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

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Abstract

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.

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Abbreviations

Fv/Fm :

Maximum photosynthetic efficiency

HNG:

High nitrogen plus glucose

LN:

Low nitrogen

LNG:

Low nitrogen plus glucose

SAG:

Senescence-associated gene

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Acknowledgements

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.

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Authors and Affiliations

  1. Department of Biology, University College London, Gower Street, WC1E 6BT, London, UK

    Nathalie Pourtau, Richard Jennings, Elise Pelzer & Astrid Wingler

  2. Bloomsbury Centre for Bioinformatics, University College London, Gower Street, WC1E 6BT, London, UK

    Jacqueline Pallas

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  1. Nathalie Pourtau
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Correspondence to Astrid Wingler.

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Pourtau, N., Jennings, R., Pelzer, E. et al. Effect of sugar-induced senescence on gene expression and implications for the regulation of senescence in Arabidopsis . Planta 224, 556–568 (2006). https://doi.org/10.1007/s00425-006-0243-y

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