Rapid Induction of Distinct Stress Responses after the Release of Singlet Oxygen in Arabidopsis Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.014662.

The conditional fluorescent (flu) mutant of Arabidopsis accumulates the photosensitizer protochlorophyllide in the dark. After a dark-to-light shift, the generation of singlet oxygen, a nonradical reactive oxygen species, starts within the first minute of illumination and was shown to be confined to plastids. Immediately after the shift, plants stopped growing and developed necrotic lesions. These early stress responses of the flu mutant do not seem to result merely from physicochemical damage. Peroxidation of chloroplast membrane lipids in these plants started rapidly and led to the transient and selective accumulation of a stereospecific and regiospecific isomer of hydroxyoctadecatrieonic acid, free (13S)-HOTE, that could be attributed almost exclusively to the enzymatic oxidation of linolenic acid. Within the first 15 min of reillumination, distinct sets of genes were activated that were different from those induced by superoxide/hydrogen peroxide. Collectively, these results demonstrate that singlet oxygen does not act primarily as a toxin but rather as a signal that activates several stress-response pathways. Its biological activity in Arabidopsis exhibits a high degree of specificity that seems to be derived from the chemical identity of this reactive oxygen species and/or the intracellular location at which it is generated.

[1]  D. Inzé,et al.  Specific checkpoints regulate plant cell cycle progression in response to oxidative stress , 1999 .

[2]  M. Timko,et al.  Chlorophyll biosynthesis from glutamate or 5-aminolevulinate in intact Euglena chloroplasts , 1985, Planta.

[3]  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.

[4]  E. Blée,et al.  Impact of phyto-oxylipins in plant defense. , 2002, Trends in plant science.

[5]  Ivo Feussner,et al.  The lipoxygenase pathway. , 2003, Annual review of plant biology.

[6]  A. Mehler.  Studies on reactions of illuminated chloroplasts. I. Mechanism of the reduction of oxygen and other Hill reagents. , 1951, Archives of biochemistry and biophysics.

[7]  R. Dixon,et al.  Reactive Oxygen Intermediates Mediate a Systemic Signal Network in the Establishment of Plant Immunity , 1998, Cell.

[8]  É. Hideg,et al.  Photoinhibition of photosynthesis in vivo results in singlet oxygen production detection via nitroxide-induced fluorescence quenching in broad bean leaves. , 1998, Biochemistry.

[9]  C. Ryan,et al.  Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[10]  A. Netting,et al.  pH, abscisic acid and the integration of metabolism in plants under stressed and non-stressed conditions: cellular responses to stress and their implication for plant water relations. , 2000, Journal of experimental botany.

[11]  K. Niyogi,et al.  PHOTOPROTECTION REVISITED: Genetic and Molecular Approaches. , 1999, Annual review of plant physiology and plant molecular biology.

[12]  K. Apel,et al.  Early Changes in Gene Expression during the Transition from Vegetative to Generative Growth in the Long-Day Plant Sinapis alba. , 1990, The Plant cell.

[13]  Paul G. Falkowski,et al.  Photoinhibition of Photosynthesis in Nature , 1994 .

[14]  K. Davies,et al.  Transient adaptation of oxidative stress in mammalian cells. , 1995, Archives of biochemistry and biophysics.

[15]  M. Rodgers,et al.  Current perspectives of singlet oxygen detection in biological environments. , 1992, Journal of photochemistry and photobiology. B, Biology.

[16]  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.

[17]  S. Ishiguro,et al.  The DEFECTIVE IN ANTHER DEHISCENCE1 Gene Encodes a Novel Phospholipase A1 Catalyzing the Initial Step of Jasmonic Acid Biosynthesis, Which Synchronizes Pollen Maturation, Anther Dehiscence, and Flower Opening in Arabidopsis , 2001, The Plant Cell Online.

[18]  J. Briat,et al.  Iron transport and storage in plants , 1997 .

[19]  É. Hideg,et al.  Detection of singlet oxygen and superoxide with fluorescent sensors in leaves under stress by photoinhibition or UV radiation. , 2002, Plant & cell physiology.

[20]  É. Hideg,et al.  Double (fluorescent and spin) sensors for detection of reactive oxygen species in the thylakoid membrane. , 1998, Free radical biology & medicine.

[21]  David B. Collinge,et al.  Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley—powdery mildew interaction , 1997 .

[22]  D. Tang,et al.  Fatty Acid Oxidation and Signaling in Apoptosis , 2002, Biological chemistry.

[23]  A. Girotti,et al.  Photosensitized oxidation of membrane lipids: reaction pathways, cytotoxic effects, and cytoprotective mechanisms. , 2001, Journal of photochemistry and photobiology. B, Biology.

[24]  A. Puga,et al.  Regulation of gene expression by reactive oxygen. , 1999, Annual review of pharmacology and toxicology.

[25]  C. Wasternack,et al.  Metabolic profiling of oxylipins in germinating cucumber seedlings – lipoxygenase-dependent degradation of triacylglycerols and biosynthesis of volatile aldehydes , 2002, Planta.

[26]  N. Baker,et al.  Imaging of photo-oxidative stress responses in leaves. , 2002, Journal of experimental botany.

[27]  A. Mehler,et al.  Studies on reactions of illuminated chloroplasts. II. Stimulation and inhibition of the reaction with molecular oxygen. , 1951, Archives of biochemistry and biophysics.

[28]  G. Fink,et al.  Plant growth homeostasis is controlled by the Arabidopsis BON1 and BAP1 genes. , 2001, Genes & development.

[29]  R. Tyrrell,et al.  Apoptosis, the Role of Oxidative Stress and the Example of Solar UV Radiation , 1999, Photochemistry and photobiology.

[30]  R. Burgess,et al.  Effect of dietary penicillin on liver vitamin A and serum carotenoids in the chick. , 1951, Archives of biochemistry and biophysics.

[31]  E. Elstner.  Mechanisms of oxygen activation in different compartments of plant cells , 1991 .

[32]  K. Apel,et al.  FLU: A negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[33]  J. Palta,et al.  Responses to abiotic stresses. , 1998 .

[34]  L. Klotz.  Oxidant-Induced Signaling: Effects of Peroxynitrite and Singlet Oxygen , 2002, Biological chemistry.

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

[36]  K. Apel,et al.  Identification of NADPH:Protochlorophyllide Oxidoreductases A and B: A Branched Pathway for Light-Dependent Chlorophyll Biosynthesis in Arabidopsis thaliana , 1995, Plant physiology.

[37]  F. Skoog,et al.  A revised medium for rapid growth and bio assays with tobacco tissue cultures , 1962 .

[38]  Y. Boo,et al.  Rice plants with a high protochlorophyllide accumulation show oxidative stress in low light that mimics water stress , 2000 .

[39]  B. C. Tripathy,et al.  Photodynamic herbicides. Recent developments and molecular basis of selectivity , 1988 .

[40]  C. Foote.  DEFINITION OF TYPE I and TYPE II PHOTOSENSITIZED OXIDATION , 1991, Photochemistry and photobiology.

[41]  C. Wasternack,et al.  Enzymatic and non-enzymatic lipid peroxidation in leaf development. , 2001, Biochimica et biophysica acta.

[42]  T. G. Truscott,et al.  Direct detection of singlet oxygen from isolated Photosystem II reaction centres , 1993 .

[43]  M. J. Terry,et al.  Holophytochrome assembly. Coupled assay for phytochromobilin synthase in organello. , 1991, The Journal of biological chemistry.

[44]  B. J. Deverall,et al.  Comparison of histological and physiological responses to Phakopsora pachyrhizi in resistant and susceptible soybean , 1980 .

[45]  M. Tsuyama,et al.  Trienoic Fatty Acids and Plant Tolerance of High Temperature , 2000 .

[46]  R. Crichton,et al.  Iron transport and storage. , 1987, European journal of biochemistry.

[47]  N. La Rocca,et al.  Amitrole treatment of etiolated barley seedlings leads to deregulation of tetrapyrrole synthesis and to reduced expression of Lhc and RbcS genes , 2001, Planta.

[48]  J. Pech,et al.  Improved Screening of cDNAs Generated by mRNA Differential Display Enables the Selection of True Positives and the Isolation of Weakly Expressed Messages , 1997, Plant Molecular Biology Reporter.

[49]  J. Piette,et al.  Non‐enzymatic triggering of the ceramide signalling cascade by solar UVA radiation , 2000, The EMBO journal.

[50]  Two Distinct Sources of Elicited Reactive Oxygen Species in Tobacco Epidermal Cells. , 1997, The Plant cell.

[51]  I. Adamska,et al.  Identification of genes expressed in response to light stress in leaves of Arabidopsis thaliana using RNA differential display. , 2001, European journal of biochemistry.

[52]  D. Inzé,et al.  The heat-shock element is a functional component of the Arabidopsis APX1 gene promoter. , 1998, Plant physiology.

[53]  J. Hancock,et al.  Hydrogen peroxide signalling. , 2002, Current opinion in plant biology.

[54]  Wilhelm Gruissem,et al.  Biochemistry & Molecular Biology of Plants , 2002 .

[55]  J. Dangl,et al.  Death Don't Have No Mercy: Cell Death Programs in Plant-Microbe Interactions. , 1996, The Plant cell.

[56]  K. Apel,et al.  Etioplast Differentiation in Arabidopsis: Both PORA and PORB Restore the Prolamellar Body and Photoactive Protochlorophyllide–F655 to the cop1 Photomorphogenic Mutant , 1998, Plant Cell.

[57]  J. Blein,et al.  Involvement of Lipoxygenase-dependent Production of Fatty Acid Hydroperoxides in the Development of the Hypersensitive Cell Death induced by Cryptogein on Tobacco Leaves* , 1999, The Journal of Biological Chemistry.

[58]  H. Teramoto,et al.  Correlated Changes in the Activity, Amount of Protein, and Abundance of Transcript of NADPH:Protochlorophyllide Oxidoreductase and Chlorophyll Accumulation during Greening of Cucumber Cotyledons , 1995, Plant physiology.

[59]  J. Briat,et al.  Structure and differential expression of the four members of the Arabidopsis thaliana ferritin gene family. , 2001, The Biochemical journal.