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Journal of Plant Research

, Volume 119, Issue 2, pp 115–123 | Cite as

Identification of sugar-modulated genes and evidence for in vivo sugar sensing in Arabidopsis

  • Silvia Gonzali
  • Elena Loreti
  • Cinzia Solfanelli
  • Giacomo Novi
  • Amedeo Alpi
  • Pierdomenico PerataEmail author
Regular Paper

Abstract

Sugar status regulates mechanisms controlling growth and development of plants. We studied the effects of sucrose at a genome-wide level in dark-grown 4-day-old Arabidopsis thaliana seedlings, identifying 797 genes strongly responsive to sucrose. Starting from the microarray analysis data, four up-regulated (At5g41670, At1g20950, At1g61800, and At2g28900) and four down-regulated (DIN6, At4g37220, At1g28330, and At1g74670) genes were chosen for further characterisation and as sugar sensing markers for in vivo analysis. The sugar modulation pattern of all eight genes was confirmed by real time RT-PCR analysis, revealing different concentration thresholds for sugar modulation. Finally, sugar-regulation of gene expression was demonstrated in vivo by using the starchless pgm mutant, which is unable to produce transitory starch. Sucrose-inducible genes are upregulated in pgm leaves at the end of a light treatment, when soluble sugars levels are higher than in the wild type. Conversely, sucrose-repressible genes show a higher expression at the end of the dark period in the mutant, when the levels of sugars in the leaf are lower. The results obtained indicate that the transcriptional response to exogenous sucrose allows the identification of genes displaying a pattern of expression in leaves compatible with their sugar-modulation in vivo.

Keywords

Arabidopsis thaliana Phosphoglucomutase mutant Sucrose Sugar sensing 

Supplementary material

Table S1

10265_2005_251_ESM_supp1.pdf (250 kb)
(PDF 250 KB)

Table S2

10265_2005_251_ESM_supp2.xls (16.4 mb)
(Excel 16.7 MB)

References

  1. Breton G, Danyluk J, Charron JB, Sarhan F (2003) Expression profiling and bioinformatic analyses of a novel stress-regulated multispanning transmembrane protein family from cereals and Arabidopsis. Plant Physiol 132:64–74CrossRefPubMedGoogle Scholar
  2. Caspar T, Huber SC, Somerville C (1985) Alterations in growth, photosynthesis, and respiration in a starchless mutant of Arabidopsis thaliana (L.) deficient in chloroplast phosphoglucomutase activity. Plant Physiol 79:11–17Google Scholar
  3. Coruzzi GM, Zhou L (2001) Carbon and nitrogen sensing and signaling in plants: emerging ‘matrix effects’. Curr Opin Plant Biol 4:247–253CrossRefPubMedGoogle Scholar
  4. Dijkwel PP, Kock PAM, Bezemer R, Weisbeek PJ, Smeekens SCM (1996) Sucrose represses the developmentally controlled transient activation of the plastocyanin gene in Arabidopsis thaliana seedlings. Plant Physiol 110:455–463PubMedGoogle Scholar
  5. 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
  6. Gazzarrini S, McCourt P (2003) Cross-talk in plant hormone signalling: what Arabidopsis mutants are telling us. Ann Bot 91:605–612CrossRefPubMedGoogle Scholar
  7. Gibon Y, Bläsing OE, Palacios-Rojas N, Pankovic D, Hendriks JHM, Fisahn J, Höhne M, Günther M, Stitt M (2004) Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-glucose pyrophosphorylase in the following light period. Plant J 39:847–862CrossRefPubMedGoogle Scholar
  8. Gibson SI (2004) Sugar and phytohormone response pathways: navigating a signalling network. J Exp Bot 55:253–264CrossRefPubMedGoogle Scholar
  9. Gibson SI (2005) Control of plant development and gene expression by sugar signaling. Curr Opin Plant Biol 8:93–102CrossRefPubMedGoogle Scholar
  10. Guglielminetti L, Perata P, Alpi A (1995) Effect of anoxia on carbohydrate metabolism in rice seedlings. Plant Physiol 108:735–741PubMedGoogle Scholar
  11. Halford NG, Paul MJ (2003) Carbon metabolite sensing and signaling. Plant Biotechnol J 1:381–398CrossRefGoogle Scholar
  12. Jang J-C, Sheen J (1994) Sugar sensing in higher plants. Plant Cell 6:1665–1679CrossRefPubMedGoogle Scholar
  13. Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol 47:509–540CrossRefPubMedGoogle Scholar
  14. Koch KE, Nolte KD, Duke ER, McCarty DR, Avigne WT (1992) Sugar levels modulate differential expression of maize sucrose synthase genes. Plant Cell 4:59–69CrossRefPubMedGoogle Scholar
  15. Lam HM, Peng SS, Coruzzi GM (1994) Metabolic regulation of the gene encoding glutamine-dependent asparagine synthetase in Arabidopsis thaliana. Plant Physiol 106:1347–1357CrossRefPubMedGoogle Scholar
  16. Lam HM, Coschigano K, Schultz C, Melo-Oliveira R, Tjaden G, Oliveira I, Ngai N, Hsieh MH, Coruzzi G (1995) Use of Arabidopsis mutants and genes to study amide amino acid biosynthesis. Plant Cell 7:887–898CrossRefPubMedGoogle Scholar
  17. Lam HM, Hsieh MH, Coruzzi G (1998) Reciprocal regulation of distinct asparagine synthetase genes by light and metabolites in Arabidopsis thaliana. Plant J 16:345–353CrossRefPubMedGoogle Scholar
  18. 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
  19. Loreti E, Alpi A, Perata P (2000) Glucose and disaccharide-sensing mechanisms modulate the expression of α-amylase in barley embryos. Plant Physiol 123:939–948CrossRefPubMedGoogle Scholar
  20. Loreti E, De Bellis L, Alpi A, Perata P (2001) Why and how plant cells sense sugars? Ann Bot 88:803–812CrossRefGoogle Scholar
  21. Loreti E, Poggi A, Novi G, Alpi A, Perata P (2005) A genome-wide analysis of the effects of sucrose on gene expression in Arabidopsis seedlings under anoxia. Plant Physiol 137:1130–1138CrossRefPubMedGoogle Scholar
  22. Mita S, Suzuki-Fujii K, Nakamura K (1995) Sugar-inducible expression of a gene for β-amylase in Arabidopsis thaliana. Plant Physiol 107:895–904CrossRefPubMedGoogle Scholar
  23. Oliveira IC, Coruzzi GM (1999) Carbon and amino acids reciprocally modulate the expression of glutamine synthetase in Arabidopsis. Plant Physiol 121:301–309CrossRefPubMedGoogle Scholar
  24. Price J, Laxmi A, St Martin SK, Jang J-C (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16:2128–2150CrossRefPubMedGoogle Scholar
  25. Roitsch T (1999) Source-sink regulation by sugar and stress. Curr Opin Plant Biol 2:198–206CrossRefPubMedGoogle Scholar
  26. Rolland F, Winderickx J, Thevelein JM (2002) Glucose-sensing and -signalling mechanisms in yeast. FEMS Yeast Res 2:183–201CrossRefPubMedGoogle Scholar
  27. Scholl RL, May ST, Ware DH (2000) Seed and molecular resources for Arabidopsis. Plant Physiol 124:1477–1480CrossRefPubMedGoogle Scholar
  28. Sinha AK, Hofmann MG, Romer U, Kockenberger W, Elling L, Roitsch T (2002) Metabolizable and non-metabolizable sugars activate different signal transduction pathways in tomato. Plant Physiol 128:1480–1489CrossRefPubMedGoogle Scholar
  29. Smeekens S (2000) Sugar-induced signal transduction in plants. Annu Rev Plant Physiol Plant Mol Biol 51:49–81CrossRefPubMedGoogle Scholar
  30. Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller 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 37:914–939CrossRefPubMedGoogle Scholar
  31. Thum KE, Shin MJ, Palenchar PM, Kouranov A, Coruzzi GM (2004) Genome-wide investigation of light and carbon signaling interactions in Arabidopsis. Genome Biol 5:R10CrossRefPubMedGoogle Scholar
  32. Umemura T, Perata P, Futsuhara Y, Yamaguchi J (1998) Sugar sensing and α-amylase gene repression in rice embryos. Planta 204:420–428CrossRefPubMedGoogle Scholar
  33. Villadsen D, Smith SM (2004) Identification of more than 200 glucose-responsive Arabidopsis genes none of which responds to 3-O-methylglucose or 6-deoxyglucose. Plant Mol Biol 55:467–477CrossRefPubMedGoogle Scholar
  34. Wingler A, Fritzius T, Wiemken A, Boller T, Aeschbacher RA (2000) Trehalose induces the ADP-glucose pyrophosphorylase gene, ApL3, and starch synthesis in Arabidopsis. Plant Physiol 124:105–114CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer-Verlag 2006

Authors and Affiliations

  • Silvia Gonzali
    • 1
  • Elena Loreti
    • 2
  • Cinzia Solfanelli
    • 1
  • Giacomo Novi
    • 1
  • Amedeo Alpi
    • 1
  • Pierdomenico Perata
    • 3
    Email author
  1. 1.Department of Crop Plant BiologyUniversity of PisaPisaItaly
  2. 2.Institute of Biology and Agricultural BiotechnologyCNRPisaItaly
  3. 3.Sant’Anna School of Advanced StudiesPisaItaly

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