Skip to main content
SpringerLink
Log in

Profiling of diurnal patterns of metabolite and transcript abundance in potato (Solanum tuberosum) leaves

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Diurnal changes in carbohydrates and a broad range of primary metabolites were analysed through a diurnal period in potato leaves (Solanum tuberosum cv. Desiree) using an established gas chromatography-mass spectrometry based metabolic profiling protocol alongside conventional spectrophotometric technologies. In tandem, we profiled transcript levels using both a custom array containing approximately 2,500 cDNA clones predominantly representing transcripts involved in primary metabolism and commercially available arrays containing approximately 12,000 cDNA clones that gave coverage of transcript levels over a broader functional range. The levels of many metabolites and transcripts varied during the diurnal period with 56 significant differences observed in the metabolite contents and 832 significant differences recorded in transcript levels. Whilst a large number of the differences would be expected from what has been known previously, several novel changes were observed in these experiments. Notably, qualitative comparison of the combined data sets obtained from the parallel analysis of transcripts and metabolites suggests relatively few changes in gene expression strongly correlate with changes in metabolite levels during a diurnal cycle. Furthermore, these changes appear to be confined to the central metabolic pathways. However, principal component analysis of the metabolic profiles obtained here revealed that metabolite patterns change progressively through a diurnal period suggesting the operation of mechanisms for tight temporal regulation of metabolite composition.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aharoni A, Giri AP, Deuerlein S, Griepink F, de Kogel WJ, Verstappen FWA, Verhoeven HA, Jongsmaa MA, Schwab W, Bouwmeester HJ (2003) Terpenoid metabolism in wild-type and transgenic Arabidopsis plants. Plant Cell 15:2866–2884

    Google Scholar 

  • Atkin OK, Evans JE, Ball MC, Lambers H, Pons TL (2000) Leaf respiration of snowgum in light and dark: interactions between temperature and irradiance. Plant Physiol 122:915–923

    Google Scholar 

  • Brandt S, Kloska S, Altmann T, Kehr J (2002) Using array hybridisation to monitor gene expression at the single cell level. J Exp Bot 53:2315–2323

    Article  CAS  PubMed  Google Scholar 

  • Budde RJA, Randall DD (1990) Pea leaf mitochondrial pyruvate dehydrogenase complex is inactivated in vivo in a light-dependent manner. Proc Natl Acad Sci USA 87:673–676

    Google Scholar 

  • Carrari F, Nunes-Nesi A, Gibon Y, Lytovchenko A, Ehlers-Lourario M, Fernie AR (2003a) Reduced expression of aconitase results in an enhanced rate of photosynthesis and marked shifts in carbon partitioning in illuminated leaves of Lycopersicon pennellii. Plant Physiol 133:1322–1335

    Google Scholar 

  • Carrari F, Urbanczyk-Wochniak E, Willmitzer L, Fernie AR (2003b) Engineering central metabolism in crop species: learning the system. Metab Eng 5:191–200

    Google Scholar 

  • Carrari F, Coll-Garcia D, Schauer N, Lytovchenko A, Palacios-Rojas N, Balbo I, Rosso M, Fernie AR (2005) Deficiency of a plastidial adenylate kinase in Arabidopsis results in elevated photosynthesis amino acid biosynthesis and enhanced growth. Plant Physiol 137:70–82

    Google Scholar 

  • Chen F, Duran AL, Blount JW, Sumner LW, Dixon RA (2003) Profiling phenolic metabolites in transgenic alfalfa modified in lignin biosynthesis. Pytochemistry 64:1013–1021

    Google Scholar 

  • Chia T, Thorneycroft D, Chapple A, Messerli G, Chen J, Zeeman SC, Smith SM, Smith AM (2004) A cytosolic glucosyltransferase is required for conversion of starch to sucrose in Arabidopsis leaves at night. Plant J 37:853–863

    Article  Google Scholar 

  • Colebatch G, Kloska S, Trevaskis B, Freund S, Altmann T, Udvardi MK (2002) Novel aspects of symbiotic nitrogen fixation uncovered by transcript profiling with cDNA arrays. Mol Plant Microbe Interact 15:411–420

    Google Scholar 

  • Czechowski T, Bari RP, Stitt M, Scheible WR, Udvardi MK (2004) Real-time RT-PCR profiling of over 1400 Arabidopsis transcription factors: unprecedented sensitivity reveals novel root- and shoot-specific genes. Plant J 38:366–379

    Article  CAS  PubMed  Google Scholar 

  • Draborg H, Villadsen D, Nielsen TH (2001) Transgenic Arabidopsis plants with decreased activity of frustose-6-phosphate,2-kinase/fructose-2,6-bisphosphatase have altered carbon partitioning. Plant Physiol 126:750–758

    Google Scholar 

  • Fejes E, Nagy F (1998) Molecular analysis of the circadian clock related gene expression in plants: features of the “output” pathways. In: Lumsden PJ, Millar AJ (eds) Biological rythyms and photoperiodism in plants. BIOS Scientific, Oxford, pp 99–118

    Google Scholar 

  • Fernie AR, Willmitzer L (2004) Carbohydrate metabolism. In: Christou P, Klee HK (eds) The handbook of plant biotechnology. Wiley, Chichester (in press)

  • Fernie AR, Roscher A, Ratcliffe RG, Kruger NJ (2001) Fructose 2,6-bisphosphate activates pyrophosphate: fructose-6-phosphate 1-phosphotransferase and increases triose phosphate to hexose phosphate cycling in heterotrophic cells. Planta 212:250–263

    Google Scholar 

  • Fernie AR, Carrari F, Sweetlove LJ (2004) Respiratory metabolism: glycolysis, the TCA cycle and the electron transport chain. Curr Opin Plant Biol 7:254–261

    Google Scholar 

  • Ferrario-Mery S, Masclaux C, Suzuki A, Valadier MH, Hirel B, Foyer CH (2001) Glutamine and alpha-ketoglutarate are metabolite signals involved in nitrate reductase gene transcription in untransformed and transformed tobacco plants deficient in ferredoxin-glutamine-alpha-ketoglutarate aminotransferase. Planta 213:265–271

    Article  Google Scholar 

  • Ferrario-Mery S, Hodges M, Hirel B, Foyer CH (2002a) Photorespiration-dependent increases in phosphoenolpyruvate carboxylase, isocitrate dehydrogenase and glutamate dehydrogenase in transformed tobacco plants deficient in ferredoxin-dependent glutamine-alpha-ketoglutarate aminotransferase. Planta 214:877–886

    Google Scholar 

  • Ferrario-Mery S, Valadier MH, Godefroy N, Miallier D, Hirel B, Foyer CH, Suzuki A (2002b) Diurnal changes in ammonia assimilation in transformed tobacco plants expressing ferredoxin-dependent glutamate synthase mRNA in the antisense orientation. Plant Sci 163:59–67

    Google Scholar 

  • Fiehn O, Kopka J, Dörmann P, Altmann T, Trethewey RN, Willmitzer L (2000) Metabolite profiling for plant functional genomics. Nat Biotechnol 18:1157–1161

    Article  CAS  PubMed  Google Scholar 

  • Geigenberger P, Stitt M (2000) Diurnal changes in sucrose, nucleotides, starch synthesis and AGPS transcript in growing potato tubers that are suppressed by decreased expression of sucrose phosphate synthase. Plant J 23:795–806

    Google Scholar 

  • Geiger DR, Servaites JC (1994) Diurnal regulation of photosynthetic carbon metabolism in C-3 plants. Annu Rev Plant Biol 45:235–256

    Google Scholar 

  • Girke T, Todd J, Ruuska S, White J, Benning C, Ohlrogge J (2000) Microarray analysis of developing Arabidopsis seeds. Plant Physiol 124:1570–1581

    Article  Google Scholar 

  • Guo DJ, Chen F, Inoue K, Blount JW, Dixon RA (2001) Downregulation of caffeic acid 3-O-methyltransferase and caffeoyl CoA 3-O-methyltransferase in transgenic alfalfa: impacts on lignin structure and implications for the biosynthesis of G and S lignin. Plant Cell 13:73–88

    Google Scholar 

  • Harmer SL, Hogenesch LB, Straume M, Chang HS, Han B, Zhu T, Wang X, Kreps JA, Kay SA (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290:2110–2113

    Article  CAS  PubMed  Google Scholar 

  • Howles PA, Sewalt VJH, Paiva NL, Elkind Y, Bate NJ, Lamb C, Dixon RA (1996) Overexpression of L-phenylalanine ammonia-lyase in transgenic tobacco plants reveals control points for flux into phenylpropanoid biosynthesis. Plant Physiol 112:1617–1624

    CAS  PubMed  Google Scholar 

  • Kruger NJ (1997) Carbohydrate synthesis and degradation. In: Dennis DT, Turpin DH, Lefebvre DD, Layzell DB (eds) Plant Metabolism. Longman, Harlow, pp 83–104

    Google Scholar 

  • Lu Y, Sharkey TD (2004) The role of amylomaltase in maltose metabolism in the cytosol of photosynthetic cells. Planta 218:466–473

    Google Scholar 

  • Lytovchenko A, Bieberich K, Willmitzer L, Fernie AR (2002a) Carbon assimilation and metabolism in potato leaves deficient in plastidial phosphoglucomutase. Planta 215:802–811

    Google Scholar 

  • Lytovchenko A, Sweetlove LJ, Pauly M, Fernie AR (2002b) The influence of cytosolic phosphoglucomutase on photosynthetic carbohydrate metabolism. Planta 215:1013–1021

    Google Scholar 

  • Masclaux-Daubresse C, Valadier MH, Carrayol E, Reisdorf-Cren M, Hirel B (2002) Diurnal changes in the expression of glutamate dehydrogenase and nitrate reductase are involved in the C/N balance of tobacco source leaves. Plant Cell Environ 25:1451–1462

    Google Scholar 

  • Matt P, Schurr U, Klein D, Krapp A, Stitt M (1998) Growth of tobacco in short-day conditions leads to high starch, low sugars, altered diurnal changes in the Nia transcript and low nitrate reductase activity, and inhibition of amino acid synthesis. Planta 207:27–41

    Google Scholar 

  • Matt P, Geiger M, Walch-Liu P, Engels C, Krapp A, Stitt M (2001) The immediate cause of the diurnal changes of nitrogen metabolism in leaves of nitrate-replete tobacco: a major imbalance between the rate of nitrate reduction and the rates of nitrate uptake and ammonium metabolism during the first part of the light period. Plant Cell Environ 24:177–190

    Google Scholar 

  • Matt P, Krapp A, Haake V, Mock HP, Stitt M (2002) Decreased Rubisco activity leads to dramatic changes of nitrate metabolism, amino acid metabolism and the levels of phenylpropanoids and nicotine in tobacco antisense RBCS transformants. Plant J 30:663–677

    Google Scholar 

  • Müller C, Scheible WR, Stitt M, Krapp A (2001) Influence of malate and 2-oxoglutarate on the NIA transcript level and nitrate reductase activity in tobacco leaves. Plant Cell Environ 24:191–203

    Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plantarum 15:473–497

    Google Scholar 

  • Niittyla T, Messerli G, Trevisan M, Chen J, Smith AM, Zeeman SC (2004) A previously unknown maltose transporter essential for starch degradation in leaves. Science 303:87–89

    Article  PubMed  Google Scholar 

  • Piechulla B (1988) Plastid and nuclear mRNA fluctuations in tomato leaves—diurnal and circadian rhythms during extended dark and light periods. Plant Mol Biol 11:345–353

    Google Scholar 

  • Raghavendra AS, Padmasree K (2003) Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Trends Plant Sci 8:546–553

    Google Scholar 

  • Roessner U, Luedemann A, Brust D, Fiehn O, Linke T, Willmitzer L, Fernie AR (2001) Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell 13:11–29

    Article  CAS  PubMed  Google Scholar 

  • Roessner-Tunali U, Hegemann B, Lytovchenko A, Carrari F, Bruedigam C, Granot D, Fernie AR (2003) Metabolic profiling of transgenic tomato plants overexpressing hexokinase reveals that the influence of hexose phosphorylation diminishes during fruit development. Plant Physiol 133:84–99

    Google Scholar 

  • Scheible W-R, Gonzalez-Fontes A, Morcuende R, Lauerer M, Geiger M, Glaab J, Gojon A, Schulze ED, Stitt M (1997) Tobacco mutants with a decreased number of functional nia genes compensate by modifying the diurnal regulation of transcription, post-translational modification and turnover of nitrate reductase. Planta 203:304–319

    Google Scholar 

  • Scheible W-R, Krapp A, Stitt M (2000) Reciprocal diurnal changes of phosphoenolpyruvate carboxylase expression and cytosolic pyruvate kinase, citrate synthase and NADP-isocitrate dehydrogenase expression regulate organic acid metabolism during nitrate assimilation in tobacco leaves. Plant Cell Environ 23:1155–1168

    Google Scholar 

  • Scott P, Kruger NJ (1995) Influence of elevated fructose-2,6-bisphosphate levels on starch mobilization in transgenic tobacco-leaves in the dark. Plant Physiol 108:1569–1577

    Google Scholar 

  • Scott P, Lange AJ, Kruger NJ (2000) Photosynthetic carbon metabolism in leaves of transgenic tobacco (Nicotiana tabacum L.) containing decreased amounts of fructose 2,6-bisphosphate. Planta 211:864–873

    Google Scholar 

  • Stitt M (1990) The flux of carbon between the chloroplast and the cytoplasm. In: Dennis DT, Turpin DH (eds) Advanced plant physiology: interaction and control of metabolism. Pitman, London, pp 319–340

    Google Scholar 

  • Stitt M, Fernie AR (2003) From measurements of metabolites to metabolomics: an ‘on the fly’ perspective illustrated by recent studies of carbon–nitrogen interactions. Curr Opin Biotech 14:136–144

    Google Scholar 

  • Strand A, Zrenner R, Trevanion S, Stitt M, Gustafsson P, Gardeström P (2000) Decreased expression of two key enzymes in the sucrose biosynthesis pathway, cytosolic fructose-1,6-bisphosphate and sucrose phosphate synthase, has remarkably different consequences for photosynthetic carbon metabolism in transgenic Arabidopsis thaliana. Plant J 23:759–770

    Article  CAS  PubMed  Google Scholar 

  • Thain SC, Murtas G, Lynn JR, McGrath RB, Millar AJ (2002) The circadian clock that controls gene expression is tissue specific. Plant Physiol 130:102–110

    Google Scholar 

  • Thimm O, Essigmann B, Kloska S, Altmann T, Buckhout TJ (2001) Response of Arabidopsis to iron deficiency stress as revealed by microarray analysis. Plant Physiol 127:1030–1043

    Google Scholar 

  • Thimm O, Blässing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914–939

    Google Scholar 

  • Trethewey RN, Krotzky AJ, Willmitzer L (1999) Metabolic profiling: a Rosetta Stone for genomics?. Curr Opin Plant Biol 2:83–85

    Google Scholar 

  • Urbanczyk-Wochniak E, Luedemann A, Kopka J, Selbig J, Roessner-Tunali U, Willmitzer L, Fernie AR (2003) Parallel analysis of transcript and metabolic profiles: a new approach in systems biology. EMBO Rep 4:989–993

    Google Scholar 

  • Van der Hoeven R, Ronning C, Giovannoni J, Martin G, Tanksley S (2002) Deductions about the number, organization, and evolution of genes in the tomato genome based on analysis of a large expressed sequence tag collection and selective genomic sequencing. Plant Cell 14:1441–1456

    PubMed  Google Scholar 

  • Weise SE, Weber AP, Sharkey TD (2004) Maltose is the major form of carbon exported from the chloroplast at night. Planta 218:474–482

    Article  CAS  PubMed  Google Scholar 

  • Winter H, Huber SC (2000) Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes. Crit Rev Biochem Mol 35:253–289

    CAS  PubMed  Google Scholar 

  • Zhu T (2003) Global analysis of gene expression using GeneChip microarrays. Curr Opin Plant Biol 6:418–425

    Google Scholar 

Download references

Acknowledgements

We thank Drs Helen Jenner and Natalia Palacios-Rojas for discussion on aspects of secondary metabolism. Equally deep discussion of various aspects of transcript data with Drs Oliver Bläsing and Oliver Thimm is gratefully acknowledged. We are also thankful to Helga Kulka for excellent care of the plants. LJS acknowledges the financial support of the BBSRC, UK. EU-W and ARF acknowledges the financial support of the Max Planck Society.

Author information

Authors and Affiliations

  1. Max-Planck-Institut für Molekulare Pflanzenphysiologie, Am Mühlenberg 1, 14476, Golm, Germany

    Ewa Urbanczyk-Wochniak, Anna Kolbe, Joachim Kopka & Alisdair R. Fernie

  2. Department of Plant Sciences, University of Oxford, South Parks Rd, Oxford, OX1 3RB, UK

    Charles Baxter & Lee J. Sweetlove

Authors
  1. Ewa Urbanczyk-Wochniak
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Charles Baxter
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anna Kolbe
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Joachim Kopka
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lee J. Sweetlove
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Alisdair R. Fernie
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alisdair R. Fernie.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Urbanczyk-Wochniak, E., Baxter, C., Kolbe, A. et al. Profiling of diurnal patterns of metabolite and transcript abundance in potato (Solanum tuberosum) leaves. Planta 221, 891–903 (2005). https://doi.org/10.1007/s00425-005-1483-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-005-1483-y

Keywords

Search

Navigation