A Novel Mechanism of Nuclear Photosynthesis Gene Regulation by Redox Signals from the Chloroplast during Photosystem Stoichiometry Adjustment*

Photosynthetic organisms acclimate to long term changes in the environmental light quality by an adjustment of their photosystem stoichiometry to maintain photosynthetic efficiency. By using light sources that predominantly excite either photosystem I (PSI) or photosystem II (PSII), we studied the effects of excitation imbalances between both photosystems on nuclear PSI gene transcription in transgenic tobacco seedlings with promoter::β-glucuronidase gene fusions. Shifts from PSI to PSII light sources (and vice versa) induced changes in the reduction/oxidation state of intersystem redox components, and acclimation of tobacco seedlings to such changes were monitored by changes in chlorophyll a/b ratios andin vivo chlorophyll a fluorescence. The ferredoxin-NADP+-oxidoreductase gene promoter did not respond to these treatments, those from the genes for subunits PsaD and PsaF of PSI are activated by a reduction signal, and the plastocyanin promoter responded to both reduction and oxidation signals. Additional experiments with photosynthetic electron transport inhibitors 3-(3′,4′-dichlorophenyl)-1,1′-dimethyl urea and 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone demonstrated that the redox state of the plastoquinone pool controls the activity of the plastocyanin promoter, whereas subunit PsaD and PsaF gene transcription is regulated by other photosynthesis-derived signals. Thus, the expression of nuclear-encoded PSI genes is controlled by diverse light quality-dependent redox signals from the plastids during photosystem stoichiometry adjustment.

[1]  John F. Allen,et al.  Principles of redox control in photosynthesis gene expression , 2001 .

[2]  J. Chory,et al.  Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[3]  I. Graham,et al.  Plastid redox state and sugars: interactive regulators of nuclear-encoded photosynthetic gene expression. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[4]  S. G. Møller,et al.  A plastidic ABC protein involved in intercompartmental communication of light signaling. , 2001, Genes & development.

[5]  J Chory,et al.  Interactions between hy1 and gun mutants of Arabidopsis, and their implications for plastid/nuclear signalling. , 2000, The Plant journal : for cell and molecular biology.

[6]  J. Kropat,et al.  Chloroplast signalling in the light induction of nuclear HSP70 genes requires the accumulation of chlorophyll precursors and their accessibility to cytoplasm/nucleus. , 2000, The Plant journal : for cell and molecular biology.

[7]  T. Pfannschmidt,et al.  Balancing the two photosystems: photosynthetic electron transfer governs transcription of reaction centre genes in chloroplasts. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[8]  T. Pfannschmidt,et al.  Photosynthetic electron flow regulates transcription of the psaB gene in pea (Pisum sativum L.) chloroplasts through the redox state of the plastoquinone pool. , 2000, Plant & cell physiology.

[9]  Sjef Smeekens,et al.  SUGAR-INDUCED SIGNAL TRANSDUCTION IN PLANTS. , 2000, Annual review of plant physiology and plant molecular biology.

[10]  D. Kirilovsky,et al.  Redox control of psbA gene expression in the cyanobacterium Synechocystis PCC 6803. Involvement of the cytochrome b(6)/f complex. , 2000, Plant physiology.

[11]  M. W. Gray,et al.  Evolution of organellar genomes. , 1999, Current opinion in genetics & development.

[12]  J. Chory,et al.  The Phosphoenolpyruvate/Phosphate Translocator Is Required for Phenolic Metabolism, Palisade Cell Development, and Plastid-Dependent Nuclear Gene Expression , 1999, Plant Cell.

[13]  W. Whelan.  A Welcome to IUBMB Life , 1999 .

[14]  J. Sullivan,et al.  Plastid Translation Is Required for the Expression of Nuclear Photosynthesis Genes in the Dark and in Roots of the Pea lip1 Mutant , 1999, Plant Cell.

[15]  P. Mullineaux,et al.  Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. , 1999, Science.

[16]  A. Nilsson,et al.  Photosynthetic control of chloroplast gene expression , 1999, Nature.

[17]  Jan M. Anderson.  Insights into the consequences of grana stacking of thylakoid membranes in vascular plants: a personal perspective , 1999 .

[18]  R. Herrmann,et al.  Gene transfer from organelles to the nucleus: how much, what happens, and Why? , 1998, Plant physiology.

[19]  C. Gatz,et al.  Ferredoxin-1 mRNA is destabilized by changes in photosynthetic electron transport. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[20]  P. León,et al.  NUCLEAR CONTROL OF PLASTID AND MITOCHONDRIAL DEVELOPMENT IN HIGHER PLANTS. , 1998, Annual review of plant physiology and plant molecular biology.

[21]  M. Hasegawa,et al.  Gene transfer to the nucleus and the evolution of chloroplasts , 1998, Nature.

[22]  ASSESSING THE POTENTIAL FOR CHLOROPLAST REDOX REGULATION OF NUCLEAR GENE EXPRESSION , 1998 .

[23]  T. Pfannschmidt,et al.  The A and B forms of plastid DNA-dependent RNA polymerase from mustard (Sinapis alba L.) transcribe the same genes in a different developmental context , 1997, Molecular and General Genetics MGG.

[24]  W. F. Thompson,et al.  Light-regulated changes in abundance and polyribosome association of ferredoxin mRNA are dependent on photosynthesis. , 1997, The Plant cell.

[25]  P. Mullineaux,et al.  Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. , 1997, The Plant cell.

[26]  J. Chory,et al.  The co-ordination of nuclear and organellar genome expression in eukaryotic cells. , 1997, Essays in biochemistry.

[27]  R. Herrmann,et al.  Intron sequences are involved in the plastid- and light-dependent expression of the spinach PsaD gene. , 1996, The Plant journal : for cell and molecular biology.

[28]  P. Falkowski,et al.  Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[29]  M. Abo-El-Saad,et al.  A Rice Membrane Calcium-Dependent Protein Kinase Is Induced by Gibberellin , 1995, Plant physiology.

[30]  John F. Allen,et al.  Thylakoid protein phosphorylation, state 1-state 2 transitions, and photosystem stoichiometry adjustment: redox control at multiple levels of gene expression , 1995 .

[31]  R. Herrmann,et al.  Promoter and leader sequences of the spinach PsaD and PsaF genes direct an opposite light response in tobacco cotyledons: PsaD sequences downstream of the ATG codon are required for a positive light response. , 1994, The Plant journal : for cell and molecular biology.

[32]  Y. Jung,et al.  Mutational analysis of photosystem I polypeptides in Synechocystis sp. PCC 6803. Subunit requirements for reduction of NADP+ mediated by ferredoxin and flavodoxin. , 1994, The Journal of biological chemistry.

[33]  R. Herrmann,et al.  The Role of Plastids in the Expression of Nuclear Genes for Thylakoid Proteins Studied with Chimeric [beta]-Glucuronidase Gene Fusions , 1994, Plant physiology.

[34]  C. Lelong,et al.  Identification of the amino acids involved in the functional interaction between photosystem I and ferredoxin from Synechocystis sp. PCC 6803 by chemical cross-linking. , 1994, The Journal of biological chemistry.

[35]  M. Karas,et al.  Electron transfer from plastocyanin to photosystem I. , 1994, The EMBO journal.

[36]  R. Oelmüller,et al.  A 42 bp promoter fragment of the gene for subunit III of photosystem I (psaF) is crucial for its activity. , 1993, The Plant journal : for cell and molecular biology.

[37]  R. Ellis.  Chaperone function: cracking the second half of the genetic code , 1991 .

[38]  C. Luong,et al.  Maize Photosystem I : Identification of the Subunit which Binds Plastocyanin. , 1989, Plant physiology.

[39]  R. J. Porra,et al.  Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy , 1989 .

[40]  M. Hippler,et al.  Identification of the plastocyanin binding subunit of photosystem I , 1989 .

[41]  R. Oelmüller.  PHOTOOXIDATIVE DESTRUCTION OF CHLOROPLASTS AND ITS EFFECT ON NUCLEAR GENE EXPRESSION AND EXTRAPLASTIDIC ENZYME LEVELS * , 1989 .

[42]  J. Briantais,et al.  The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence , 1989 .

[43]  H. Sternbach,et al.  Tyrosyl‐tRNA synthetase from baker's yeast , 1988 .

[44]  U. Johanningmeier.  Possible control of transcript levels by chlorophyll precursors in Chlamydomonas. , 1988, European journal of biochemistry.

[45]  R. Malkin,et al.  Ferredoxin Cross-Links to a 22 kD Subunit of Photosystem I. , 1988, Plant physiology.

[46]  A. Trebst.  [65] Inhibitors in electron flow: Tools for the functional and structural localization of carriers and energy conservation sites , 1980 .

[47]  D. Arnon.  COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS. , 1949, Plant physiology.