1. Department of Genetics, Harvard Medical School, and Department of Molecular Biology, Massachusetts General Hospital, Boston Massachusetts 02114, USA
2. Department of Molecular Microbiology, VIB, B-3001 Leuven-Heverlee, Flanders, Belgium
3. Laboratory of Molecular Cell Biology, Institute of Botany and Microbiology, K.U.Leuven, Kasteelpark Arenberg 31, B-3001 Leuven-Heverlee, Flanders, Belgium
4. These authors contributed equally to this work.

Correspondence to: Elena Baena-González^1,4Filip Rolland^1,2,3,4 Correspondence should be addressed to F.R. (Email: filip.rolland@bio.kuleuven.be) and requests for materials should be addressed to F.R. and E.B.-G. (Email: baena@molbio.mgh.harvard.edu).

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 mechanisms^{1, 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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