Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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

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.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

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.

References

  1. Yamaguchi-Shinozaki, K. & Shinozaki, K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol. 57, 781–803 (2006)

    Article  CAS  Google Scholar 

  2. Hasegawa, P. M., Bressan, R. A., Zhu, J.-K. & Bohnert, H. J. Plant cellular and molecular responses to high salinity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 57, 463–499 (2000)

    Article  Google Scholar 

  3. Halford, N. G. et al. Metabolic signalling and carbon partitioning: role of Snf1-related (SnRK1) protein kinase. J. Exp. Bot. 54, 467–475 (2003)

    Article  CAS  Google Scholar 

  4. Bhalerao, R. P. et al. Regulatory interaction of PRL1 WD protein with Arabidopsis SNF1-like protein kinases. Proc. Natl Acad. Sci. USA 96, 5322–5327 (1999)

    Article  ADS  CAS  Google Scholar 

  5. Purcell, P. C., Smith, A. M. & Halford, N. G. Antisense expression of a sucrose non-fermenting-1-related protein kinase sequence in potato results in decreased expression of sucrose synthase in tubers and loss of sucrose-inducibility of sucrose synthase transcripts in leaves. Plant J. 14, 195–202 (1998)

    Article  CAS  Google Scholar 

  6. Tiessen, A. et al. Evidence that SNF1-related kinase and hexokinase are involved in separate sugar-signalling pathways modulating post-translational redox activation of ADP-glucose pyrophosphorylase in potato tubers. Plant J. 35, 490–500 (2003)

    Article  CAS  Google Scholar 

  7. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L. & Gruissem, W. GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621–2632 (2004)

    Article  CAS  Google Scholar 

  8. Fujiki, Y. et al. Dark-inducible genes from Arabidopsis thaliana are associated with leaf senescence and repressed by sugars. Physiol. Plant. 111, 345–352 (2001)

    Article  CAS  Google Scholar 

  9. Moore, B. et al. Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300, 332–336 (2003)

    Article  ADS  CAS  Google Scholar 

  10. Rolland, F., Baena-González, E. & Sheen, J. Sugar sensing and signaling in plants: conserved and novel Mechanisms. Annu. Rev. Plant Biol. 57, 675–709 (2006)

    Article  CAS  Google Scholar 

  11. Lin, J. F. & Wu, S. H. Molecular events in senescing Arabidopsis leaves. Plant J. 39, 612–628 (2004)

    Article  CAS  Google Scholar 

  12. Price, J., Laxmi, A., St Martin, S. K. & Jang, J. C. Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16, 2128–2150 (2004)

    Article  CAS  Google Scholar 

  13. Palenchar, P. M., Kouranov, A., Lejay, L. V. & Coruzzi, G. M. Genome-wide patterns of carbon and nitrogen regulation of gene expression validate the combined carbon and nitrogen (CN)-signaling hypothesis in plants. Genome Biol. 5, R91 (2004)

    Article  Google Scholar 

  14. Hardie, D. G., Carling, D. & Carlson, M. The AMP-activated/SNF1 protein kinase subfamily: metabolic sensors of the eukaryotic cell? Annu. Rev. Biochem. 67, 821–855 (1998)

    Article  CAS  Google Scholar 

  15. Kahn, B. B., Alquier, T., Carling, D. & Hardie, D. G. AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab. 1, 15–25 (2005)

    Article  CAS  Google Scholar 

  16. Jakoby, M. et al. bZIP transcription factors in Arabidopsis. Trends Plant Sci. 7, 106–111 (2002)

    Article  CAS  Google Scholar 

  17. Zhang, Y. et al. Expression of antisense SnRK1 protein kinase sequence causes abnormal pollen development and male sterility in transgenic barley. Plant J. 28, 431–441 (2001)

    Article  CAS  Google Scholar 

  18. Radchuk, R., Radchuk, V., Weschke, W., Borisjuk, L. & Weber, H. Repressing the expression of the SUCROSE NONFERMENTING-1-RELATED PROTEIN KINASE gene in pea embryo causes pleiotropic defects of maturation similar to an abscisic acid-insensitive phenotype. Plant Physiol. 140, 263–278 (2006)

    Article  CAS  Google Scholar 

  19. Bläsing, O. E. et al. Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell 17, 3257–3281 (2005)

    Article  Google Scholar 

  20. Buchanan-Wollaston, V. et al. Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J. 42, 567–585 (2005)

    Article  CAS  Google Scholar 

  21. Contento, A. L., Kim, S. J. & Bassham, D. C. Transcriptome profiling of the response of Arabidopsis suspension culture cells to Suc starvation. Plant Physiol. 135, 2330–2347 (2004)

    Article  CAS  Google Scholar 

  22. Thimm, O. et al. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 37, 914–939 (2004)

    Article  CAS  Google Scholar 

  23. Schluepmann, H., Pellny, T., van Dijken, A., Smeekens, S. & Paul, M. Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 100, 6849–6854 (2003)

    Article  ADS  CAS  Google Scholar 

  24. Gomez, L. D., Baud, S., Gilday, A., Li, Y. & Graham, I. A. Delayed embryo development in the ARABIDOPSIS TREHALOSE-6-PHOSPHATE SYNTHASE 1 mutant is associated with altered cell wall structure, decreased cell division and starch accumulation. Plant J. 46, 69–84 (2006)

    Article  CAS  Google Scholar 

  25. Sugden, C., Donaghy, P. G., Halford, N. G. & Hardie, D. G. Two SNF1-related protein kinases from spinach leaf phosphorylate and inactivate 3-hydroxy-3-methylglutaryl-coenzyme A reductase, nitrate reductase, and sucrose phosphate synthase in vitro. Plant Physiol. 120, 257–274 (1999)

    Article  CAS  Google Scholar 

  26. Kaiser, W. M. & Huber, S. C. Post-translational regulation of nitrate reductase: Mechanism, physiological relevance and environmental triggers. J. Exp. Bot. 52, 1981–1989 (2001)

    Article  CAS  Google Scholar 

  27. Li, Y. et al. Establishing glucose- and ABA-regulated transcription networks in Arabidopsis by microarray analysis and promoter classification using a Relevance Vector Machine. Genome Res. 16, 414–427 (2006)

    Article  CAS  Google Scholar 

  28. Burch-Smith, T. M., Schiff, M., Liu, Y. & Dinesh-Kumar, S. P. Efficient virus induced gene silencing in Arabidopsis thaliana. Plant Physiol. 142, 21–27 (2006)

    Article  CAS  Google Scholar 

  29. Thelander, M., Olsson, T. & Ronne, H. Snf1-related protein kinase 1 is needed for growth in a normal day–night light cycle. EMBO J. 23, 1900–1910 (2004)

    Article  CAS  Google Scholar 

  30. Smith, A. M., Zeeman, S. C. & Smith, S. M. Starch degradation. Annu. Rev. Plant Biol. 56, 73–98 (2005)

    Article  CAS  Google Scholar 

  31. Kovtun, Y., Chiu, W.-L., Zeng, W. & Sheen, J. Suppression of auxin signal transduction by a MAPK cascade in higher plants. Nature 395, 716–720 (1998)

    Article  ADS  CAS  Google Scholar 

  32. Kovtun, Y., Chiu, W.-L., Tena, G. & Sheen, J. Functional analysis of oxidative stress-activated MAPK cascade in plants. Proc. Natl Acad. Sci. USA 97, 2940–2945 (2000)

    Article  ADS  CAS  Google Scholar 

  33. Hwang, I. & Sheen, J. Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413, 383–389 (2001)

    Article  ADS  CAS  Google Scholar 

  34. Guo, Y., Halfter, U., Ishitani, M. & Zhu, J. K. Molecular characterization of functional domains in the protein kinase SOS2 that is required for plant salt tolerance. Plant Cell 13, 1383–1400 (2001)

    Article  CAS  Google Scholar 

  35. Boudsocq, M., Barbier-Brygoo, H. & Lauriere, C. Identification of nine sucrose nonfermenting 1-related protein kinases 2 activated by hyperosmotic and saline stresses in Arabidopsis thaliana. J. Biol. Chem. 279, 41758–41766 (2004)

    Article  CAS  Google Scholar 

  36. Lam, H. M., Peng, S. S. & Coruzzi, G. M. Metabolic regulation of the gene encoding glutamine-dependent asparagine synthetase in Arabidopsis thaliana. Plant Physiol. 106, 1347–1357 (1994)

    Article  CAS  Google Scholar 

  37. Sheen, J. Signal transduction in maize and Arabidopsis mesophyll protoplasts. Plant Physiol. 127, 1466–1475 (2001)

    Article  CAS  Google Scholar 

  38. Gonzali, S. et al. The use of microarrays to study the anaerobic response in Arabidopsis. Ann. Bot. (Lond.) 96, 661–668 (2005)

    Article  CAS  Google Scholar 

  39. Loreti, E., Poggi, A., Novi, G., Alpi, A. & Perata, P. A genome-wide analysis of the effects of sucrose on gene expression in Arabidopsis seedlings under anoxia. Plant Physiol. 137, 1130–1138 (2005)

    Article  CAS  Google Scholar 

  40. Cheng, S.-H., Sheen, J., Gerrish, C. & Bolwell, G. P. Molecular identification of phenylalanine ammonia-lyase as a substrate of a specific constitutively active Arabidopsis CDPK expressed in maize protoplasts. FEBS Lett. 503, 185–188 (2001)

    Article  CAS  Google Scholar 

  41. Huang, J. Z. & Huber, S. C. Phosphorylation of synthetic peptides by a CDPK and plant SNF1-related protein kinase. Influence of proline and basic amino acid residues at selected positions. Plant Cell Physiol. 42, 1079–1087 (2001)

    Article  CAS  Google Scholar 

  42. Liu, Y., Schiff, M. & Dinesh-Kumar, S. P. Virus-induced gene silencing in tomato. Plant J. 31, 777–786 (2002)

  43. Ryu, C. M. A. n. a. n. d. A., Kang, L. & Mysore, K. S. Agrodrench: a novel and effective agroinoculation method for virus-induced gene silencing in roots and diverse Solanaceous species. Plant J. 40, 322–331 (2004)

    Article  CAS  Google Scholar 

  44. Burch-Smith, T. M., Anderson, J. C., Martin, G. B. & Dinesh-Kumar, S. P. Applications and advantages of virus-induced gene silencing for gene function studies in plants. Plant J. 39, 734–746 (2004)

    Article  CAS  Google Scholar 

  45. Kötting, O. et al. Identification of a novel enzyme required for starch metabolism in Arabidopsis leaves. The phosphoglucan, water dikinase. Plant Physiol. 137, 242–52 (2005)

    Article  Google Scholar 

Download references

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

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Elena Baena-González or Filip Rolland.

Ethics declarations

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)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature06069

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing