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Systemic Photooxidative Stress Signalling

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Long-Distance Systemic Signaling and Communication in Plants

Part of the book series: Signaling and Communication in Plants ((SIGCOMM,volume 19))

Abstract

Systemic signalling of photooxidative stress from a high light (HL)-exposed leaf to a shaded leaf results in systemic acquired acclimation (SAA) in the distal tissue. As yet unanswered questions in systemic photooxidative stress signalling are in regard to what type of signal and what form of travel the signal takes from a small area of exposed tissue to as yet unstressed distal tissues. Issues such as the specificity of different stress responses, how different ROS signalling pathways converge, and antagonistically regulated systems are all currently being investigated. The majority of studies in this field, however, focus on the intercellular signalling aspects rather than leaf-to-leaf movement of the signal. Traditional studies of biotic long-distance signalling have not as yet been comprehensively applied to abiotic stress signalling research, particularly in regard to whether an abiotic signal is able to rapidly travel through the vasculature from leaf to leaf. This review covers literature relating to the effects that HL intensity and the production of ROS have on the stress signalling processes of light perception, retrograde and intercellular signalling, as well as leaf-to-leaf systemic signalling in the model organism Arabidopsis thaliana.

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References

  • Ache P, Bauer H, Kollist H, Al-Rasheid KAS, Lautner S et al (2010) Stomatal action directly feeds back on leaf turgor: new insights into the regulation of the plant water status from non-invasive pressure probe measurements. Plant J 62:1072–1082

    PubMed  CAS  Google Scholar 

  • Araya T, Noguchi K, Terashima I (2008) Manipulation of light and CO2 environments of the primary leaves of bean (Phaseolus vulgaris L.) affects photosynthesis in both the primary and the first trifoliate leaves: involvement of systemic regulation. Plant Cell Environ 31:50–61

    PubMed  CAS  Google Scholar 

  • Arimura G-I, Ozawa R, Maffei ME (2011) Recent advances in plant early signaling in response to herbivory. Int J Mol Sci 12:3723–3739

    Article  PubMed  CAS  Google Scholar 

  • Bainbridge K, Bennett T, Turnbull C, Leyser O (2006) Grafting. Methods Mol Biol 323:39–44

    PubMed  Google Scholar 

  • Bellafiore S, Barneche F, Peltier G, Rochaix J-D (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433:892–895

    Article  PubMed  CAS  Google Scholar 

  • Bhattacharjee S (2005) Reactive oxygen species and oxidative burst: roles in stress, senescence and signal transduction in plants. Curr Sci 89:1113–1121

    CAS  Google Scholar 

  • Bienert GP, Moller ALB, Kristiansen KA, Schulz A, Moller IM et al (2007) Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem 282:1183–1192

    Article  PubMed  CAS  Google Scholar 

  • Bonardi V, Pesaresi P, Becker T, Schleiff E, Wagner R et al (2005) Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases. Nature 437:1179–1182

    Article  PubMed  CAS  Google Scholar 

  • Boyer JS (1974) Water transport in plants: mechanism of apparent changes in resistance during absorption. Planta 117:187–207

    Article  Google Scholar 

  • Breitenbach T, Kuimova MK, Gbur P, Hatz S, Schack NB et al (2009) Photosensitized production of singlet oxygen: spatially-resolved optical studies in single cells. Photochem Photobiol 8:442–452

    Article  CAS  Google Scholar 

  • Buhtz A, Pieritz J, Springer F, Kehr J (2010) Phloem small RNAs, nutrient stress responses, and systemic mobility. BMC Plant Biol 10:64

    Article  PubMed  CAS  Google Scholar 

  • Chang CC-C, Ball L, Fryer MJ, Baker NR, Karpinski S, Mullineaux PM (2004) Induction of ASCORBATE PEROXIDASE 2 expression in wounded Arabidopsis leaves does not involve known wound-signalling pathways but is associated with changes in photosynthesis. Plant J 38:499–511

    Article  PubMed  CAS  Google Scholar 

  • Chitwood DH, Timmermans MCP (2010) Small RNAs are on the move. Nature 467:415–419

    Article  PubMed  CAS  Google Scholar 

  • Coupe SA, Palmer BG, Lake JA, Overy SA, Oxborough K et al (2006) Systemic signalling of environmental cues in Arabidopsis leaves. J Exp Bot 57:329–341

    Article  PubMed  CAS  Google Scholar 

  • D’Autréaux B, Toledano MB (2007) ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 8:813–824

    Article  PubMed  CAS  Google Scholar 

  • Darwin C (1875) Insectivorous plants. John Murray, London

    Google Scholar 

  • Davletova S, Schlauch K, Coutu J, Mittler R (2005) The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol 139:847–856

    Article  PubMed  CAS  Google Scholar 

  • Desikan R, Mackerness SAH, Hancock JT, Neill SJ (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol 127:159–172

    Article  PubMed  CAS  Google Scholar 

  • Esau K (1953) Plant anatomy, vol xii. Wiley, New York, 735 p

    Google Scholar 

  • Estavillo GM, Crisp PA, Pornsiriwong W, Wirtz M, Collinge D et al (2011) Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. Plant Cell 23:3992–4012

    Article  PubMed  CAS  Google Scholar 

  • Evert RF, Esau K (2006) Esau’s plant anatomy: meristems, cells, and tissues of the plant body. Wiley, New York

    Book  Google Scholar 

  • Evert RF, Botha CEJ, Mierzwa RJ (1985) Free-space marker studies on the leaf of Zea mays L. Protoplasma 126:62–73

    Article  Google Scholar 

  • Fischer BB, Krieger-Liszkay A, Hideg E, Snyrychová I, Wiesendanger M, Eggen RIL (2007) Role of singlet oxygen in chloroplast to nucleus retrograde signaling in Chlamydomonas reinhardtii. FEBS Lett 581:5555–5560

    Article  PubMed  CAS  Google Scholar 

  • Frangne N, Maeshima M, Schäffner AR, Mandel T, Martinoia E, Bonnemain JL (2001) Expression and distribution of a vaculoar aquaporin in young and mature leaf tissues of Brassica napus in relation to water fluxes. Planta 212:270–278

    Article  PubMed  CAS  Google Scholar 

  • Frost CJ, Appel HM, Carlson JE, De Moraes CM, Mescher MC, Schultz JC (2007) Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol Lett 10:490–498

    Article  PubMed  Google Scholar 

  • Fryer MJ, Ball L, Oxborough K, Karpinski S, Mullineaux PM, Baker NR (2003) Control of Ascorbate Peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organisation of Arabidopsis leaves. Plant J 33:691–705

    Article  PubMed  CAS  Google Scholar 

  • Fuchs EE, Livingston NJ (1996) Hydraulic control of stomatal conductance in Douglas fir [Pseudotsuga menziesii (Mirb.) Franco] and alder [Alnus rubra (Bong)] seedlings. Plant Cell Environ 19:1091–1098

    Article  Google Scholar 

  • Gadjev I, Vanderauwera S, Gechev TS, Laloi C, Minkov IN et al (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol 141:436–445

    Article  PubMed  CAS  Google Scholar 

  • Galvez-Valdivieso G, Fryer MJ, Lawson T, Slattery K, Truman W et al (2009) The high light response in Arabidopsis involves ABA signaling between vascular and bundle sheath cells. Plant Cell 21:2143–2162

    Article  PubMed  CAS  Google Scholar 

  • Gao DJ, Knight MR, Trewavas AJ, Sattelmacher B, Plieth C (2004) Self-reporting Arabidopsis expressing pH and [Ca2+] indicators unveil ion dynamics in the cytoplasm and in the apoplast under abiotic stress. Plant Physiol 134:898–908

    Article  PubMed  CAS  Google Scholar 

  • Gigolashvilia T, Geierb M, Ashykhmina N, Frerigmann H, Wulfert S et al (2012) The Arabidopsis thylakoid ADP/ATP carrier TAAC has an additional role in supplying plastidic phosphoadenosine 5′-phosphosulfate to the cytosol. Plant Cell 24(10):4187–4204

    Article  CAS  Google Scholar 

  • Gorman AA, Rodgers MAJ (1992) New trends in photobiology. J Photochem Photobiol B 14:159–176

    Article  PubMed  CAS  Google Scholar 

  • Harris N, Chaffey NJ (1985) Plasmatubules in transfer cells of pea (Pisum sativum L.). Planta 165:191–196

    Article  Google Scholar 

  • Hatz S, Lambert JDC, Ogilby PR (2007) Measuring the lifetime of singlet oxygen in a single cell: addressing the issue of cell viability. Photochem Photobiol Sci 6:1106–1116

    Article  PubMed  CAS  Google Scholar 

  • Hatz S, Poulsen L, Ogilby PR (2008) Time-resolved singlet oxygen phosphorescence measurements from photosensitized experiments in single cells: effects of oxygen diffusion and oxygen concentration. Photochem Photobiol 84:1284–1290

    Article  PubMed  CAS  Google Scholar 

  • Heil M, Ton J (2008) Long-distance signalling in plant defence. Trends Plant Sci 13:264–272

    Article  PubMed  CAS  Google Scholar 

  • Heil M, Bueno S, Carlos J (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci USA 104:5467–5472

    Article  PubMed  CAS  Google Scholar 

  • Heinen RB, Ye Q, Chaumont F (2009) Role of aquaporins in leaf physiology. J Exp Bot 60:2971–2985

    Article  PubMed  CAS  Google Scholar 

  • Hensel LL, Grbić V, Baumgarten DA, Bleecker AB (1993) Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues in Arabidopsis. Plant Cell 5:553–564

    PubMed  CAS  Google Scholar 

  • Henzler T, Steudle E (2000) Transport and metabolic degradation of hydrogen peroxide in Chara corallina: model calculations and measurements with the pressure probe suggest transport of H2O2 across water channels. J Exp Bot 51:2053–2066

    Article  PubMed  CAS  Google Scholar 

  • Hihara Y, Kamei A, Kanehisa M, Kaplan A, Ikeuchi M (2001) DNA microarray analysis of cyanobacterial gene expression during acclimation to high light. Plant Cell 13:793–806

    PubMed  CAS  Google Scholar 

  • Ihnatowicz A, Pesaresi P, Lohrig K, Wolters D, Müller B, Leister D (2008) Impaired photosystem I oxidation induces STN7-dependent phosphorylation of the light-harvesting complex I protein Lhca4 in Arabidopsis thaliana. Planta 227:717–722

    Article  PubMed  CAS  Google Scholar 

  • Iida A, Kazuoka T, Torikai S, Kikuchi H, Oeda K (2001) A zinc finger protein RHL41 mediates the light acclimatization response in Arabidopsis. Plant J 24:191–203

    Article  Google Scholar 

  • Ishikawa K, Yoshimura K, Ogawa T, Shigeoka S (2010) Distinct regulation of Arabidopsis ADP-ribose/NADH pyrophosphohydrolases, AtNUDX6 and 7, in biotic and abiotic stress responses. Plant Signal Behav 5:839–841

    Article  PubMed  CAS  Google Scholar 

  • Jackson MB, Saker LR, Crisp CM, Else MA, Janowiak F (2003) Ionic and pH signalling from roots to shoots of flooded tomato plants in relation to stomatal closure. Plant Soil 253:103–113

    Article  CAS  Google Scholar 

  • Jambunathan N, Penaganti A, Tang Y, Mahalingam R (2010) Modulation of redox homeostasis under suboptimal conditions by Arabidopsis nudix hydrolase 7. BMC Plant Biol 10:173

    Article  PubMed  CAS  Google Scholar 

  • Jia W, Zhang J (2008) Stomatal movements and long-distance signaling in plants. Plant Signal Behav 3:772–777

    Article  PubMed  Google Scholar 

  • Karpinski S (2006) Holistic analysis of stress signalling network; new reactive oxygen species- and sugar-specific DNA cis-regulatory elements and functional interdependence between salicylic acid and glutathione signalling. Free Radic Res 40:S43–S43

    Google Scholar 

  • Karpinski S, Muhlenbock P (2007) Genetic, molecular and physiological mechanisms controlling cell death, defenses, and antioxidant network in response to abiotic and biotic stresses in plants. Comp Biochem Physiol 146:S60

    Google Scholar 

  • Karpinski S, Szechynska-Hebda M (2010) Secret life of plants: from memory to intelligence. Plant Signal Behav 5:1391–1394

    Article  PubMed  CAS  Google Scholar 

  • Karpinski S, Escobar C, Karpinska B, Creissen G, Mullineaux PM (1997) Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell 9:627–640

    PubMed  CAS  Google Scholar 

  • Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P (1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284:654–657

    Article  PubMed  CAS  Google Scholar 

  • Karpinski S, Gabrys H, Mateo A, Karpinska B, Mullineaux PM (2003) Light perception in plant disease defence signalling. Curr Opin Plant Biol 6:390–396

    Article  PubMed  CAS  Google Scholar 

  • Katiyar-Agarwal S, Jin H (2010) Role of small RNAs in host-microbe interactions. Annu Rev Phytopathol 48:225–246

    Article  PubMed  CAS  Google Scholar 

  • Kato Y, Miura E, Matsushima R, Sakamoto W (2007) White leaf sectors in yellow variegated2 are formed by viable cells with undifferentiated plastids. Plant Physiol 144:952–960

    Article  PubMed  CAS  Google Scholar 

  • Keen NT (1990) Gene-for-gene complementarity in plant-pathogen interactions. Annu Rev Genet 24:447–463

    Article  PubMed  CAS  Google Scholar 

  • Kehr J, Buhtz A (2008) Long distance transport and movement of RNA through the phloem. J Exp Bot 59:85–92

    Article  PubMed  CAS  Google Scholar 

  • Kerchev PI, Pellny TK, Vivancos PD, Kiddle G, Hedden P et al (2011) The transcription factor ABI4 Is required for the ascorbic acid-dependent regulation of growth and regulation of jasmonate-dependent defense signaling pathways in Arabidopsis. Plant Cell 23:3319–3334

    Article  PubMed  CAS  Google Scholar 

  • Kim C, Meskauskiene R, Apel K, Laloi C (2008) No single way to understand singlet oxygen signalling in plants. EMBO Rep 9:435–439

    Article  PubMed  CAS  Google Scholar 

  • Kimura M, Yoshizumi T, Manabe K, Yamamoto YY, Matsui M (2001) Arabidopsis transcriptional regulation by light stress via hydrogen peroxide-dependent and -independent pathways. Genes Cells 6:607–617

    Article  PubMed  CAS  Google Scholar 

  • Kimura M, Yamamoto YY, Seki M, Sakurai T, Sato M et al (2003) Identification of Arabidopsis genes regulated by high light-stress using cDNA microarray. Photochem Photobiol 77:226–233

    PubMed  CAS  Google Scholar 

  • Kinsman EA, Pyke KA (1998) Bundle sheath cells and cell-specific plastid development in Arabidopsis leaves. Development 125:1815–1822

    PubMed  CAS  Google Scholar 

  • Kitajima S, Shimaoka T, Kurioka M, Yokota A (2007) Irreversible cross-linking of heme to the distal tryptophan of stromal ascorbate peroxidase in response to rapid inactivation by H2O2. FEBS J 274:3013–3020

    Article  PubMed  CAS  Google Scholar 

  • Kleine T, Kindgren P, Benedict C, Hendrickson L, Strand A (2007) Genome-wide gene expression analysis reveals a critical role for CRYPTOCHROME1 in the response of Arabidopsis to high irradiance. Plant Physiol 144:1391–1406

    Article  PubMed  CAS  Google Scholar 

  • Koussevitzky S, Suzuki N, Huntington S, Armijo L, Sha W et al (2008) Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. J Biol Chem 283:34197–34203

    Article  PubMed  CAS  Google Scholar 

  • Kuimova MK, Yahioglu G, Ogilby PR (2009) Singlet oxygen in a cell: spatially dependent lifetimes and quenching rate constants. J Am Chem Soc 131:332–340

    Article  PubMed  CAS  Google Scholar 

  • Kwak JM, Mori IC, Pei Z-M, Leonhardt N, Torres MA et al (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633

    Article  PubMed  CAS  Google Scholar 

  • Kwak JM, Nguyen V, Schroeder JI (2006) The role of reactive oxygen species in hormonal responses. Plant Physiol 141:323–329

    Article  PubMed  CAS  Google Scholar 

  • Lake JA, Woodward FI, Quick WP (2002) Long-distance CO2 signalling in plants. J Exp Bot 53:183–193

    Article  PubMed  CAS  Google Scholar 

  • Laloi C, Stachowiak M, Pers-Kamczyc E, Warzych E, Murgia I, Apel K (2007) Cross-talk between singlet oxygen- and hydrogen peroxide-dependent signaling of stress responses in Arabidopsis thaliana. Proc Natl Acad Sci USA 104:672–677

    Article  PubMed  CAS  Google Scholar 

  • Lalonde S, Wipf D, Frommer WB (2004) Transport mechanisms for organic forms of carbon and nitrogen between source and sink. Annu Rev Plant Biol 55:341–372

    Article  PubMed  CAS  Google Scholar 

  • Lee KP, Kim C, Landgraf F, Apel K (2007) EXECUTER1- and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana. Proc Natl Acad Sci USA 104:10270–10275

    Article  PubMed  CAS  Google Scholar 

  • Leegood RC (2008) Roles of the bundle sheath cells in leaves of C3 plants. J Exp Bot 59:1663–1673

    Article  PubMed  CAS  Google Scholar 

  • Leisinger U, Rüfenacht K, Fischer B, Pesaro M, Spengler A et al (2001) The glutathione peroxidase homologous gene from Chlamydomonas reinhardtii is transcriptionally up-regulated by singlet oxygen. Plant Mol Biol 46:395–408

    Article  PubMed  CAS  Google Scholar 

  • Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and responding to excess light. Annu Rev Plant Biol 60:239–260

    Article  PubMed  CAS  Google Scholar 

  • Liu GS, Greenshields DL, Sammynaiken R, Hirji RN, Selvaraj G, Wei YD (2007) Targeted alterations in iron homeostasis underlie plant defense responses. J Cell Sci 120:596–605

    Article  PubMed  CAS  Google Scholar 

  • Lough TJ, Lucas WJ (2006) Integrative plant biology: role of phloem long-distance macromolecular trafficking. Annu Rev Plant Biol 57:203–232

    Article  PubMed  CAS  Google Scholar 

  • Mano J, Ohno C, Domae Y, Asada K (2001) Chloroplastic ascorbate peroxidase is the primary target of methylviologen-induced photooxidative stress in spinach leaves: its relevance to monodehydroascorbate radical detected with in vivo ESR. Biochim Biophys Acta 1504:275–287

    Article  PubMed  CAS  Google Scholar 

  • Martre P, Morillon R, Barrieu F, North GB, Nobel PS, Chrispeels MJ (2002) Plasma membrane aquaporins play a significant role during recovery from water deficit. Plant Physiol 130:2101–2110

    Article  PubMed  CAS  Google Scholar 

  • Maruta T, Noshi M, Tanouchi A, Tamoi M, Yabuta Y et al (2012) H2O2-triggered retrograde signaling from chloroplasts to nucleus plays specific role in response to stress. J Biol Chem 287:11717–11729

    Article  PubMed  CAS  Google Scholar 

  • Mateo A, Mühlenbock P, Rustérucci C, Chang CC-C, Miszalski Z et al (2004) LESION SIMULATING DISEASE 1 is required for acclimation to conditions that promote excess excitation energy. Plant Physiol 136:2818–2830

    Article  PubMed  CAS  Google Scholar 

  • Mateo A, Funck D, Mühlenbock P, Kular B, Mullineaux PM, Karpinski S (2006) Controlled levels of salicylic acid are required for optimal photosynthesis and redox homeostasis. J Exp Bot 57:1795–1807

    Article  PubMed  CAS  Google Scholar 

  • Meskauskiene R, Nater M, Goslings D, Kessler F, op den Camp R, Apel K (2001) FLU: a negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 98:12826–12831

    Article  PubMed  CAS  Google Scholar 

  • Miao Y, Lv D, Wang P, Wang X-C, Chen J et al (2006) An Arabidopsis glutathione peroxidase functions as both a redox transducer and a scavenger in abscisic acid and drought stress responses. Plant Cell 18:2749–2766

    Article  PubMed  CAS  Google Scholar 

  • Miller G, Schlauch K, Tam R, Cortes D, Torres MA et al (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal 2:ra45

    Article  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  PubMed  CAS  Google Scholar 

  • Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB et al (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309

    Article  PubMed  CAS  Google Scholar 

  • Miyake C, Shinzaki Y, Nishioka M, Horiguchi S, Tomizawa K-I (2006) Photoinactivation of ascorbate peroxidase in isolated tobacco chloroplasts: Galdieria partita APX maintains the electron flux through the water-water cycle in transplastomic tobacco plants. Plant Cell Physiol 47:200–210

    Article  PubMed  CAS  Google Scholar 

  • Miyao M (1994) Involvement of active oxygen species in degradation of the D1 protein under strong illumination in isolated subcomplexes of photosystem II. Biochemistry 33:9722–9730

    Article  PubMed  CAS  Google Scholar 

  • Møller IM, Sweetlove LJ (2010) ROS signalling—specificity is required. Trends Plant Sci 15:370–374

    Article  PubMed  CAS  Google Scholar 

  • Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–944

    Article  PubMed  CAS  Google Scholar 

  • Mubarakshina MM, Ivanov BN, Naydov IA, Hillier W, Badger MR, Krieger-Liszkay A (2010) Production and diffusion of chloroplastic H2O2 and its implication to signalling. J Exp Bot 61:3577–3587

    Article  PubMed  CAS  Google Scholar 

  • Mühlenbock P, Szechynska-Hebda M, Plaszczyca M, Baudo M, Mateo A et al (2008) Chloroplast signaling and LESION SIMULATING DISEASE1 regulate crosstalk between light acclimation and immunity in Arabidopsis. Plant Cell 20:2339–2356

    Article  PubMed  CAS  Google Scholar 

  • Muhling KH, Lauchli A (2000) Light-induced pH and K+ changes in the apoplast of intact leaves. Planta 212:9–15

    Article  PubMed  CAS  Google Scholar 

  • Mullineaux P (2009) ROS in retrograde signalling from the chloroplast to the nucleus. In: Rio LA, Puppo A (eds) Reactive oxygen species in plant signaling. Springer, Berlin, pp 221–240

    Chapter  Google Scholar 

  • Mullineaux PM, Baker NR (2010) Oxidative stress: antagonistic signaling for acclimation or cell death? Plant Physiol 154:521–525

    Article  PubMed  CAS  Google Scholar 

  • Nelson T, Dengler N (1997) Leaf vascular pattern formation. Plant Cell 9:1121–1135

    Article  PubMed  CAS  Google Scholar 

  • Nühse TS, Bottrill AR, Jones AME, Peck SC (2007) Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses. Plant J 51:931–940

    Article  PubMed  CAS  Google Scholar 

  • Ochsenbein C, Przybyla D, Danon A, Landgraf F, Göbel C et al (2006) The role of EDS1 (enhanced disease susceptibility) during singlet oxygen-mediated stress responses of Arabidopsis. Plant J 47:445–456

    Article  PubMed  CAS  Google Scholar 

  • Oelze M-L, Vogel MO, Alsharafa K, Kahmann U, Viehhauser A et al (2012) Efficient acclimation of the chloroplast antioxidant defence of Arabidopsis thaliana leaves in response to a 10- or 100-fold light increment and the possible involvement of retrograde signals. J Exp Bot 63:1297–1313

    Article  PubMed  CAS  Google Scholar 

  • op den Camp RGL, Przybyla D, Ochsenbein C, Laloi C, Kim C et al (2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15:2320–2332

    Article  PubMed  CAS  Google Scholar 

  • Orians C (2005) Herbivores, vascular pathways, and systemic induction: facts and artifacts. J Chem Ecol 31:2231–2242

    Article  PubMed  CAS  Google Scholar 

  • Palauqui JC, Elmayan T, Pollien JM, Vaucheret H (1997) Systemic acquired silencing: transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. EMBO J 16:4738–4745

    Article  PubMed  CAS  Google Scholar 

  • Pesaresi P, Hertle A, Pribil M, Kleine T, Wagner R et al (2009) Arabidopsis STN7 kinase provides a link between short- and long-term photosynthetic acclimation. Plant Cell 21:2402–2423

    Article  PubMed  CAS  Google Scholar 

  • Pilot G, Stransky H, Bushey DF, Pratelli R, Ludewig U et al (2004) Overexpression of GLUTAMINE DUMPER1 leads to hypersecretion of glutamine from hydathodes of Arabidopsis leaves. Plant Cell 16:1827–1840

    Article  PubMed  CAS  Google Scholar 

  • Pnueli L, Liang H, Rozenberg M, Mittler R (2003) Growth suppression, altered stomatal responses, and augmented induction of heat shock proteins in cytosolic ascorbate peroxidase (Apx1)-deficient Arabidopsis plants. Plant J 34:187–203

    Article  PubMed  CAS  Google Scholar 

  • Pogson BJ, Woo NS, Förster B, Small ID (2008) Plastid signalling to the nucleus and beyond. Trends Plant Sci 13:602–609

    Article  PubMed  CAS  Google Scholar 

  • Polle A (2001) Dissecting the superoxide dismutase-ascorbate-glutathione-pathway in chloroplasts by metabolic modeling. Computer simulations as a step towards flux analysis. Plant Physiol 126:445–462

    Article  PubMed  CAS  Google Scholar 

  • Przybyla D, Göbel C, Imboden A, Hamberg M, Feussner I, Apel K (2008) Enzymatic, but not non-enzymatic, 1O2 -mediated peroxidation of polyunsaturated fatty acids forms part of the EXECUTER1-dependent stress response program in the flu mutant of Arabidopsis thaliana. Plant J 54:236–248

    Article  PubMed  CAS  Google Scholar 

  • Puppo A (1992) Effect of flavonoids on hydroxyl radical formation by fenton-type reactions; influence of the iron chelator. Phytochemistry 31:85–88

    Article  CAS  Google Scholar 

  • Ramel F, Birtic S, Ginies C, Soubigou-Taconnat L, Triantaphylides C, Havaux M (2012) Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants. Proc Natl Acad Sci USA 109:5535–5540

    Article  PubMed  CAS  Google Scholar 

  • Redmond RW, Kochevar IE (2006) Spatially resolved cellular responses to singlet oxygen. Photochem Photobiol 82:1178–1186

    Article  PubMed  CAS  Google Scholar 

  • Rochaix J-D (2007) Role of thylakoid protein kinases in photosynthetic acclimation. FEBS Lett 581:2768–2775

    Article  PubMed  CAS  Google Scholar 

  • Rossel JB, Wilson IW, Pogson BJ (2002) Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol 130:1109–1120

    Article  PubMed  CAS  Google Scholar 

  • Rossel JB, Wilson PB, Hussain D, Woo NS, Gordon MJ et al (2007) Systemic and intracellular responses to photooxidative stress in Arabidopsis. Plant Cell 19:4091–4110

    Article  PubMed  CAS  Google Scholar 

  • Ruckle ME, DeMarco SM, Larkin RM (2007) Plastid signals remodel light signaling networks and are essential for efficient chloroplast biogenesis in Arabidopsis. Plant Cell 19:3944–3960

    Article  PubMed  CAS  Google Scholar 

  • Rusterucci C (2001) The disease resistance signaling components EDS1 and PAD4 are essential regulators of the cell death pathway controlled by LSD1 in Arabidopsis. Plant Cell 13:2211–2224

    PubMed  CAS  Google Scholar 

  • Sack L, Holbrook NM (2006) Leaf hydraulics. Annu Rev Plant Biol 57:361–381

    Article  PubMed  CAS  Google Scholar 

  • Sagi M, Fluhr R (2006) Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol 141:336–340

    Article  PubMed  CAS  Google Scholar 

  • Samol I, Shapiguzov A, Ingelsson B, Fucile G, Crèvecoeura M et al (2012) Identification of a photosystem II phosphatase involved in light acclimation in Arabidopsis. Plant Cell 24:2596–2609

    Article  PubMed  CAS  Google Scholar 

  • Schwach F, Vaistij FE, Jones L, Baulcombe DC (2005) An RNA-dependent RNA polymerase prevents meristem invasion by potato virus X and is required for the activity but not the production of a systemic silencing signal. Plant Physiol 138:1842–1852

    Article  PubMed  CAS  Google Scholar 

  • Shatil-Cohen A, Attia Z, Moshelion M (2011) Bundle-sheath cell regulation of xylem-mesophyll water transport via aquaporins under drought stress: a target of xylem-borne ABA? Plant J 67:72–80

    Article  PubMed  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223

    PubMed  CAS  Google Scholar 

  • Sies H, Menck CFM (1992) Singlet oxygen induced DNA damage. Mutat Res 275:367–375

    Article  PubMed  CAS  Google Scholar 

  • Sirichandra C, Gu D, Hu H-C, Davanture M, Lee S et al (2009) Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Lett 583:2982–2986

    Article  PubMed  CAS  Google Scholar 

  • Sobeih WY, Dodd IC, Bacon MA, Grierson D, Davies WJ (2004) Long-distance signals regulating stomatal conductance and leaf growth in tomato (Lycopersicon esculentum) plants subjected to partial root-zone drying. J Exp Bot 55:2353–2363

    Article  PubMed  CAS  Google Scholar 

  • Straus MR, Rietz S, Loren V, van Themaat E, Bartsch M, Parker JE (2010) Salicylic acid antagonism of EDS1-driven cell death is important for immune and oxidative stress responses in Arabidopsis. Plant J 62:628–640

    Article  PubMed  CAS  Google Scholar 

  • Szechynska-Hebda M, Kruk J, Gorecka M, Karpinska B, Karpinski S (2010) Evidence for light wavelength-specific photoelectrophysiological signaling and memory of excess light episodes in Arabidopsis. Plant Cell 22:2201–2218

    Article  PubMed  CAS  Google Scholar 

  • Sztatelman O, Waloszek A, BanaÅ› AK, GabryÅ› H (2010) Photoprotective function of chloroplast avoidance movement: in vivo chlorophyll fluorescence study. J Plant Physiol 167:709–716

    Article  PubMed  CAS  Google Scholar 

  • Tardieu F, Davies WJ (1993) Integration of hydraulic and chemical signalling in the control of stomatal conductance and water status of droughted plants. Plant Cell Environ 16:341–349

    Article  CAS  Google Scholar 

  • Terashima I, Hikosaka K (1995) Comparative ecophysiology of leaf and canopy photosynthesis. Plant Cell Environ 18:1111–1128

    Article  Google Scholar 

  • Thomas PW, Woodward FI, Quick WP (2003) Systemic irradiance signalling in tobacco. New Phytol 161:193–198

    Article  CAS  Google Scholar 

  • Tikkanen M, Piippo M, Suorsa M, Sirpiö S, Mulo P et al (2006) State transitions revisited—a buffering system for dynamic low light acclimation of Arabidopsis. Plant Mol Biol 62:779–793

    Article  PubMed  CAS  Google Scholar 

  • Tikkanen M, Grieco M, Kangasjärvi S, Aro E-M (2010) Thylakoid protein phosphorylation in higher plant chloroplasts optimizes electron transfer under fluctuating light. Plant Physiol 152:723–735

    Article  PubMed  CAS  Google Scholar 

  • Torres MA, Jones JDG, Dangl JL (2005) Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat Genet 37:1130–1134

    Article  PubMed  CAS  Google Scholar 

  • Triantaphylidès C, Krischke M, Hoeberichts FA, Ksas B, Gresser G et al (2008) Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiol 148:960–968

    Article  PubMed  CAS  Google Scholar 

  • Turnbull C (2011) Long-distance regulation of flowering time. J Exp Bot 62:4399–4413

    Article  PubMed  CAS  Google Scholar 

  • Van Breusegem F, Bailey-Serres J, Mittler R (2008) Unraveling the tapestry of networks involving reactive oxygen species in plants. Plant Physiol 147:978–984

    Article  PubMed  CAS  Google Scholar 

  • Vandenbroucke K, Robbens S, Vandepoele K, Inze D, de Peer YV, Van Breusegem F (2008) Hydrogen peroxide-induced gene expression across kingdoms: a comparative analysis. Mol Biol Evol 25:507–516

    Article  PubMed  CAS  Google Scholar 

  • Vanderauwera S, Zimmermann P, Rombauts S, Vandenabeele S, Langebartels C et al (2005) Genome-wide analysis of hydrogen peroxide-regulated gene expression in Arabidopsis reveals a high light-induced transcriptional cluster involved in anthocyanin biosynthesis. Plant Physiol 139:806–821

    Article  PubMed  CAS  Google Scholar 

  • Vranova E, Inze D, Van Breusegem F (2002) Signal transduction during oxidative stress. J Exp Bot 53:1227–1236

    Article  PubMed  CAS  Google Scholar 

  • Wagner D, Przybyla D, Op den Camp R, Kim C, Landgraf F et al (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306:1183–1185

    Article  PubMed  CAS  Google Scholar 

  • Wiermer M, Feys BJ, Parker JE (2005) Plant immunity: the EDS1 regulatory node. Curr Opin Plant Biol 8:383–389

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson S, Davies WJ (2002) ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant Cell Environ 25:195–210

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson S, Davies WJ (2008) Manipulation of the apoplastic pH of intact plants mimics stomatal and growth responses to water availability and microclimatic variation. J Exp Bot 59:619–631

    Article  PubMed  CAS  Google Scholar 

  • Xiao Y, Savchenko T, Baidoo EEK, Chehab WE, Hayden DM et al (2012) Retrograde signaling by the plastidial metabolite MEcPP regulates expression of nuclear stress-response genes. Cell 149:1525–1535

    Article  PubMed  CAS  Google Scholar 

  • Yabuta Y, Maruta T, Yoshimura K, Ishikawa T, Shigeoka S (2004) Two distinct redox signaling pathways for cytosolic APX induction under photooxidative stress. Plant Cell Physiol 45:1586–1594

    Article  PubMed  CAS  Google Scholar 

  • Yang D, Andersson B, Aro E, Ohad I (2001) 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. Photosynth Res 68:163–174

    Article  PubMed  CAS  Google Scholar 

  • Yano S, Terashima I (2001) Separate localization of light signal perception for sun or shade type chloroplast and palisade tissue differentiation in Chenopodium album. Plant Cell Physiol 42:1303–1310

    Article  PubMed  CAS  Google Scholar 

  • Zavaliev R, Sagi G, Gera A, Epel BL (2010) The constitutive expression of Arabidopsis plasmodesmal-associated class 1 reversibly glycosylated polypeptide impairs plant development and virus spread. J Exp Bot 61:131–142

    Article  PubMed  CAS  Google Scholar 

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Carmody, M., Pogson, B. (2013). Systemic Photooxidative Stress Signalling. In: Baluška, F. (eds) Long-Distance Systemic Signaling and Communication in Plants. Signaling and Communication in Plants, vol 19. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-36470-9_13

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