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Energy signaling in the stress response

Final Report Summary - ESIS (Energy signaling in the stress response)

Abiotic stresses like cold, drought, salinity or floods are major determinants of crop loss. Regardless of their site and mode of perception, different types of stress often generate similar signals and downstream responses, resulting e. g. in overlapping patterns of gene expression. Energy deficiency is associated with many stress conditions due to their impact on photosynthesis and/or respiration. Using Arabidopsis thaliana as a model plant, we have recently shown that different types of stress do converge in an energy deficiency signal that is translated into a vast transcriptional response by two closely related protein kinases (PKs), KIN10 and KIN11, collectively known as SnRK1s. The SnRK1-mediated metabolic switch prevents cell death and promotes cell survival under adverse conditions by inhibiting major biosynthetic pathways and by promoting nutrient remobilisation. Intriguingly, disruption of SnRK1 signaling results in developmental alterations, suggesting that the function of these PKs is not the mere regulation of metabolism, but rather its integration with hormonal and environmental signals for optimising growth and development.

Despite the importance of the SnRK1 pathway for plant growth and acclimation, virtually nothing is known about how this pathway operates, and how energy-deficiency information is transduced into transcriptional changes and ultimately into long-term adaptation. To mitigate this, the goal of this project was to gain insight into the SnRK1 energy-signaling pathway through the characterisation of the underlying regulatory mechanisms and the identification of some of its upstream and downstream components.

Using a combination of cell-based assays, functional genomics, and transgenics approaches we have identified specific protein phosphatases that act as negative upstream regulators of SnRK1, providing insight on how the system is reset when the stress signal subsides. In addition, we have discovered a novel SnRK1 modification that may be involved in its subcellular localisation and/or activation by stress and downstream gene expression changes. Finally, we have found that part of the repression of gene expression exerted by SnRK1 is mediated by microRNAs (miRNAs). In depth analyses of specific miRNAs and their targets is helping us uncover new cellular processes that are under the regulation of the SnRK1 pathway.

Despite the obvious agricultural importance of stress and its socioeconomic implications, knowledge on the molecular mechanisms underlying stress tolerance is still rather limited. The finding that a common response to various stresses is partly triggered at the transcriptional level through the action of the SnRK1 energy sensors opened an exciting new direction of research. Given the impact of SnRK1 not only on stress tolerance, but also on plant architecture, flowering, senescence, and carbon allocation to seeds and tubers, this pathway can be considered a promising target for modulating plant development, growth and yield in an ever-changing environment. Therefore, understanding how it is regulated through mechanisms like the ones that are the focus of this work may facilitate the manipulation of this system and thereby the processes that are under its control. Aside from the agricultural implications a deeper understanding of the SnRK1 pathway may shine light on the amazing but elusive plasticity of plant development. Unraveling this energy signaling cascade will likely contribute to our understanding on how plants base their growth and developmental decisions on cues from the environment.

http://www.igc. gulbenkian. pt/research/unit/94 ebaena@igc. gulbenkian. pt