Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool

Jean Michel Escoubas, Michael Lomas, Julie LaRoche, Paul Falkowski

Research output: Contribution to journalArticle

500 Citations (Scopus)

Abstract

The eukaryotic green alga Dunaliella tertiolecta acclimates to decreased growth irradiance by increasing cellular levels of light-harvesting chlorophyll protein complex apoproteins associated with photosystem II (LHCIIs), whereas increased growth irradiance elicits the opposite response. Nuclear run-on transcription assays and measurements of cab mRNA stability established that light intensity-dependent changes in LHCII are controlled at the level of transcription. cab gene transcription in high-intensity light was partially enhanced by reducing plastoquinone with 3-(3,4- dichlorophenyl)-1,1-dimethyl urea (DCMU), whereas it was repressed in low- intensity light by partially inhibiting the oxidation of plastoquinol with 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone (DBMIB). Uncouplers of photosynthetic electron transport and inhibition of water splitting had no effect on LHCII levels. These results strongly implicate the redox state of the plastoquinone pool in the chloroplast as a photon-sensing system that is coupled to the light-intensity regulation of nuclear-encoded cab gene transcription. The accumulation of cellular chlorophyll at low-intensity light can be blocked with cytoplasmically directed phosphatase inhibitors, such as okadaic acid, microcystin L-R, and tautomycin. Gel mobility-shift assays revealed that cells grown in high-intensity light contained proteins that bind to the promoter region of a cab gene carrying sequences homologous to higher plant light-responsive elements. On the basis of these experimental results, we propose a model for a light intensity signaling system where cab gene expression is reversibly repressed by a phosphorylated factor coupled to the redox status of plastoquinone through a chloroplast protein kinase.

Original languageEnglish (US)
Pages (from-to)10237-10241
Number of pages5
JournalProceedings of the National Academy of Sciences of the United States of America
Volume92
Issue number22
DOIs
StatePublished - Oct 24 1995

Fingerprint

Plastoquinone
Oxidation-Reduction
Light
Genes
Dibromothymoquinone
Light-Harvesting Protein Complexes
Chloroplast Proteins
Okadaic Acid
Chlorophyta
Apoproteins
Photosystem II Protein Complex
RNA Stability
Electrophoretic Mobility Shift Assay
Chloroplasts
Chlorophyll
Growth
Sequence Homology
Electron Transport
Photons
Phosphoric Monoester Hydrolases

All Science Journal Classification (ASJC) codes

  • General

Keywords

  • algae
  • phosphorylation
  • photoacclimation

Cite this

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abstract = "The eukaryotic green alga Dunaliella tertiolecta acclimates to decreased growth irradiance by increasing cellular levels of light-harvesting chlorophyll protein complex apoproteins associated with photosystem II (LHCIIs), whereas increased growth irradiance elicits the opposite response. Nuclear run-on transcription assays and measurements of cab mRNA stability established that light intensity-dependent changes in LHCII are controlled at the level of transcription. cab gene transcription in high-intensity light was partially enhanced by reducing plastoquinone with 3-(3,4- dichlorophenyl)-1,1-dimethyl urea (DCMU), whereas it was repressed in low- intensity light by partially inhibiting the oxidation of plastoquinol with 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone (DBMIB). Uncouplers of photosynthetic electron transport and inhibition of water splitting had no effect on LHCII levels. These results strongly implicate the redox state of the plastoquinone pool in the chloroplast as a photon-sensing system that is coupled to the light-intensity regulation of nuclear-encoded cab gene transcription. The accumulation of cellular chlorophyll at low-intensity light can be blocked with cytoplasmically directed phosphatase inhibitors, such as okadaic acid, microcystin L-R, and tautomycin. Gel mobility-shift assays revealed that cells grown in high-intensity light contained proteins that bind to the promoter region of a cab gene carrying sequences homologous to higher plant light-responsive elements. On the basis of these experimental results, we propose a model for a light intensity signaling system where cab gene expression is reversibly repressed by a phosphorylated factor coupled to the redox status of plastoquinone through a chloroplast protein kinase.",
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Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool. / Escoubas, Jean Michel; Lomas, Michael; LaRoche, Julie; Falkowski, Paul.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 92, No. 22, 24.10.1995, p. 10237-10241.

Research output: Contribution to journalArticle

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T1 - Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool

AU - Escoubas, Jean Michel

AU - Lomas, Michael

AU - LaRoche, Julie

AU - Falkowski, Paul

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N2 - The eukaryotic green alga Dunaliella tertiolecta acclimates to decreased growth irradiance by increasing cellular levels of light-harvesting chlorophyll protein complex apoproteins associated with photosystem II (LHCIIs), whereas increased growth irradiance elicits the opposite response. Nuclear run-on transcription assays and measurements of cab mRNA stability established that light intensity-dependent changes in LHCII are controlled at the level of transcription. cab gene transcription in high-intensity light was partially enhanced by reducing plastoquinone with 3-(3,4- dichlorophenyl)-1,1-dimethyl urea (DCMU), whereas it was repressed in low- intensity light by partially inhibiting the oxidation of plastoquinol with 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone (DBMIB). Uncouplers of photosynthetic electron transport and inhibition of water splitting had no effect on LHCII levels. These results strongly implicate the redox state of the plastoquinone pool in the chloroplast as a photon-sensing system that is coupled to the light-intensity regulation of nuclear-encoded cab gene transcription. The accumulation of cellular chlorophyll at low-intensity light can be blocked with cytoplasmically directed phosphatase inhibitors, such as okadaic acid, microcystin L-R, and tautomycin. Gel mobility-shift assays revealed that cells grown in high-intensity light contained proteins that bind to the promoter region of a cab gene carrying sequences homologous to higher plant light-responsive elements. On the basis of these experimental results, we propose a model for a light intensity signaling system where cab gene expression is reversibly repressed by a phosphorylated factor coupled to the redox status of plastoquinone through a chloroplast protein kinase.

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