal cellulose and starch production. Proc Natl Acad Sci USA 109:321–326

    Article  PubMed  Google Scholar 

  • Baud S, Vaultier MN, Rochat C (2004) Structure and expression profile of the sucrose synthase multigene family in Arabidopsis. J Exp Bot 55:397–409

    Article  CAS  PubMed  Google Scholar 

  • Bieniawska Z, Paul Barratt DH, Garlick AP, Thole V, Kruger NJ, Martin C, Zrenner R, Smith AM (2007) Analysis of the sucrose synthase gene family in Arabidopsis. Plant J 49:810–828

    Article  CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Coruzzi G, Bush DR (2001) Nitrogen and carbon nutrient and metabolite signaling in plants. Plant Physiol 125:61–64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coruzzi GM, Zhou L (2001) Carbon and nitrogen sensing and signaling in plants: emerging ‘matrix effects’. Curr Opin Plant Biol 4:247–253

    Article  CAS  PubMed  Google Scholar 

  • 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 278:28508–28515

    Article  PubMed  Google Scholar 

  • Crevillén P, Ventriglia T, Pinto F, Orea A, Merida A, Romero JM (2005) Differential pattern of expression and sugar regulation of Arabidopsis thaliana ADP-Glc pyrophosphorylase-encoding genes. J Biol Chem 280:8143–8149

    Article  PubMed  Google Scholar 

  • Dellero Y, Lamothe-Sibold M, Jossier M, Hodges M (2015) Arabidopsis thaliana ggt1 photorespiratory mutants maintain leaf carbon/nitrogen balance by reducing RuBisCO content and plant growth. Plant J 83:1005–1018

    Article  CAS  PubMed  Google Scholar 

  • Ferrario-Méry S, Bouvet M, Leleu O, Savino G, Hodges M, Meyer C (2005) Physiological characterization of Arabidopsis mutants affected in the expression of the putative regulatory protein PII. Planta 223:28–39

    Article  PubMed  Google Scholar 

  • Foyer CH, Lescure JC, Lefebvre C, Morot-Gaudry JF, Vincentz M, Vaucheret H (1994) Adaptations of photosynthetic electron transport, carbon assimilation, and carbon partitioning in transgenic Nicotiana plumbaginifolia plants to changes in nitrate reductase activity. Plant Physiol 104:171–178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fritz C, Mueller C, Matt P, Feil R, Stitt M (2006) Impact of the C–N status on the amino acid profile in tobacco source leaves. Plant Cell Environ 29:2055–2076

    Article  CAS  PubMed  Google Scholar 

  • Fulton DC, Stettler M, Mettler T, Vaughan CK, Li J, Francisco P, Gil M, Reinhold H, Eicke S, Messerli G, Dorken G, Halliday K, Smith AM, Smith SM, Zeeman SC (2008) Beta-AMYLASE4, a noncatalytic protein required for starch breakdown, acts upstream of three active beta-amylases in Arabidopsis chloroplasts. Plant Cell 20:1040–1058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galtier N, Foyer C, Murchie E, Aired R, Quick P, Voelker T, Thépenier C, Lascève G, Betsche T (1995) 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

    Article  Google Scholar 

  • Gaufichon L, Masclaux-Daubresse C, Tcherkez G, Reisdorf-Cren M, Sakakibara Y, Hase T, Clément G, Avice JC, Grandjean O, Marmagne A, Boutet-Mercey S, Azzopardi M, Soulay F, Suzuki A (2013) Arabidopsis thaliana ASN2 encoding asparagine synthetase is involved in the control of nitrogen assimilation and export during vegetative growth. Plant Cell Environ 36:328–342

    Article  CAS  PubMed  Google Scholar 

  • Gutiérrez RA, Lejay LV, Dean A, Chiaromonte F, Shasha DE, Coruzzi GM (2007) Qualitative network models and genome-wide expression data define carbon/nitrogen-responsive molecular machines in Arabidopsis. Genome Biol 8:R7

    Article  PubMed  PubMed Central  Google Scholar 

  • Hachiya T, Sugiura D, Kojima M, Sato S, Yanagisawa S, Sakakibara H, Terashima I, Noguchi K (2014) High CO2 triggers preferential root growth of Arabidopsis thaliana via two distinct systems under low pH and low N stresses. Plant Cell Physiol 55:269–280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harrison EP, Olcer H, Lloyd JC, Long SP, Raines CA (2001) Small decreases in SBPase cause a linear decline in the apparent RuBP regeneration rate, but do not affect Rubisco carboxylation capacity. J Exp Bot 52:1779–1784

    Article  CAS  PubMed  Google Scholar 

  • Ho CH, Lin SH, Hu HC, Tsay YF (2009) CHL1 functions as a nitrate sensor in plants. Cell 138:1184–1194

    Article  CAS  PubMed  Google Scholar 

  • Hsieh MH, Lam HM, van de Loo FJ, Coruzzi G (1998) A PII-like protein in Arabidopsis: putative role in nitrogen sensing. Proc Natl Acad Sci USA 95:13965–13970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsu PK, Tsay YF (2013) Two phloem nitrate transporters, NRT1.11 and NRT1.12, are important for redistributing xylem-borne nitrate to enhance plant growth. Plant Physiol 163:844–856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ichikawa Y, Tamoi M, Sakuyama H, Maruta T, Ashida H, Yokota A, Shigeoka S (2010) Generation of transplastomic lettuce with enhanced growth and high yield. GM Crops 1:322–326

    Article  PubMed  Google Scholar 

  • Igarashi D, Miwa T, Seki M, Kobayashi M, Kato T, Tabata S, Shinozaki K, Ohsumi C (2003) Identification of photorespiratory glutamate:glyoxylate aminotransferase (GGAT) gene in Arabidopsis. Plant J 33:975–987

    Article  CAS  PubMed  Google Scholar 

  • Ishikawa T, Takeda T, Kohno H, Shigeoka S (1996) Molecular characterization of Euglena ascorbate peroxidase using monoclonal antibody. Biochim Biophys Acta 21:69–75

    Article  Google Scholar 

  • Jeong E-Y, Seo PJ, Woo JC, Park C-M (2015) AKIN10 delays flowering by interactivating IDD8 transcription factor through protein phosphorylation in Arabidopsis. BMC Plant Biol 15:110

    Article  PubMed  PubMed Central  Google Scholar 

  • Kanda Y (2013) Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant 48:452–458

    Article  CAS  PubMed  Google Scholar 

  • Kang J, Turano FJ (2003) The putative glutamate receptor 1.1 (AtGLR1.1) functions as a regulator of carbon and nitrogen. Bone Marrow Transplant 100:6872–6877

    CAS  Google Scholar 

  • Koch KE (1996) Carbohydrate-modulated gene expression in plants. Ann Rev Plant Physiol Plant Mol Biol 47:509–540

    Article  CAS  Google Scholar 

  • Konishi M, Yanagisawa S (2011) The regulatory region controlling the nitrate-responsive expression of a nitrate reductase gene, NIA1, in Arabidopsis. Plant Cell Physiol 52:824–836

    Article  CAS  PubMed  Google Scholar 

  • Konishi M, Yanagisawa S (2014) Emergence of a new step towards understanding the molecular mechanisms underlying nitrate-regulated gene expression. J Exp Bot 65:5589–5600

    Article  CAS  PubMed  Google Scholar 

  • Krapp A, David LC, Chardin C, Girin T, Marmagne A, Leprince AS, Chaillou S, Ferrario-Méry S, Meyer C, Daniel-Vedele F (2014) Nitrate transport and signaling in Arabidopsis. J Exp Bot 65:789–798

    Article  CAS  PubMed  Google Scholar 

  • Lam HM, Peng SS, Coruzzi GM (1994) Metabolic regulation of the gene encoding glutamine-dependent asparagine synthetase in Arabidopsis thaliana. Plant Physiol 106:1347–1357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lam HM, Hsieh MH, Coruzzi G (1998) Reciprocal regulation of distinct asparagine synthetase genes by light and metabolites in Arabidopsis thaliana. Plant J 16:345–353

    Article  CAS  PubMed  Google Scholar 

  • Lefebvre S, Lawson T, Fryer M, Zakhleniuk OV, Lloyd JC, Raines CA (2005) Increased sedoheptulose-1,7-bisphosphatase activity in transgenic tobacco plants stimulates potosynthesis and growth from an early stage in development. Plant Physiol 138:451–460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lillo C (2008) Signalling cascades integrating light-enhanced nitrate metabolism. Biochem J 415:11–19

    Article  CAS  PubMed  Google Scholar 

  • Liu XL, Yu HD, Guan Y, Li JK, Guo FQ (2012) Carbonylation and loss-of-function analyses of SBPase reveal its metabolic interface role in oxidative stress, carbon assimilation, and multiple aspects of growth and development in Arabidopsis. Mol Plant 5:1082–1099

    Article  CAS  PubMed  Google Scholar 

  • Lu Y, Sasaki Y, Li X, Mori IC, Matsuura T, Hirayama T, Sato T, Yamaguchi J (2015) ABI1 regulates carbon/nitrogen-nutrient signal transduction independent of ABA biosynthesis and canonical ABA signaling pathways in Arabidopsis. J Exp Bot 66:2763–2771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maruta T, Otori K, Tabuchi T, Tanabe N, Tamoi M, Shigeoka S (2010) New insights into the regulation of greening and carbon–nitrogen balance by sugar metabolism through a plastidic invertase. Plant Signal Behav 5:1131–1133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miyagawa Y, Tamoi M, Shigeoka S (2001) Overexpression of a cyanobacterial fructose-1,6-/sedoheptulose-1,7-bisphosphatase in tobacco enhances photosynthesis and growth. Nat Biotechnol 19:965–969

    Article  CAS  PubMed  Google Scholar 

  • Monroe JD, Storm AR, Badley EM, Lehman MD, Platt SM, Saunders LK, Schmitz JM, Torres CE (2014) β-Amylase1 and β-amylase3 are plastidic starch hydrolases in Arabidopsis that seem to be adapted for different thermal, pH, and stress conditions. Plant Physiol 166:1748–1763

    Article  PubMed  PubMed Central  Google Scholar 

  • Okamoto M, Vidmar JJ, Glass AD (2003) Regulation of NRT1 and NRT2 gene families of Arabidopsis thaliana: responses to nitrate provision. Plant Cell Physiol 44:304–317

    Article  CAS  PubMed  Google Scholar 

  • Rideout JW, Raper CD Jr, Miner GS (1992) Changes in ratio of soluble sugars and free amino nitrogen in the apical meristem during floral transition of tobacco. Int J Plant Sci 153:78–88

    Article  CAS  PubMed  Google Scholar 

  • Rojas-González JA, Soto-Súarez M, García-Díez A, Romero-Puertas MC, Sandalio LM, Mérida A, Thormálen I, Geigenberger P, Serrato AJ, Sahrawy M (2015) Disruption of both chloroplastic and cytosolic FBPase genes results in a dwarf phenotype and important starch and metabolite changes in Arabidopsis thaliana. J Exp Bot 66:2673–2689

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosenthal DM, Locke AM, Khozaei M, Raines CA, Long SP, Ort DR (2011) Over-expressing the C3 photosynthesis cycle enzyme sedoheptulose-1-7 Bisphosphatase improves photosynthetic carbon gain and yield under fully open air CO2 fumigation (FACE). BMC Plant Biol 11:123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato S, Yanagisawa S (2010) Capillary electrophoresis–electrospray ionization-mass spectrometry using fused-silica capillaries to profile anionic metabolites. Metabolomics 6:529–540

    Article  CAS  Google Scholar 

  • Sato S, Soga T, Nishioka T, Tomita M (2004) Simultaneous determination of the main metabolites in rice leaves using capillary electrophoresis mass spectrometry and capillary electrophoresis diode array detection. Plant J 40:151–163

    Article  CAS  PubMed  Google Scholar 

  • Sato T, Maekawa S, Yasuda S, Sonoda Y, Katoh E, Ichikawa T, Nakazawa M, Seki M, Shinozaki K, Matsui M, Goto DB, Ikeda A, Yamaguchi J (2009) CNI1/ATL31, a RING-type ubiquitin ligase that functions in the carbon/nitrogen response for growth phase transition in Arabidopsis seedlings. Plant J 60:852–864

    Article  CAS  PubMed  Google Scholar 

  • Scheible WR, González-Fontes A, Lauerer M, Müller-Rober B, Caboche M, Stitt M (1997) Nitrate acts as signal to induce organic acid metabolism and repress starch metabolism in tobacco. Plant Cell 9:783–798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sheen J (1990) Metabolic repression of transcription in higher plants. Plant Cell 2:1027–1038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi J, Yi K, Liu Y, Xie L, Zhou Z, Chen Y, Hu Z, Zheng T, Liu R, Chen Y, Chen J (2015) Phosphoenolpyruvate carboxylase in Arabidopsis leaves plays a crucial role in carbon and nitrogen metabolism. Plant Physiol 167:671–681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simkin AJ, McAusland L, Headland LR, Lawson T, Raines CA (2015) Multigene manipulation of photosynthetic carbon assimilation increases CO2 fixation and biomass yield in tobacco. J Exp Bot 66:4075–4090

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stadtman ER (2001) The story of glutamine synthetase regulation. J Biol Chem 276:44357–44364

    Article  CAS  PubMed  Google Scholar 

  • Stitt M, Zeeman SC (2012) Starch turnover: pathways, regulation and role in growth. Curr Opin Plant Biol 5:282–292

    Article  Google Scholar 

  • Szydlowski N, Ragel P, Raynaud S, Lucas MM, Roldán I, Montero M, Muñoz FJ, Ovecka M, Bahaji A, Planchot V, Pozueta-Romero J, D’Hulst C, Mérida A (2009) Starch granule initiation in Arabidopsis requires the presence of either class IV or class III starch synthases. Plant Cell 21:2443–2457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamoi M, Murakami A, Takeda T, Shigeoka S (1998) Acquisition of a new type of fructose-1,6-bisphosphatase with resistance to hydrogen peroxide in cyanobacteria: molecular characterization of the enzyme from Synechocystis PCC 6803. Biochim Biophys Acta 1383:232–244

    Article  CAS  PubMed  Google Scholar 

  • Tamoi M, Tabuchi T, Demuratani M, Otori K, Tanabe N, Maruta T, Shigeoka S (2010) Point mutation of a plastidic invertase inhibits deveropment of the photosynthetic apparatus and enhances nitrate assimilation in sugar-treated Arabidopsis seedling. J Biol Chem 285:15399–15407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Velez-Ramirez A, Ieperen WV, Vreugdenhil D, Millenaar FF (2011) Plants under continuous light. Trends in Plant Sci 16:310–318

    Article  CAS  Google Scholar 

  • Wang R, Guegler K, LaBrie ST, Crawford NM (2000) Genomic analysis of a nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes induced by nitrate. Plant Cell 12:1491–1509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang R, Okamoto M, Xing X, Crawford NM (2003) Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1,000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron, and sulfate metabolism. Plant Physiol 132:556–567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams SP, Rangarajan P, Donahue JL, Hess JE, Gillaspy GE (2014) Regulation of sucrose non-fermenting related kinase 1 genes in Arabidopsis thaliana. Front Plant Sci 5:324

    PubMed  PubMed Central  Google Scholar 

  • Yabuta Y, Tamoi M, Yamamoto K, Tomizawa K, Yokota A, Shigeoka S (2008) Molecular design of photosynthesis-elevated chloroplasts for mass accumulation of a foreign protein. Plant Cell Physiol 49:375–385

    Article  CAS  PubMed  Google Scholar 

  • Yanagisawa S, Akiyama A, Kisaka H, Uchimiya H, Miwa T (2004) Metabolic engineering with Dof1 transcription factor in plants: Improved nitrogen assimilation and growth under low-nitrogen conditions. Proc Natl Acad Sci USA 101:7833–7838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng ZL (2009) Carbon and nitrogen nutrient balance signaling in plants. Plant Signal Behav 4:584–591

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang L, Zhang H, Zhang H, Deng XW, Wei N (2015) HY5 regulates nitrite reductase 1 (NIR1) and ammonium transporter1;2 (AMT1;2) in Arabidopsis seedlings. Plant Sci 238:330–339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marchive C, Roudier F, Castaings L, Bréhaut V, Blondet E, Colot V, Meyer C, Krapp A (2013) Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants. Nat Commun 4:1713

    Article  PubMed  Google Scholar 

  • Price J (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16(8):2128–2150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roldán I, Wattebled F, Mercedes Lucas M, Delvallé D, Planchot V, Jiménez S, Pérez R, Ball S, D'Hulst C, Mérida A (2007) The phenotype of soluble starch synthase IV defective mutants of Arabidopsis thaliana suggests a novel function of elongation enzymes in the control of starch granule formation. Plant J 49:492–504

  • Ventriglia T, Kuhn ML, Ruiz MT, Ribeiro-Pedro M, Valverde F, Ballicora MA, Preiss J, Romero JM (2008) Two Arabidopsis ADP-glucose pyrophosphorylase large subunits (APL1 and APL2) are catalytic. Plant Physiol 148(1):65–76

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by JST CREST Grant Number JPMJCR12B3 (S.S.) and JPMJCR15O5 (S.Y.), Japan.

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    Authors and Affiliations

    1. Department of Advanced Bioscience, Faculty of Agriculture, Kindai University, Nakamachi, Nara, 631-8505, Japan

      Kumi Otori, Noriaki Tanabe, Toshiki Maruyama, Masahiro Tamoi & Shigeru Shigeoka

    2. Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency, Kawaguchi, 332-0012, Japan

      Kumi Otori, Noriaki Tanabe, Shuichi Yanagisawa, Masahiro Tamoi & Shigeru Shigeoka

    3. Biotechnology Research Center, The University of Tokyo, Yayoi 1-1-1, Bunkyo-ku, Tokyo, 113-8657, Japan

      Shigeru Sato & Shuichi Yanagisawa

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    1. Kumi Otori
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    Correspondence to Masahiro Tamoi.

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    Kumi Otori and Noriaki Tanabe contributed equally to this work.

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    Otori, K., Tanabe, N., Maruyama, T. et al. Enhanced photosynthetic capacity increases nitrogen metabolism through the coordinated regulation of carbon and nitrogen assimilation in Arabidopsis thaliana . J Plant Res 130, 909–927 (2017). https://doi.org/10.1007/s10265-017-0950-4

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