, Volume 224, Issue 3, pp 556–568 | Cite as

Effect of sugar-induced senescence on gene expression and implications for the regulation of senescence in Arabidopsis

  • Nathalie Pourtau
  • Richard Jennings
  • Elise Pelzer
  • Jacqueline Pallas
  • Astrid Wingler
Original Article


There has been some debate whether leaf senescence is induced by sugar starvation or by sugar accumulation. External supply of sugars has been shown to induce symptoms of senescence such as leaf yellowing. However, it was so far not clear if sugars have a signalling function during developmental senescence. Glucose and fructose accumulate strongly during senescence in Arabidopsis thaliana (L.) Heynh. leaves. Using Affymetrix GeneChip analysis we determined the effect of sugar-induced senescence on gene expression. Growth on glucose in combination with low nitrogen supply induced leaf yellowing and changes in gene expression that are characteristic of developmental senescence. Most importantly, the senescence-specific gene SAG12, which was previously thought to be sugar-repressible, was induced over 900-fold by glucose. Induction of SAG12, which is expressed during late senescence, demonstrates that processes characteristic for late stages are sugar-inducible. Two MYB transcription factor genes, PAP1 and PAP2, were identified as senescence-associated genes that are induced by glucose. Moreover, growth on glucose induced genes for nitrogen remobilisation that are typically enhanced during developmental senescence, including the glutamine synthetase gene GLN1;4 and the nitrate transporter gene AtNRT2.5. In contrast to wild-type plants, the hexokinase-1 mutant gin2-1 did not accumulate hexoses and senescence was delayed. Induction of senescence by externally supplied glucose was partially abolished in gin2-1, indicating that delayed senescence was a consequence of decreased sugar sensitivity. Taken together, our results show that Arabidopsis leaf senescence is induced rather than repressed by sugars.


Arabidopsis Glucose signalling Hexokinase-1 Nitrogen remobilisation SAG12 Senescence 



Maximum photosynthetic efficiency


High nitrogen plus glucose


Low nitrogen


Low nitrogen plus glucose


Senescence-associated gene



This work was financially supported by the Biotechnology and Biological Sciences Research Council, United Kingdom (research grant 31/P16341). We would like to thank Jen Sheen (Department of Molecular Biology, Massachusetts General Hospital) for providing the gin2-1 mutant, Vicky Buchanan-Wollaston (Warwick HRI, University of Warwick) for providing unpublished results, Céline Masclaux-Daubresse (Unité de Nutrition Azotée des Plantes, INRA Versailles) for helpful comments on nitrogen metabolism, Sarah Purdy (Department of Biology, University College London) for providing sugar data for plants grown on agar and the Nottingham Arabidopsis Stock Centre for conducting the Affymetrix GeneChip analysis.

Supplementary material


  1. Al-Shahrour F, Díaz-Uriarte R, Dopazo J (2004) FatiGO: a web tool for finding significant associations of Gene Ontology terms with groups of genes. Bioinformatics 20:578–580CrossRefPubMedGoogle Scholar
  2. Balibrea Lara ME, Gonzales Garcia MC, Fatima T, Ehneß R, Lee TK, Proels R, Tanner W, Roitsch T (2004) Extracellular invertase is an essential component of cytokinin-mediated delay of senescence. Plant Cell 16:1276–1287CrossRefPubMedGoogle Scholar
  3. Bernard WR, Matile P (1994) Differential expression of glutamine synthetase genes during the senescence of Arabidopsis thaliana rosette leaves. Plant Sci 98:7–14CrossRefGoogle Scholar
  4. Borevitz JO, Xia Y, Blount J, Dixon RA, Lamb C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12:2383–2393CrossRefPubMedGoogle Scholar
  5. Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Görlach J (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13:1499–1510CrossRefPubMedGoogle Scholar
  6. Brugière N, Dubois F, Masclaux C, Sangwan RS, Hirel B (2000) Immunolocalization of glutamine synthetase in senescing tobacco (Nicotiana tobacum L) leaves suggests that ammonia assimilation is progressively shifted to the mesophyll cytosol. Planta 211:519–527CrossRefPubMedGoogle Scholar
  7. Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, Lin JF, Wu SH, Swidzinski J, Ishizaki K, Leaver C (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J 42:567–585CrossRefPubMedGoogle Scholar
  8. Chen ZH, Walker RP, Acheson RM, Técsi LI, Wingler A, Lea PJ, Leegood RC (2000) Are isocitrate lyase and phosphoenolpyruvate carboxykinase involved in gluconeogenesis during senescence of barley leaves and cucumber cotyledons? Plant Cell Physiol 41:960–967CrossRefPubMedGoogle Scholar
  9. Chung BC, Lee SY, Oh SA, Rhew TH, Nam HG, Lee CH (1997) The promoter activity of sen1, a senescence-associated gene of Arabidopsis, is repressed by sugars. J Plant Physiol 151:339–345Google Scholar
  10. Dai N, Schaffer A, Petreikov M, Shahak Y, Giller Y, Ratner K, Levine A, Granot D (1999) Overexpression of Arabidopsis hexokinase in tomato plants inhibits growth, reduces photosynthesis, and induces rapid senescence. Plant Cell 11:1253–1266CrossRefPubMedGoogle Scholar
  11. Dekkers BJW, Schuurmans JAMJ, Smkeekens SCM (2004) Glucose delays seed germination in Arabidopsis thaliana. Planta 218:579–588CrossRefPubMedGoogle Scholar
  12. Diaz C, Purdy S, Christ A, Morot-Gaudry J-F, Wingler A, Masclaux-Daubresse C (2005) Characterization of markers to determine the extent and variability of leaf senescence in Arabidopsis thaliana: a metabolic profiling approach. Plant Physiol 138:898–908CrossRefPubMedGoogle Scholar
  13. van Doorn WG (2004) Is petal senescence due to sugar starvation? Plant Physiol 134:35–42CrossRefPubMedGoogle Scholar
  14. Fujiki Y, Yoshikawa Y, Sato T, Inada N, Ito M, Nishida I, Watanabe A (2001) Dark-inducible genes from Arabidopsis thaliana are associated with leaf senescence and repressed by sugars. Physiol Plant 111:345–352CrossRefPubMedGoogle Scholar
  15. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JYH, Zhang J (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5:R80CrossRefPubMedGoogle Scholar
  16. Halford NG, Hey S, Jhurreea D, Laurie S, McKibbin RS, Paul M, Zhang Y (2003) Metabolic signalling and carbon partitioning: role of Snf1-related (SnRK1) protein kinase. J Exp Bot 54:467–475CrossRefPubMedGoogle Scholar
  17. Hensel LL, Grbić V, Baumgarten DA, Bleecker AB (1993) Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues in Arabidopsis. Plant Cell 5:553–564CrossRefPubMedGoogle Scholar
  18. Herrero J, Valencia A, Dopazo J (2001) A hierarchical unsupervised growing neural network for clustering gene expression patterns. Bioinformatics 17:126–136CrossRefPubMedGoogle Scholar
  19. Howitz KT, Bitterman KJ, Cohen HY, Lamming DW, Lavu S, Wood JG, Zipkin RE, Chung P, Kisielewski A, Zhang LL, Scherer B, Sinclair DA (2003) Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 425:191–196CrossRefPubMedGoogle Scholar
  20. Jang JC, León P, Zhou L, Sheen J (1997) Hexokinase as a sugar sensor in higher plants. Plant Cell 9:5–19CrossRefPubMedGoogle Scholar
  21. Jongebloed U, Szederkényi J, Hartig K, Schobert C, Komor E (2004) Sequence of morphological and physiological events during natural ageing of a castor bean leaf: sieve tube occlusions and carbohydrate back-up precede chlorophyll degradation. Physiol Plant 120:338–346CrossRefPubMedGoogle Scholar
  22. Lee EJ, Koizumi N, Sano H (2004) Identification of genes that are up-regulated in concert during sugar depletion in Arabidopsis. Plant Cell Environ 27:337–345CrossRefGoogle Scholar
  23. Levey S, Wingler A (2005) Natural variation in the regulation of leaf senescence and relation to other traits in Arabidopsis. Plant Cell Environ 28:223–231CrossRefGoogle Scholar
  24. Lin SJ, Ford E, Haigis M, Liszt G, Guarente L (2004) Calorie restriction extends yeast life span by lowering the level of NADH. Genes Dev 18:12–16CrossRefPubMedGoogle Scholar
  25. Lloyd JC, Zakhleniuk OV (2004) Responses of primary and secondary metabolism to sugar accumulation revealed by microarray expression analysis of the Arabidopsis mutant, pho3. J Exp Bot 55:1221–1230CrossRefPubMedGoogle Scholar
  26. Logemann J, Schell J, Willmitzer L (1987) Improved method for the isolation of RNA from plant tissues. Anal Biochem 163:16–20CrossRefPubMedGoogle Scholar
  27. Lohman KN, Gan S, John MC, Amasino RM (1994) Molecular analysis of natural leaf senescence in Arabidopsis. Physiol Plant 92:322–328CrossRefGoogle Scholar
  28. Longo VD, Fabrizio P (2002) Regulation of longevity and stress resistance: a molecular strategy conserved from yeast to humans? Cell Mol Life Sci 59:903–908CrossRefPubMedGoogle Scholar
  29. Masclaux C, Valadier MH, Brugière N, Morot-Gaudry JF, Hirel B (2000) Characterization of the sink/source transition in tobacco (Nicotiana tabacum L) shoots in relation to nitrogen management and leaf senescence. Planta 211:510–518CrossRefPubMedGoogle Scholar
  30. 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 25:1451–1462CrossRefGoogle Scholar
  31. Matile P, Schellenberg M, Peisker C (1992) Production and release of a chlorophyll catabolite in isolated senescent chloroplasts. Planta 187:230–235CrossRefGoogle Scholar
  32. Miller JD, Arteca RN, Pell EJ (1999) Senescence-associated gene expression during ozone-induced leaf senescence in Arabidopsis. Plant Physiol 120:1015–1023CrossRefPubMedGoogle Scholar
  33. Moore B, Zhou L, Rolland F, Hall Q, Cheng WH, Liu YX, Hwang I, Jones T, Sheen J (2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300:332–336CrossRefPubMedGoogle Scholar
  34. Noh YS, Amasino RM (1999) Identification of a promoter region responsible for the senescence-specific expression of SAG12. Plant Mol Biol 41:181–194CrossRefPubMedGoogle Scholar
  35. Noodén LD, Hillsberg JW, Schneider MJ (1996) Induction of leaf senescence in Arabidopsis thaliana by long days through a light-dosage effect. Physiol Plant 96:491–495CrossRefGoogle Scholar
  36. Noodén LD, Guiamét JJ, John I (1997) Senescence mechanisms. Physiol Plant 101:746–753CrossRefGoogle Scholar
  37. Oh SA, Lee SY, Chung IK, Lee CH, Nam HG (1996) A senescence-associated gene of Arabidopsis thaliana is distinctively regulated during natural and artificially induced leaf senescence. Plant Mol Biol 30:739–754CrossRefPubMedGoogle Scholar
  38. Okamoto M (2003) Regulation of NRT1 and NRT2 gene families of Arabidopsis thaliana: responses to nitrate provision. Plant Cell Physiol 44:304–317CrossRefPubMedGoogle Scholar
  39. Orsel M, Eulenburg K, Krapp A, Daniel-Vedele F (2004) Disruption of the nitrate transporter genes AtNRT2.1 and AtNRT2.2 restricts growth at low external nitrate concentration. Planta 219:714–721CrossRefPubMedGoogle Scholar
  40. Paul MJ, Pellny TK (2003) Carbon metabolite feedback regulation of leaf photosynthesis and development. J Exp Bot 54:539–547CrossRefPubMedGoogle Scholar
  41. Pourtau N, Marès M, Purdy S, Quentin N, Ruël A, Wingler A (2004) Interactions of abscisic acid and sugar signalling in the regulation of leaf senescence. Planta 219:765–772 CrossRefPubMedGoogle Scholar
  42. Price J, Li T-C, Kang SG, Na JK, Jang JC (2003) Mechanisms of glucose signalling during germination of Arabidopsis. Plant Physiol 132:1424–1438CrossRefPubMedGoogle Scholar
  43. Quirino BF, Reiter WD, Amasino RM (2001) One of two tandem Arabidopsis genes homologous to monosaccharide transporters is senescence-associated. Plant Mol Biol 46:447–457CrossRefPubMedGoogle Scholar
  44. Rolland F, Moore B, Sheen J (2002) Sugar sensing and signaling in plants. Plant Cell 14:S185–S205PubMedGoogle Scholar
  45. Rossato L, Lainé P, Ourry A (2001) Nitrogen storage and remobilization in Brassica napus L during the growth cycle: nitrogen fluxes within the plant and changes in soluble protein patterns. J Exp Bot 52:1655–1663CrossRefPubMedGoogle Scholar
  46. Scheible W-R, Morcuende R, Czechowski T, Fritz C, Osuna D, Palacios-Rojas N, Schindelasch D, Thimm O, Udvardi MK, Stitt M (2004) Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol 136:2483–2499CrossRefPubMedGoogle Scholar
  47. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Schölkopf B, Weigel D, Lohmann J (2005) A gene expression map of Arabidopsis thaliana development. Nature Gen 37:501–506CrossRefPubMedGoogle Scholar
  48. Smyth GK (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Gen Mol Biol 3: No. 1, Article 3Google Scholar
  49. Stessman D, Miller A, Spalding M, Rodermel S (2002) Regulation of photosynthesis during Arabidopsis leaf development in continuous light. Photosynth Res 72:27–37CrossRefPubMedGoogle Scholar
  50. Stitt M, Lilley RMC, Gerhardt R, Heldt HW (1989) Metabolite levels in specific cells and subcellular compartments of plant leaves. Methods Enzymol 174:518–552CrossRefGoogle Scholar
  51. Teng S, Keurentjes J, Bentsink L, Koornneef M, Smeekens S (2005) Sucrose-specific induction of anthocyanin biosynthesis in Arabidopsis requires the MYB75/PAP1 Gene. Plant Physiol 139:1840–1852CrossRefPubMedGoogle Scholar
  52. Tercé-Laforgue T, Mäck G, Hirel B (2004) New insights towards the function of glutamate dehydrogenase revealed during source-sink transition of tobacco (Nicotiana tabacum) plants grown under different nitrogen regimes. Physiol Plant 120:220–228CrossRefPubMedGoogle Scholar
  53. Wanner L, Keller F, Matile P (1991) Metabolism of radiolabelled galactolipids in senescent barley leaves. Plant Sci 78: 199–206CrossRefGoogle Scholar
  54. Weaver LM, Amasino RM (2001) Senescence is induced in individually darkened Arabidopsis leaves, but inhibited in whole darkened plants. Plant Physiol 127:876–886CrossRefPubMedGoogle Scholar
  55. Weaver LM, Gan S, Quirino B, Amasino RM (1998) A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. Plant Mol Biol 37:455–469CrossRefPubMedGoogle Scholar
  56. Wingler A, von Schaewen A, Leegood RC, Lea PJ, Quick WP (1998) Regulation of leaf senescence by cytokinin, sugars, and light effects on NADH-dependent hydroxypyruvate reductase. Plant Physiol 116:329–335CrossRefGoogle Scholar
  57. Wingler A, Marès M, Pourtau N (2004) Spatial patterns and metabolic regulation of photosynthetic parameters during leaf senescence. New Phytol 161:781–789CrossRefGoogle Scholar
  58. Wingler A, Purdy S, MacLean JA, Pourtau N (2006) The role of sugars in integrating environmental signals during the regulation of leaf senescence. J Exp Bot 57: 391–399CrossRefPubMedGoogle Scholar
  59. Wu Z, Irizarry RA, Gentleman R, Martinez-Murillo F, Spencer F (2004) A model-based background adjustment for oligonucleotide expression arrays. J Am Stat Assoc 99:909–917CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Nathalie Pourtau
    • 1
  • Richard Jennings
    • 1
  • Elise Pelzer
    • 1
  • Jacqueline Pallas
    • 2
  • Astrid Wingler
    • 1
  1. 1.Department of BiologyUniversity College LondonLondonUK
  2. 2.Bloomsbury Centre for BioinformaticsUniversity College LondonLondonUK

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