Systemic and Intracellular Responses to Photooxidative Stress in Arabidopsis[W]

As the sun tracks daily through the sky from east to west, different parts of the canopy are exposed to high light (HL). The extent of and mechanisms by which a systemic acquired acclimation (SAA) response might preacclimate shaded leaves that will be subsequently exposed to full sunlight is largely undefined. We investigated the role of an Arabidopsis thaliana zinc finger transcription factor, ZAT10, in SAA. ZAT10 overexpression resulted in enhanced tolerance to photoinhibitory light and exogenous H2O2, increased expression of antioxidative genes whose products are targeted to multiple subcellular compartments. Partial HL exposure of a leaf or leaves rapidly induced ZAT10 mRNA in distal, shaded photosynthetic tissues, including the floral stem, cauline leaves, and rosette, but not in roots. Fully 86% of fivefold HL-upregulated and 71% of HL-downregulated genes were induced and repressed, respectively, in distal, shaded leaves. Between 15 and 23% of genes whose expression changed in the HL and/or distal tissues were coexpressed in the ZAT10 overexpression plants, implicating ZAT10 in modulating the expression of SAA-regulated genes. The SAA response was detectable in plants with mutations in abscisic acid, methyl jasmonate, or salicylic acid synthesis or perception, and systemic H2O2 diffusion was not detected. Hence, SAA is distinct from pathogen-stimulated systemic acquired resistance and apparently involves a novel signal or combination of signals that preacclimate photosynthetic tissues to HL.

[1]  Ho Bang Kim,et al.  A knock-out mutation in allene oxide synthase results in male sterility and defective wound signal transduction in Arabidopsis due to a block in jasmonic acid biosynthesis. , 2002, The Plant Journal.

[2]  W. Kao,et al.  The effects of nitrogen, light and water availability on tropic leaf movements in soybean (Glycine max) , 1991 .

[3]  S. V. Caemmerer,et al.  Rubisco: Physiology in vivo , 2000 .

[4]  Y. Sakihama,et al.  Bleaching of the red anthocyanin induced by superoxide radical. , 1996, Archives of biochemistry and biophysics.

[5]  M. Grant,et al.  Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates , 2007, Proceedings of the National Academy of Sciences.

[6]  Murray Grant,et al.  Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease , 2007, The EMBO journal.

[7]  S. Driscoll,et al.  Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration? , 2002, Annals of botany.

[8]  K. Kazan Negative regulation of defence and stress genes by EAR-motif-containing repressors. , 2006, Trends in plant science.

[9]  S. Clough,et al.  Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

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

[11]  K. Shinozaki,et al.  The effect of overexpression of two Brassica CBF/DREB1-like transcription factors on photosynthetic capacity and freezing tolerance in Brassica napus. , 2005, Plant & cell physiology.

[12]  J. BENNETT,et al.  Phosphorylation of chloroplast membrane polypeptides , 1977, Nature.

[13]  Jian-Kang Zhu,et al.  Gain‐ and loss‐of‐function mutations in Zat10 enhance the tolerance of plants to abiotic stress , 2006, FEBS letters.

[14]  K. Hiratsu,et al.  Repression Domains of Class II ERF Transcriptional Repressors Share an Essential Motif for Active Repression , 2001, The Plant Cell Online.

[15]  E. Grill,et al.  A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. , 1994, Science.

[16]  D. R. Hoagland,et al.  The Water-Culture Method for Growing Plants Without Soil , 2018 .

[17]  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 .

[18]  K. Kloppstech,et al.  The protective functions of carotenoid and flavonoid pigments against excess visible radiation at chilling temperature investigated in Arabidopsisnpq and tt mutants , 2001, Planta.

[19]  R. Mittler,et al.  The Water-Water Cycle Is Essential for Chloroplast Protection in the Absence of Stress* , 2003, Journal of Biological Chemistry.

[20]  B. Pogson,et al.  Antisense inhibition of the beta-carotene hydroxylase enzyme in Arabidopsis and the implications for carotenoid accumulation, photoprotection and antenna assembly , 2004, Photosynthesis Research.

[21]  Xinnian Dong,et al.  Characterization of an Arabidopsis Mutant That Is Nonresponsive to Inducers of Systemic Acquired Resistance. , 1994, The Plant cell.

[22]  K. Gould,et al.  Do anthocyanins function as antioxidants in leaves? Imaging of H2O2 in red and green leaves after mechanical injury , 2002 .

[23]  M. Ohta,et al.  LOS2, a genetic locus required for cold‐responsive gene transcription encodes a bi‐functional enolase , 2002, The EMBO journal.

[24]  R. Ugalde,et al.  Thylakoid-Bound Ascorbate Peroxidase Mutant Exhibits Impaired Electron Transport and Photosynthetic Activity1 , 2003, Plant Physiology.

[25]  P. Mullineaux,et al.  A mutation affecting ASCORBATE PEROXIDASE 2 gene expression reveals a link between responses to high light and drought tolerance. , 2006, Plant, cell & environment.

[26]  C. Pieterse,et al.  A Novel Signaling Pathway Controlling Induced Systemic Resistance in Arabidopsis , 1998, Plant Cell.

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

[28]  J. Chory,et al.  Genetic interactions between phytochrome A, phytochrome B, and cryptochrome 1 during Arabidopsis development. , 1998, Plant physiology.

[29]  J. Allen How does protein phosphorylation regulate photosynthesis? , 1992, Trends in biochemical sciences.

[30]  D. von Wettstein,et al.  Chlorophyll Biosynthesis. , 1995, The Plant cell.

[31]  Ping Xu,et al.  Computational Estimation and Experimental Verification of Off-Target Silencing during Posttranscriptional Gene Silencing in Plants1[W][OA] , 2006, Plant Physiology.

[32]  P. Mullineaux,et al.  Control of Ascorbate Peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organisation of Arabidopsis leaves. , 2003, The Plant journal : for cell and molecular biology.

[33]  S. Wand,et al.  Anthocyanins in vegetative tissues: a proposed unified function in photoprotection. , 2002, The New phytologist.

[34]  B. Demmig‐Adams,et al.  Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among higher plant species , 1996, Planta.

[35]  P. Hasegawa,et al.  Genes that are uniquely stress regulated in salt overly sensitive (sos) mutants. , 2001, Plant physiology.

[36]  M. Geisler,et al.  A universal algorithm for genome-wide in silicio identification of biologically significant gene promoter putative cis-regulatory-elements; identification of new elements for reactive oxygen species and sucrose signaling in Arabidopsis. , 2006, The Plant journal : for cell and molecular biology.

[37]  Viswanathan Chinnusamy,et al.  Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. , 2003, Journal of experimental botany.

[38]  D. J. Widgery,et al.  From laboratory to field , 2003 .

[39]  B. Pogson,et al.  Chlorophyll Biosynthesis. Expression of a Second Chl I Gene of Magnesium Chelatase in Arabidopsis Supports Only Limited Chlorophyll Synthesis1 , 2002, Plant Physiology.

[40]  T. Sakurai,et al.  Identification of Arabidopsis Genes Regulated by High Light–Stress Using cDNA Microarray¶ , 2003, Photochemistry and photobiology.

[41]  K. Niyogi,et al.  Altered xanthophyll compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutants. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[42]  M. Thomashow,et al.  Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. , 2004, The Plant journal : for cell and molecular biology.

[43]  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.

[44]  B. Pogson,et al.  Improved survival of very high light and oxidative stress is conferred by spontaneous gain-of-function mutations in Chlamydomonas. , 2005, Biochimica et biophysica acta.

[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]  C. Foyer,et al.  Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria , 2003 .

[47]  Martin J. Mueller,et al.  NPR1 Modulates Cross-Talk between Salicylate- and Jasmonate-Dependent Defense Pathways through a Novel Function in the Cytosol Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.009159. , 2003, The Plant Cell Online.

[48]  R. Mittler,et al.  Reactive oxygen gene network of plants. , 2004, Trends in plant science.

[49]  G. Farquhar,et al.  Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves , 1981, Planta.

[50]  J. Giraudat,et al.  Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. , 1994, Science.

[51]  A. V. Arnim,et al.  The Early Dark-Response in Arabidopsis thaliana Revealed by cDNA Microarray Analysis , 2006, Plant Molecular Biology.

[52]  B. Pogson,et al.  Comparative proteomics of high light stress in the model alga Chlamydomonas reinhardtii , 2006, Proteomics.

[53]  Peter M Waterhouse,et al.  RNA silencing platforms in plants , 2005, FEBS letters.

[54]  R. Mittler,et al.  Abiotic stress, the field environment and stress combination. , 2006, Trends in plant science.

[55]  J. Ryals,et al.  Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[56]  Thomas D. Schmittgen,et al.  Effect of experimental treatment on housekeeping gene expression: validation by real-time, quantitative RT-PCR. , 2000, Journal of biochemical and biophysical methods.

[57]  P. Mullineaux,et al.  Evidence for a Direct Link between Glutathione Biosynthesis and Stress Defense Gene Expression in Arabidopsisw⃞ , 2004, The Plant Cell Online.

[58]  M. Pfaffl,et al.  A new mathematical model for relative quantification in real-time RT-PCR. , 2001, Nucleic acids research.

[59]  J. Micol,et al.  The Short-Chain Alcohol Dehydrogenase ABA2 Catalyzes the Conversion of Xanthoxin to Abscisic Aldehyde Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.002477. , 2002, The Plant Cell Online.

[60]  B. Pogson,et al.  Vitamin synthesis in plants: tocopherols and carotenoids. , 2006, Annual review of plant biology.

[61]  John D. Storey,et al.  Statistical significance for genomewide studies , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[62]  M. Iwabuchi,et al.  Expression of a subset of the Arabidopsis Cys(2)/His(2)-type zinc-finger protein gene family under water stress. , 2000, Gene.

[63]  C. Foyer Prospects for enhancement of the soluble antioxidants, ascorbate and glutathione , 2001, BioFactors.

[64]  G. Wagner Content and vacuole/extravacuole distribution of neutral sugars, free amino acids, and anthocyanin in protoplasts. , 1979, Plant physiology.

[65]  S. Merlot,et al.  The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. , 1997, The Plant cell.

[66]  B. Pogson,et al.  Global Changes in Gene Expression in Response to High Light in Arabidopsis1,212 , 2002, Plant Physiology.

[67]  M. Merzlyak,et al.  Light-stress-induced pigment changes and evidence for anthocyanin photoprotection in apples. , 2000, Journal of photochemistry and photobiology. B, Biology.

[68]  K. V. van Wijk,et al.  High Light Response of the Thylakoid Proteome in Arabidopsis Wild Type and the Ascorbate-Deficient Mutant vtc2-2. A Comparative Proteomics Study1[W] , 2006, Plant Physiology.

[69]  Kazuo Shinozaki,et al.  Arabidopsis Cys2/His2-Type Zinc-Finger Proteins Function as Transcription Repressors under Drought, Cold, and High-Salinity Stress Conditions1 , 2004, Plant Physiology.

[70]  E. Titarenko,et al.  Reversible protein phosphorylation regulates jasmonic acid-dependent and -independent wound signal transduction pathways in Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[71]  Jennifer L. Nemhauser,et al.  Different Plant Hormones Regulate Similar Processes through Largely Nonoverlapping Transcriptional Responses , 2006, Cell.

[72]  J. Cushman,et al.  Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles , 2007, Functional & Integrative Genomics.

[73]  D. Baulcombe,et al.  Size constraints for targeting post-transcriptional gene silencing and for RNA-directed methylation in Nicotiana benthamiana using a potato virus X vector. , 2001, The Plant journal : for cell and molecular biology.

[74]  J. Glazebrook,et al.  Loss of non-host resistance of Arabidopsis NahG to Pseudomonas syringae pv. phaseolicola is due to degradation products of salicylic acid. , 2003, The Plant journal : for cell and molecular biology.

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

[76]  P. Waterhouse,et al.  Construct design for efficient, effective and high-throughput gene silencing in plants. , 2001, The Plant journal : for cell and molecular biology.

[77]  S. Jacobsen,et al.  Isolation and characterization of abscisic acid-deficient Arabidopsis mutants at two new loci. , 1996, The Plant journal : for cell and molecular biology.

[78]  M. Ohta,et al.  LOS 2 , a genetic locus required for cold-responsive gene transcription encodes a bifunctional enolase , 2022 .

[79]  D. Inzé,et al.  Overproduction of Arabidopsis thaliana FeSOD confers oxidative stress tolerance to transgenic maize. , 1999, Plant & cell physiology.

[80]  F. Ausubel,et al.  Roles of Salicylic Acid, Jasmonic Acid, and Ethylene in cpr-Induced Resistance in Arabidopsis , 2000, Plant Cell.

[81]  T. Kazuoka,et al.  A zinc finger protein RHL41 mediates the light acclimatization response in Arabidopsis. , 2000, The Plant journal : for cell and molecular biology.

[82]  R. Creelman,et al.  From Laboratory to Field. Using Information from Arabidopsis to Engineer Salt, Cold, and Drought Tolerance in Crops1 , 2004, Plant Physiology.

[83]  K. Asada,et al.  THE WATER-WATER CYCLE IN CHLOROPLASTS: Scavenging of Active Oxygens and Dissipation of Excess Photons. , 1999, Annual review of plant physiology and plant molecular biology.

[84]  Masahiro Kasahara,et al.  Chloroplast avoidance movement reduces photodamage in plants , 2002, Nature.