Dynamic plastid redox signals integrate gene expression and metabolism to induce distinct metabolic states in photosynthetic acclimation in Arabidopsis

Publikation: Beitrag in FachzeitschriftArtikelForschungPeer-Review

Autoren

  • Katharina Bräutigam
  • Lars Dietzel
  • Tatjana Kleine
  • Elke Ströher
  • Dennis Wormuth
  • Karl-Josef Dietz
  • Dörte Radke
  • Markus Wirtz
  • Rüdiger Hell
  • Peter Dörmann
  • Adriano Nunes-Nesi
  • Nicolas Schauer
  • Alisdair R Fernie
  • Sandra N Oliver
  • Peter Geigenberger
  • Dario Leister
  • Thomas Pfannschmidt

Organisationseinheiten

Externe Organisationen

  • Friedrich-Schiller-Universität Jena
Forschungs-netzwerk anzeigen

Details

OriginalspracheEnglisch
Seiten (von - bis)2715-32
Seitenumfang18
FachzeitschriftThe plant cell
Jahrgang21
Ausgabenummer9
PublikationsstatusVeröffentlicht - Sept. 2009

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.

Zitieren

Dynamic plastid redox signals integrate gene expression and metabolism to induce distinct metabolic states in photosynthetic acclimation in Arabidopsis. / Bräutigam, Katharina; Dietzel, Lars; Kleine, Tatjana et al.
in: The plant cell, Jahrgang 21, Nr. 9, 09.2009, S. 2715-32.

Publikation: Beitrag in FachzeitschriftArtikelForschungPeer-Review

Bräutigam, K, Dietzel, L, Kleine, T, Ströher, E, Wormuth, D, Dietz, K-J, Radke, D, Wirtz, M, Hell, R, Dörmann, P, Nunes-Nesi, A, Schauer, N, Fernie, AR, Oliver, SN, Geigenberger, P, Leister, D & Pfannschmidt, T 2009, 'Dynamic plastid redox signals integrate gene expression and metabolism to induce distinct metabolic states in photosynthetic acclimation in Arabidopsis', The plant cell, Jg. 21, Nr. 9, S. 2715-32. https://doi.org/10.1105/tpc.108.062018
Bräutigam, K., Dietzel, L., Kleine, T., Ströher, E., Wormuth, D., Dietz, K.-J., Radke, D., Wirtz, M., Hell, R., Dörmann, P., Nunes-Nesi, A., Schauer, N., Fernie, A. R., Oliver, S. N., Geigenberger, P., Leister, D., & Pfannschmidt, T. (2009). Dynamic plastid redox signals integrate gene expression and metabolism to induce distinct metabolic states in photosynthetic acclimation in Arabidopsis. The plant cell, 21(9), 2715-32. https://doi.org/10.1105/tpc.108.062018
Bräutigam K, Dietzel L, Kleine T, Ströher E, Wormuth D, Dietz KJ et al. Dynamic plastid redox signals integrate gene expression and metabolism to induce distinct metabolic states in photosynthetic acclimation in Arabidopsis. The plant cell. 2009 Sep;21(9):2715-32. doi: 10.1105/tpc.108.062018
Bräutigam, Katharina ; Dietzel, Lars ; Kleine, Tatjana et al. / Dynamic plastid redox signals integrate gene expression and metabolism to induce distinct metabolic states in photosynthetic acclimation in Arabidopsis. in: The plant cell. 2009 ; Jahrgang 21, Nr. 9. S. 2715-32.
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title = "Dynamic plastid redox signals integrate gene expression and metabolism to induce distinct metabolic states in photosynthetic acclimation in Arabidopsis",
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.",
keywords = "Acclimatization/genetics, Arabidopsis/genetics, Gene Expression Profiling, Gene Expression Regulation, Plant, Light, Metabolome, Oxidation-Reduction, Photosynthesis, Plastids/metabolism, RNA, Plant/genetics, Signal Transduction",
author = "Katharina Br{\"a}utigam and Lars Dietzel and Tatjana Kleine and Elke Str{\"o}her and Dennis Wormuth and Karl-Josef Dietz and D{\"o}rte Radke and Markus Wirtz and R{\"u}diger Hell and Peter D{\"o}rmann and Adriano Nunes-Nesi and Nicolas Schauer and Fernie, {Alisdair R} and Oliver, {Sandra N} and Peter Geigenberger and Dario Leister and Thomas Pfannschmidt",
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journal = "The plant cell",
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T1 - Dynamic plastid redox signals integrate gene expression and metabolism to induce distinct metabolic states in photosynthetic acclimation in Arabidopsis

AU - Bräutigam, Katharina

AU - Dietzel, Lars

AU - Kleine, Tatjana

AU - Ströher, Elke

AU - Wormuth, Dennis

AU - Dietz, Karl-Josef

AU - Radke, Dörte

AU - Wirtz, Markus

AU - Hell, Rüdiger

AU - Dörmann, Peter

AU - Nunes-Nesi, Adriano

AU - Schauer, Nicolas

AU - Fernie, Alisdair R

AU - Oliver, Sandra N

AU - Geigenberger, Peter

AU - Leister, Dario

AU - Pfannschmidt, Thomas

PY - 2009/9

Y1 - 2009/9

N2 - 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.

AB - 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.

KW - Acclimatization/genetics

KW - Arabidopsis/genetics

KW - Gene Expression Profiling

KW - Gene Expression Regulation, Plant

KW - Light

KW - Metabolome

KW - Oxidation-Reduction

KW - Photosynthesis

KW - Plastids/metabolism

KW - RNA, Plant/genetics

KW - Signal Transduction

U2 - 10.1105/tpc.108.062018

DO - 10.1105/tpc.108.062018

M3 - Article

C2 - 19737978

VL - 21

SP - 2715

EP - 2732

JO - The plant cell

JF - The plant cell

SN - 1040-4651

IS - 9

ER -

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