Abstract
Chloroplasts can serve as sensors for detecting perturbations in the subcellular environment and actively communicate these signals to other organelles. They also play a critical role in plant immunity. Previous studies have indicated that some plastid-signaling deficient mutants have impaired abiotic stresses tolerance. However, whether plastid signals are involved in biotic stress response is rarely reported. In this study, the relationship between plastid signals and Cucumber mosaic virus (CMV) stress response was investigated in Arabidopsis thaliana. Our results showed that plastid-signaling defective mutants were more susceptible to CMV infection and showed more serious stress damages [higher oxidative damages, more compromised in PSII photochemistry and more reactive oxygen species accumulation] compared with the wild-type plants. Furthermore, the induction of defense-associated genes and antioxidant enzymes activity in plastid-signaling defective mutants gun1 and abi4 were lesser than that observed in the wild-type plants after CMV infection. Collectively, our reports provide evidences that plastid signals are necessary for defense responses to CMV in A. thaliana. Moreover, the present study contributes to the understanding of the signaling pathway mediated by chloroplast in response to virus pathogens.
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References
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
Barajas-López JD, Blanco NE, Strand Å (2013) Plastid-to-nucleus communication, signals controlling the running of the plant cell. BBA-Mol Cell Res 1833:425–437
Bilger W, Björkman O (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth Res 25:173–185
Birkenbihl RP, Diezel C, Somssich IE (2012) Arabidopsis WRKY33 is a key transcriptional regulator of hormonal and metabolic responses toward Botrytis cinerea infection. Plant Physiol 159:266–285
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Chen L, Zhang L, Li D, Wang F, Yu D (2013) WRKY8 transcription factor functions in the TMV-cg defense response by mediating both abscisic acid and ethylene signaling in Arabidopsis. Proc Natl Acad Sci USA 110:1963–1971
Cheng J, He CX, Zhang ZW, Xu F, Zhang DW, Wang X, Yuan S, Lin HH (2011) Plastid signals confer Arabidopsis tolerance to water stress. Z Naturforsch C 66:47–54
Cummins I, Wortley DJ, Sabbadin F, He Z, Coxon CR, Straker HE, Sellars JD, Knight K, Edwards L, Hughes D (2013) Key role for a glutathione transferase in multiple-herbicide resistance in grass weeds. Proc Natl Acad Sci USA 110:5812–5817
Durrant W, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209
Estavillo GM, Crisp PA, Pornsiriwong W, Wirtz M, Collinge D, Carrie C, Giraud E, Whelan J, David P, Javot H (2011) Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. Plant Cell 23:3992–4012
Fernández AP, Strand Å (2008) Retrograde signaling and plant stress: plastid signals initiate cellular stress responses. Curr Opin Plant Biol 11:509–513
Foyer CH, Bloom AJ, Queval G, Noctor G (2009) Photorespiratory metabolism: genes, mutants, energetics, and redox signaling. Annu Rev Plant Biol 60:455–484
Fu ZQ, Dong X (2013) Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol 64:839–863
Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. BBA-Gen Subj 990:87–92
Guo DP, Guo YP, Zhao JP, Liu H, Peng Y, Wang QM, Chen JS, Rao GZ (2005) Photosynthetic rate and chlorophyll fluorescence in leaves of stem mustard (Brassica juncea var. tsatsai) after turnip mosaic virus infection. Plant Sci 168:57–63
Hu Y, Dong Q, Yu D (2012) Arabidopsis WRKY46 coordinates with WRKY70 and WRKY53 in basal resistance against pathogen Pseudomonas syringae. Plant Sci 185:288–297
Huang J, Gu M, Lai Z, Fan B, Shi K, Zhou YH, Yu JQ, Chen Z (2010) Functional analysis of the Arabidopsis PAL gene family in plant growth, development, and response to environmental stress. Plant Physiol 153:1526–1538
Jelenska J, Yao N, Vinatzer BA, Wright CM, Brodsky JL, Greenberg JT (2007) AJ domain virulence effector of Pseudomonas syringae remodels host chloroplasts and suppresses defenses. Curr Biol 17:499–508
Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins G, Surpin M, Lim J, Mittler R, Chory J (2007) Signals from chloroplasts converge to regulate nuclear gene expression. Science 316:715–719
Kwak JM, Nguyen V, Schroeder JI (2006) The role of reactive oxygen species in hormonal responses. Plant Physiol 141:323–329
Larkin RM, Alonso JM, Ecker JR, Chory J (2003) GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299:902–906
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
Leister D (2012) Retrograde signaling in plants: from simple to complex scenarios. Front Plant Sci 3:135
Mao G, Meng X, Liu Y, Zheng Z, Chen Z, Zhang S (2011) Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23:1639–1653
Miller G, Suzuki N, Rizhsky L, Hegie A, Koussevitzky S, Mittler R (2007) Double mutants deficient in cytosolic and thylakoid ascorbate peroxidase reveal a complex mode of interaction between reactive oxygen species, plant development, and response to abiotic stresses. Plant Physiol 144:1777–1785
Mochizuki N, Brusslan JA, Larkin R, Nagatani A, Chory J (2001) Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc Natl Acad Sci USA 98:2053–2058
Møller IM, Sweetlove LJ (2010) ROS signaling-specificity is required. Trends Plant Sci 15:370–374
Nott A, Jung HS, Koussevitzky S, Chory J (2006) Plastid-to-nucleus retrograde signaling. Annu Rev Plant Biol 57:739–759
op den Camp RG, Przybyla D, Ochsenbein C, Laloi C, Kim C, Danon A, Wagner D, Hideg É, Göbel C, Feussner I (2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15:2320–2332
Pesaresi P, Schneider A, Kleine T, Leister D (2007) Interorganellar communication. Curr Opin Plant Biol 10:600–606
Rahoutei J, García-Luque I, Barón M (2000) Inhibition of photosynthesis by viral infection: effect on PSII structure and function. Physiol Plantarum 110:286–292
Ramel F, Mialoundama AS, Havaux M (2013) Nonenzymic carotenoid oxidation and photooxidative stress signaling in plants. J Exp Bot 64:799–805
Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration-and cold-inducible gene expression. Biochem Biophys Res Commun 290:998–1009
Shang J, Xi DH, Xu F, Wang SD, Cao S, Xu MY, Zhao PP, Wang JH, Jia SD, Zhang ZW (2011) A broad-spectrum, efficient and nontransgenic approach to control plant viruses by application of salicylic acid and jasmonic acid. Planta 233:299–308
Spoel SH, Koornneef A, Claessens SMC, Korzelius JP, Van Pelt JA, Mueller MJ, Buchala AJ, Metraux JP, Brown R, Kazan K, Van Loon LC, Dong XN, Pieterse CMJ (2003) NPR1 modulates cross-talk between salicylate-and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760–770
Strand Å, Asami T, Alonso J, Ecker JR, Chory J (2003) Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrin IX. Nature 421:79–83
Sun X, Feng P, Xu X, Guo H, Ma J, Chi W, Lin R, Lu C, Zhang L (2011) A chloroplast envelope-bound PHD transcription factor mediates chloroplast signals to the nucleus. Nat Commun 2:477
Susek RE, Ausubel FM, Chory J (1993) Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell 74:787–799
Talboys PJ, Zhang HM, Paul Knox J (2011) ABA signaling modulates the detection of the LM6 arabinan cell wall epitope at the surface of Arabidopsis thaliana seedling root apices. New Phytol 190:618–626
Tang H, Zhang DW, Yuan S, Zhu F, Xu F, Fu FQ, Wang SX, Lin HH (2014) Plastid signals induce ALTERNATIVE OXIDASE expression to enhance the cold stress tolerance in Arabidopsis thaliana. Plant Growth Regul. doi:10.1007/s10725-014-9918-8
Ton J, Mauch-Mani B (2004) β-amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. Plant J 38:119–130
Torres MA, Jones JD, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141:373–378
Vinti G, Hills A, Campbell S, Bowyer JR, Mochizuki N, Chory J, López-Juez E (2000) Interactions between hy1 and gun mutants of Arabidopsis, and their implications for plastid/nuclear signaling. Plant J 24:883–894
Vlot AC, Dempsey DMA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206
Wagner D, Przybyla D, op den Camp R, Kim C, Landgraf F, Lee KP, Würsch M, Laloi C, Nater M, Hideg E (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306:1183–1185
Wang SD, Zhu F, Yuan S, Yang H, Xu F, Shang J, Xu MY, Jia SD, Zhang ZW, Wang JH, Xi DH, Lin HH (2011) The roles of ascorbic acid and glutathione in symptom alleviation to SA-deficient plants infected with RNA viruses. Planta 234:171–181
Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot Lond 100:681–697
Woodson JD, Perez-Ruiz JM, Chory J (2011) Heme synthesis by plastid ferrochelatase I regulates nuclear gene expression in plants. Curr Biol 21:897–903
Wu Y, Zhang D, Chu JY, Boyle P, Wang Y, Brindle ID, De Luca V, Després C (2012) The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep 1:639–647
Xi D, Feng H, Lan L, Du J, Wang J, Zhang Z, Xue L, Xu W, Lin H (2007) Characterization of synergy between Cucumber mosaic virus and Tobacco necrosis virus in Nicotiana benthamiana. J Phytopathol 155:570–573
Xia XJ, Wang YJ, Zhou YH, Tao Y, Mao WH, Shi K, Asami T, Chen Z, Yu JQ (2009) Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol 150:801–814
Xiao Y, Savchenko T, Baidoo EE, Chehab WE, Hayden DM, Tolstikov V, Corwin JA, Kliebenstein DJ, Keasling JD, Dehesh K (2012) Retrograde signaling by the plastidial metabolite MEcPP regulates expression of nuclear stress-response genes. Cell 149:1525–1535
Zhang ZW, Yuan S, Xu F, Yang H, Chen YE, Yuan M, Xu MY, Xue LW, Xu XC, Lin HH (2011) Mg-protoporphyrin, haem and sugar signals double cellular total RNA against herbicide and high-light-derived oxidative stress. Plant Cell Environ 34:1031–1042
Acknowledgments
This study was supported by the National Basic Research Program of China (973 Program) (2015CB150100), the National Natural Science Foundation of China (31470342, 31400211) and the Doctoral Foundation of the Ministry of Education (20120181130008, 20110181110059).
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Fa-Qiong Fu, Da-Wei Zhang and Xing-Guang Deng have contributed equally to this work.
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Fu, FQ., Zhang, DW., Deng, XG. et al. Role of plastid signals in modulating Arabidopsis responses to Cucumber mosaic virus . Plant Growth Regul 75, 761–769 (2015). https://doi.org/10.1007/s10725-014-9979-8
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DOI: https://doi.org/10.1007/s10725-014-9979-8