Master Energy-Regulator Kinases in Plants

Abstract

Plants undergo dramatic changes in metabolism as environmental conditions change and stressful situations are encountered. Most obviously, anabolic processes that operate during the day, when photosynthesis is active, switch to catabolic ones at night, or when sugars are unavailable, or under stresses like exposure to herbicides or to excessive amounts of water. Baena-González et al . identify a pair of protein kinases that have a central role in orchestrating common cellular transcriptional responses to such diverse stimuli. Through analysis of public databases, the authors identified dark-induced ( DIN ) genes whose expression increased in plant cells exposed to dark but decreased after exposure to light or sugars. Experiments monitoring expression of a reporter gene designed from one of the DIN genes revealed sensitivity of the response to a protein kinase inhibitor. Taking cues from work on yeast and mammalian kinases that control metabolism, the authors focused on members of the Snf1-related kinase gene families, which are related to the yeast protein Snf1. Two such proteins, KIN10 and KIN11, activated expression of the DIN reporter when expressed in Arabidopsis leaves. Systematic mutagenesis of regulatory elements implicated a role for G-box binding factors in controlling the response of DIN genes to stress or to KIN10 or KIN11. The authors explored the global transcriptional response to expression of KIN10 with whole-genome GeneChips and identified more than 1000 genes with altered rates of transcription. Comparison to published gene expression patterns showed strong correlation of a subset of these genes with those regulated in plants deprived of sugar or energy. There were negative correlations with expression profiles from plants treated with sugars. A gene expression response highly correlated to that induced by KIN10 was also detected in protoplasts stressed by hypoxia. KIN10 activated (and sugars repressed) genes functioning in major catabolic pathways, whereas genes that promote energy consumption and anabolic processes were repressed in response to KIN10. The authors propose that Kin10 and Kin11 can thus be considered global regulators of primary and secondary metabolism and protein synthesis. The authors went on to generate whole Arabadopsis plants overexpressing KIN10 or depleted of the KIN10 and KIN11 proteins by RNAi. Expression of KIN10 enhanced survival of plants kept in sugar-free medium in the presence of low amounts of light. Overexpression of KIN10 slowed development and--reminiscent of caloric restriction in animals--delayed the onset of senescence. Depletion of KIN10 and KIN11 blocked the transcriptional changes normally associated with transition to dark or stressful conditions and suggested an additional role of the kinases in control of development and flowering. The authors propose that KIN10 and KIN11 may be, like AMPK (adenosine monophosphate-activated protein kinase) of mammals, central regulators of signaling that control energy homeostasis. E. Baena-González, F. Rolland, J. M. Thevelein, J. Sheen, A central integrator of transcription networks in plant stress and energy signaling. Nature 448 , 938-942 (2007). [PubMed]