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A central integrator of transcription networks in plant stress and energy signalling

Nature volume 448, pages 938–942 (2007)Cite this article

Abstract

Photosynthetic plants are the principal solar energy converter sustaining life on Earth. Despite its fundamental importance, little is known about how plants sense and adapt to darkness in the daily light–dark cycle, or how they adapt to unpredictable environmental stresses that compromise photosynthesis and respiration and deplete energy supplies. Current models emphasize diverse stress perception and signalling mechanisms1,2. Using a combination of cellular and systems screens, we show here that the evolutionarily conserved Arabidopsis thaliana protein kinases, KIN10 and KIN11 (also known as AKIN10/At3g01090 and AKIN11/At3g29160, respectively), control convergent reprogramming of transcription in response to seemingly unrelated darkness, sugar and stress conditions. Sensing and signalling deprivation of sugar and energy, KIN10 targets a remarkably broad array of genes that orchestrate transcription networks, promote catabolism and suppress anabolism. Specific bZIP transcription factors partially mediate primary KIN10 signalling. Transgenic KIN10 overexpression confers enhanced starvation tolerance and lifespan extension, and alters architecture and developmental transitions. Significantly, double kin10 kin11 deficiency abrogates the transcriptional switch in darkness and stress signalling, and impairs starch mobilization at night and growth. These studies uncover surprisingly pivotal roles of KIN10/11 in linking stress, sugar and developmental signals to globally regulate plant metabolism, energy balance, growth and survival. In contrast to the prevailing view that sucrose activates plant SnRK1s (Snf1-related protein kinases)3,4,5,6, our functional analyses of Arabidopsis KIN10/11 provide compelling evidence that SnRK1s are inactivated by sugars and share central roles with the orthologous yeast Snf1 and mammalian AMPK in energy signalling.

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Figure 1: DIN genes are activated by diverse stresses and repressed by sugars.
Figure 2: Convergent transcriptional control through a G-box and specific GBFs.
Figure 3: Global gene expression regulation by KIN10.
Figure 4: Role of KIN10 in plant development, stress responses and starch mobilization at night.

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Acknowledgements

We thank S. P. Dinesh-Kumar for generously sharing the TRV-based vectors and the VIGS protocol for Arabidopsis plants before publication, O. Thimm and M. Stitt for the MAPMAN program and the original functional classification files, J.C. Jang, S. Wu and D.C. Bassham for sharing the original GeneChip data, B. Wittner for consultation on the RankProd analysis, Q. Hall for the pQH29 RNAi vector, L. Zhou for the DIN6-LUC construct, L. Shan and P. He for the VIGS GFP control vector and the infiltration procedure, J. Bush for plant management, K. Chu for data analysis, and the Sheen laboratory members for stimulating discussions. The work was supported by grants from the National Science Foundation and National Institute of Health to J.S. F.R. was supported by a return grant from the Belgian Office for Scientific, Technical and Cultural Affairs and fellowships from the Belgian American Educational Foundation and the Research Foundation–Flanders (FWO–Vlaanderen).

All microarray data are available at the Gene Expression Array Omnibus website (http://www.ncbi.nlm.nih.gov/geo/) under accession numbers GSE8248 and GSE8257.

Author information

Author notes

  1. Elena Baena-González and Filip Rolland: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Genetics, and Department of Molecular Biology, Harvard Medical School, Massachusetts General Hospital, Boston Massachusetts 02114, USA,

    Elena Baena-González, Filip Rolland & Jen Sheen

  2. Department of Molecular Microbiology, VIB, B-3001 Leuven-Heverlee, Flanders, Belgium,

    Filip Rolland & Johan M. Thevelein

  3. Laboratory of Molecular Cell Biology, Institute of Botany and Microbiology, K.U.Leuven, Kasteelpark Arenberg 31, B-3001 Leuven-Heverlee, Flanders, Belgium,

    Filip Rolland & Johan M. Thevelein

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Correspondence to Elena Baena-González or Filip Rolland.

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Competing interests

All microarray data are available at the Gene Expression Array Omnibus website (http://www.ncbi.nlm.nih.gov/geo/) under accession numbers GSE8248 and GSE8257. Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Figures S1-S9 with Legends, Supplementary Tables S1-S7, Supplementary Methods and additional references. (PDF 7241 kb)

Supplementary Table S1

This file contains Supplementary Table S1 with global gene expression regulation by KIN10 and hypoxic conditions. Raw data. The document contains an Excel file with original unfiltered data from two biologically independent replicates of the KIN10 experiment and one hypoxia experiment (Affymetrix ATH1 Arabidopsis GeneChips) after data compilation and normalization using the GCOS v. 1.0 software. (XLS 17318 kb)

Supplementary Table S3

This file contains Supplementary Table S3 with global gene expression regulation by KIN10 (1021 genes). Data filtered as outlined in Supplementary Fig. S6). (XLS 389 kb)

Supplementary Table S4

This file contains Supplementary Table S4 with the transcriptional program induced by KIN10 markedly overlaps with that induced by starvation conditions and is antagonized by increased sugar availability (600 genes). The genes listed in Supplementary Table S3 were subjected to more stringent filtering by comparing their expression to published microarray datasets as explained in the text and outlined in Supplementary Fig. S6. (XLS 297 kb)

Supplementary Table S7

This file contains Supplementary Table S7 with sequences of primers used in this study. (XLS 28 kb)

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Baena-González, E., Rolland, F., Thevelein, J. et al. A central integrator of transcription networks in plant stress and energy signalling. Nature 448, 938–942 (2007). https://doi.org/10.1038/nature06069

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