Dynamic Plastid Redox Signals Integrate Gene Expression and Metabolism to Induce Distinct Metabolic States in Photosynthetic Acclimation in Arabidopsis

Braeutigam K, Dietzel L, Kleine T, Stroeher E, Wormuth D, Dietz K-J, Radke D, Wirtz M, Hell R, Doermann P, Nunes-Nesi A, et al. (2009)
PLANT CELL 21(9): 2715-2732.

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Abstract
Plants possess acclimation responses in which structural reconfigurations adapt the photosynthetic apparatus to fluctuating illumination. Long-term acclimation involves changes in plastid and nuclear gene expression and is controlled by redox signals from photosynthesis. The kinetics of these signals and the adjustments of energetic and metabolic demands to the changes in the photosynthetic apparatus are currently poorly understood. Using a redox signaling system that preferentially excites either photosystem I or II, we measured the time-dependent impact of redox signals on the transcriptome and metabolome of Arabidopsis thaliana. We observed rapid 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. These states reflect reallocation of energy resources in a defined and reversible manner, indicating that structural changes in the photosynthetic apparatus during long-term acclimation are additionally supported at the level of metabolism. We propose that photosynthesis can act as an environmental sensor, producing retrograde redox signals that trigger two parallel adjustment loops that coordinate photosynthesis and metabolism to adapt plant primary productivity to the environment.
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Braeutigam K, Dietzel L, Kleine T, et al. Dynamic Plastid Redox Signals Integrate Gene Expression and Metabolism to Induce Distinct Metabolic States in Photosynthetic Acclimation in Arabidopsis. PLANT CELL. 2009;21(9):2715-2732.
Braeutigam, K., Dietzel, L., Kleine, T., Stroeher, E., Wormuth, D., Dietz, K. - J., Radke, D., et al. (2009). Dynamic Plastid Redox Signals Integrate Gene Expression and Metabolism to Induce Distinct Metabolic States in Photosynthetic Acclimation in Arabidopsis. PLANT CELL, 21(9), 2715-2732. doi:10.1105/tpc.108.062018
Braeutigam, K., Dietzel, L., Kleine, T., Stroeher, E., Wormuth, D., Dietz, K. - J., Radke, D., Wirtz, M., Hell, R., Doermann, P., et al. (2009). Dynamic Plastid Redox Signals Integrate Gene Expression and Metabolism to Induce Distinct Metabolic States in Photosynthetic Acclimation in Arabidopsis. PLANT CELL 21, 2715-2732.
Braeutigam, K., et al., 2009. Dynamic Plastid Redox Signals Integrate Gene Expression and Metabolism to Induce Distinct Metabolic States in Photosynthetic Acclimation in Arabidopsis. PLANT CELL, 21(9), p 2715-2732.
K. Braeutigam, et al., “Dynamic Plastid Redox Signals Integrate Gene Expression and Metabolism to Induce Distinct Metabolic States in Photosynthetic Acclimation in Arabidopsis”, PLANT CELL, vol. 21, 2009, pp. 2715-2732.
Braeutigam, K., Dietzel, L., Kleine, T., Stroeher, E., Wormuth, D., Dietz, K.-J., Radke, D., Wirtz, M., Hell, R., Doermann, P., Nunes-Nesi, A., Schauer, N., Fernie, A.R., Oliver, S.N., Geigenberger, P., Leister, D., Pfannschmidt, T.: Dynamic Plastid Redox Signals Integrate Gene Expression and Metabolism to Induce Distinct Metabolic States in Photosynthetic Acclimation in Arabidopsis. PLANT CELL. 21, 2715-2732 (2009).
Braeutigam, Katharina, Dietzel, Lars, Kleine, Tatjana, Stroeher, Elke, Wormuth, Dennis, Dietz, Karl-Josef, Radke, Doerte, Wirtz, Markus, Hell, Ruediger, Doermann, Peter, Nunes-Nesi, Adriano, Schauer, Nicolas, Fernie, Alisdair R., Oliver, Sandra N., Geigenberger, Peter, Leister, Dario, and Pfannschmidt, Thomas. “Dynamic Plastid Redox Signals Integrate Gene Expression and Metabolism to Induce Distinct Metabolic States in Photosynthetic Acclimation in Arabidopsis”. PLANT CELL 21.9 (2009): 2715-2732.
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Photosynthetic light reactions: integral to chloroplast retrograde signalling.
Gollan PJ, Tikkanen M, Aro EM., Curr. Opin. Plant Biol. 27(), 2015
PMID: 26318477
Metabolites and chloroplast retrograde signaling.
Chi W, Feng P, Ma J, Zhang L., Curr. Opin. Plant Biol. 25(), 2015
PMID: 25912815
Identification of Early Nuclear Target Genes of Plastidial Redox Signals that Trigger the Long-Term Response of Arabidopsis to Light Quality Shifts.
Dietzel L, Glaßer C, Liebers M, Hiekel S, Courtois F, Czarnecki O, Schlicke H, Zubo Y, Borner T, Mayer K, Grimm B, Pfannschmidt T., Mol Plant 8(8), 2015
PMID: 25778986
Let there be light: regulation of gene expression in plants.
Petrillo E, Godoy Herz MA, Barta A, Kalyna M, Kornblihtt AR., RNA Biol 11(10), 2014
PMID: 25590224
Metabolic control of redox and redox control of metabolism in plants.
Geigenberger P, Fernie AR., Antioxid. Redox Signal. 21(9), 2014
PMID: 24960279
Identification of target genes and transcription factors implicated in translation-dependent retrograde signaling in Arabidopsis.
Leister D, Romani I, Mittermayr L, Paieri F, Fenino E, Kleine T., Mol Plant 7(7), 2014
PMID: 24874869
The GUN4 protein plays a regulatory role in tetrapyrrole biosynthesis and chloroplast-to-nucleus signalling in Chlamydomonas reinhardtii.
Brzezowski P, Schlicke H, Richter A, Dent RM, Niyogi KK, Grimm B., Plant J. 79(2), 2014
PMID: 24861705
Induced deactivation of genes encoding chlorophyll biosynthesis enzymes disentangles tetrapyrrole-mediated retrograde signaling.
Schlicke H, Hartwig AS, Firtzlaff V, Richter AS, Glasser C, Maier K, Finkemeier I, Grimm B., Mol Plant 7(7), 2014
PMID: 24658417
Interaction between plastid and mitochondrial retrograde signalling pathways during changes to plastid redox status.
Blanco NE, Guinea-Diaz M, Whelan J, Strand A., Philos. Trans. R. Soc. Lond., B, Biol. Sci. 369(1640), 2014
PMID: 24591717
The essential role of sugar metabolism in the acclimation response of Arabidopsis thaliana to high light intensities.
Schmitz J, Heinrichs L, Scossa F, Fernie AR, Oelze ML, Dietz KJ, Rothbart M, Grimm B, Flugge UI, Hausler RE., J. Exp. Bot. 65(6), 2014
PMID: 24523502
Structural control of metabolic flux.
Sajitz-Hermstein M, Nikoloski Z., PLoS Comput. Biol. 9(12), 2013
PMID: 24367246
Photosynthetic acclimation responses of maize seedlings grown under artificial laboratory light gradients mimicking natural canopy conditions.
Hirth M, Dietzel L, Steiner S, Ludwig R, Weidenbach H, And JP, Pfannschmidt T., Front Plant Sci 4(), 2013
PMID: 24062753
Isochorismate synthase 1 is required for thylakoid organization, optimal plastoquinone redox status, and state transitions in Arabidopsis thaliana.
Gawronski P, Gorecka M, Bederska M, Rusaczonek A, Slesak I, Kruk J, Karpinski S., J. Exp. Bot. 64(12), 2013
PMID: 23956412
PGR5 ensures photosynthetic control to safeguard photosystem I under fluctuating light conditions.
Suorsa M, Grieco M, Jarvi S, Gollan PJ, Kangasjarvi S, Tikkanen M, Aro EM., Plant Signal Behav 8(1), 2013
PMID: 23221748
Expression of the chloroplast thioredoxins f and m is linked to short-term changes in the sugar and thiol status in leaves of Pisum sativum.
de Dios Barajas-Lopez J, Tezycka J, Travaglia CN, Serrato AJ, Chueca A, Thormahlen I, Geigenberger P, Sahrawy M., J. Exp. Bot. 63(13), 2012
PMID: 22791824
Defects in leaf carbohydrate metabolism compromise acclimation to high light and lead to a high chlorophyll fluorescence phenotype in Arabidopsis thaliana.
Schmitz J, Schottler MA, Krueger S, Geimer S, Schneider A, Kleine T, Leister D, Bell K, Flugge UI, Hausler RE., BMC Plant Biol. 12(), 2012
PMID: 22248311
Hypothesis: A binary redox control mode as universal regulator of photosynthetic light acclimation.
Brautigam K, Dietzel L, Pfannschmidt T., Plant Signal Behav 5(1), 2010
PMID: 20592819

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