The Rebeiz Foundation for Basic Research (RFFBR) Paper Award for 2009 has been awarded to Dr. Thomas Pfannschmidt and his colleagues: Katharina Brautigam, Lars Dietzel, Tatjana Kleine. Elke Stroher, Dennis Wormuth, Karl-Joseph Dietz, Dorte Radke, Markus Wirtz, Rudiger Hell, Peter Dormann, Adriano Nunes Nesi, Nicolas Schauer, Alisdair R. Fernie, Sandra, N. Oliver, Peter Geigenberger, and Dario Leister, for their paper entitled "Dynamic Plastid Redox Signals Integrate Gene Expression and Metabolism to Induce Distinct Metabolic States in Phptpsynthetic Acclimation in Arabidopsis”. The paper appeared in The Plant Cell, 21: 2715-2732(2009).
In dense plant population such as forests or crop fields strong and persistent light quality gradients occur. These cause excitation imbalances of the two photosystems and reduce photosynthetic efficiency. Plants developed acclimation mechanisms in which structural reconfigurations of the photosynthetic apparatus redistribute light energy between the photosystems and, by this means, restore photosynthetic efficiency. A long-term response (LTR) to light quality gradients is the adjustment of photosystem (PS) stoichiometry which requires a controlled change in the expression of both nuclear and chloroplast genes. This appears to be controlled and coordinated by redox signals from photosynthetic electron transport, i.e. from the plastoquinone pool. However, the kinetics of such signals and the adjustment of energetic and metabolic demands to the changes of the photosynthetic apparatus are currently poorly understood. Using a redox signalling system that is based on the preferential excitation of either Photosystem (PS) I or PSII (PSI- or PSII-light) the time-dependent impact of plastid redox signals on nuclear transcriptome and total metabolome of Arabidopsis thaliana was determined. We observed rapid (within a minute range) and dynamic changes in nuclear transcript accumulation resulting in differential and specific expression patterns for genes associated with photosynthesis and metabolism. Metabolite pools also exhibited dynamic changes and indicate readjustments between distinct metabolic states depending on the respective illumination condition. These states were termed metabolic state 1 and state 2 corresponding to the respective states of the light harvesting complexes of the photosynthetic apparatus upon state transitions. They reflect reallocation of energy resources in a defined and reversible manner, indicating that structural changes in the photosynthetic apparatus during LTR are additionally supported at the level of metabolism. Starch accumulation was found to be an effective reporter for these metabolic states displaying higher amounts under PSII- than under PSI-light. In the mutant stn7 lacking the important regulatory kinase STN7 these adjustments were abolished confirming that redox signals from photosynthesis are responsible for the observed changes. Suppression of these metabolic adjustments resulted in severe growth retardation in the mutant compared to wild-type plants grown in parallel demonstrating the importance of this acclimation mechanism. We propose that photosynthesis acts as an environmental sensor, producing retrograde redox signals that trigger two parallel adjustment loops. These loops coordinate photosynthesis and metabolism to adapt plant primary productivity to the environment.
In selecting this paper for the fourth RFFBR Paper Award, the Board of directors of the Rebeiz Foundation felt that the described work will greatly benefit other chloroplast researchers, and enhance our knowledge of the relationship of photosynthesis to other metabolic processes in the plant cell.