Chloroplast redox control of nuclear gene expression--a new class of plastid signals in interorganellar communication.

Chloroplasts are genetically semiautonomous organelles that contain their own subset of 100-120 genes coding for chloroplast proteins, tRNAs, and rRNAs. However, the great majority of the chloroplast proteins are encoded in the nucleus and must be imported into the organelle after their translation in the cytosol. This arrangement requires a high degree of coordination between the gene expression machineries in chloroplasts and nucleus, which is achieved by a permanent exchange of information between both compartments. The existence of such coordinating signals has long been known; however, the underlying molecular mechanisms and signaling routes are not understood. The present data indicate that the expression of nuclear-encoded chloroplast proteins is coupled to the functional state of the chloroplasts. Photosynthesis, which is the major function of chloroplasts, plays a crucial role in this context. Changes in the reduction/oxidation (redox) state of components of the photosynthetic machinery act as signals, which regulate the expression of chloroplast proteins in both chloroplasts and nucleus and help to coordinate the expression both in compartments. Recent advances in understanding chloroplast redox regulation of nuclear gene expression are summarized, and the importance for intracellular signaling is discussed.

[1]  R. Oelmüller,et al.  Expression of nuclear genes as affected by treatments acting on the plastids , 1986, Planta.

[2]  I. Ohad,et al.  The redox state of the plastoquinone pool controls the level of the light-harvesting chlorophyll a/b binding protein complex II (LHC II) during photoacclimation , 2004, Photosynthesis Research.

[3]  R. Oelmüller,et al.  Photosynthetic Electron Transport Determines Nitrate Reductase Gene Expression and Activity in Higher Plants* , 2002, The Journal of Biological Chemistry.

[4]  S. Rodermel.  Pathways of plastid-to-nucleus signaling. , 2001, Trends in plant science.

[5]  R. Oelmüller,et al.  A Novel Mechanism of Nuclear Photosynthesis Gene Regulation by Redox Signals from the Chloroplast during Photosystem Stoichiometry Adjustment* , 2001, The Journal of Biological Chemistry.

[6]  C. Beck.  Signaling pathways in chloroplast-to-nucleus communication. , 2001, Protist.

[7]  J. Papenbrock,et al.  Regulatory network of tetrapyrrole biosynthesis – studies of intracellular signalling involved in metabolic and developmental control of plastids , 2001, Planta.

[8]  J. Hancock,et al.  Regulation of the Arabidopsis transcriptome by oxidative stress. , 2001, Plant physiology.

[9]  H. Scheller,et al.  Balance of power: a view of the mechanism of photosynthetic state transitions. , 2001, Trends in plant science.

[10]  J F Allen,et al.  Molecular recognition in thylakoid structure and function. , 2001, Trends in plant science.

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

[12]  F. J. Corpas,et al.  Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells. , 2001, Trends in plant science.

[13]  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.

[14]  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.

[15]  Cytoplasmic kinase and phosphatase activities can induce PsaF gene expression in the absence of functional plastids: evidence that phosphorylation/dephosphorylation events are involved in interorganellar crosstalk , 2001, Molecular Genetics and Genomics.

[16]  Gerhard Link.  Redox Regulation of Photosynthetic Genes , 2001 .

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

[18]  M. Furuya,et al.  Phytochrome regulation of nuclear gene expression in plants. , 2000, Seminars in cell & developmental biology.

[19]  P. Mullineaux,et al.  Are diverse signalling pathways integrated in the regulation of arabidopsis antioxidant defence gene expression in response to excess excitation energy? , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[20]  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.

[21]  Harry Smith,et al.  Phytochromes and light signal perception by plants—an emerging synthesis , 2000, Nature.

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

[23]  G. Tena,et al.  Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[24]  J. Chory,et al.  Light: an indicator of time and place. , 2000, Genes & development.

[25]  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.

[26]  S. Kay,et al.  Cryptochromes--bringing the blues to circadian rhythms. , 1999, Trends in cell biology.

[27]  A. Wellburn,et al.  Elevated Glutathione Biosynthetic Capacity in the Chloroplasts of Transgenic Tobacco Plants Paradoxically Causes Increased Oxidative Stress , 1999, Plant Cell.

[28]  M. Ahmad,et al.  Seeing the world in red and blue: insight into plant vision and photoreceptors. , 1999, Current opinion in plant biology.

[29]  Bruick,et al.  Light-activated translation of chloroplast mRNAs. , 1999, Trends in plant science.

[30]  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.

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

[32]  P. Quail,et al.  Signalling in light-controlled development. , 1999, Seminars in cell & developmental biology.

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

[34]  A. Batschauer.  Light perception in higher plants , 1999, Cellular and Molecular Life Sciences CMLS.

[35]  M. Takahashi,et al.  An Alternative Electron Transfer Pathway Mediated by Chloroplast Envelope , 1999 .

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

[37]  E. Huala,et al.  Blue-light photoreceptors in higher plants. , 1999, Annual review of cell and developmental biology.

[38]  J. Chory,et al.  New Arabidopsis cue mutants suggest a close connection between plastid- and phytochrome regulation of nuclear gene expression. , 1998, Plant physiology.

[39]  R. Dixon,et al.  Nitric oxide functions as a signal in plant disease resistance , 1998, Nature.

[40]  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.

[41]  M. Goldschmidt-Clermont.  Coordination of nuclear and chloroplast gene expression in plant cells. , 1998, International review of cytology.

[42]  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.

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

[44]  J. Dat,et al.  Hydrogen peroxide‐ and glutathione‐associated mechanisms of acclimatory stress tolerance and signalling , 1997 .

[45]  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.

[46]  N. Huner,et al.  Redox Regulation of Light-Harvesting Complex II and cab mRNA Abundance in Dunaliella salina , 1995, Plant physiology.

[47]  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.

[48]  B. Bruce,et al.  Biosynthesis of the chloroplast cytochrome b6f complex: studies in a photosynthetic mutant of Lemna. , 1991, The Plant cell.

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

[50]  W. Taylor.  Regulatory Interactions between Nuclear and Plastid Genomes , 1989 .

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