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The Role of Ascorbic Acid in Plant–Pathogen Interactions

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Ascorbic Acid in Plant Growth, Development and Stress Tolerance

Abstract

Ascorbic acid (AsA) is one of the most abundant antioxidant molecules in plants. AsA provides the first line of defense against damaging reactive oxygen species (ROS), protecting plant cells from many environmental factors that induce oxidative stress, including wounding, ozone, high salinity, and pathogen attacks. AsA interacts with key elements of a complex network orchestrating plant defense mechanisms, thereby influencing the outcome of plant–pathogen interaction. It can act in coordination with glutathione (GSH) and important enzymatic antioxidants in the AsA-GSH cycle to provide the appropriate redox environment regulating diverse defense pathways such as the expression of defense genes through the activation of the NPR1 (Nonexpressor of Pathogenesis-Related protein 1) regulatory transcription factor, the strengthening of cell walls, and the modulation of defense-hormonal signalling networks. On the other hand, AsA was found to act either as an inducer per se or as a component of induced resistance (IR) process to pathogens when elicited by other inducers/elicitors such as β-aminobutyric acid (BABA, a non-proteinic amino acid), jasmonic acid (JA) and its methyl ester (methyljasmonate, MEJA), and extracellular polysaccharides (EPSs). This chapter provides a broad picture on the mechanisms by which AsA interacts with key components of a complex network regulating both basal and induced resistance in different pathosystems.

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References

  • Almagro L, Carbonell-Bejerano P, Belchi-Navarro S, Bru R, Martinez-Zapater JM, Lijavetzky D, Pedreno MA (2014) Dissecting the transcriptional response to elicitors in Vitis vinifera cells. PLoS One 9(10):109777

    Article  Google Scholar 

  • Almagro L, Gómez Ros LV, Belchi-Navarro S, Bru R, Ros Barceló A, Pedreño MA (2009) Class III peroxidases in plant defence reactions. J Exp Bot 60:377–390

    Article  CAS  PubMed  Google Scholar 

  • Bala R, Thukral AK (2011) Phytoremediation of Cr (VI) by Spirodela polyrrhiza (L.) Schleiden employing reducing and chelating agents. Int J Phytoremediation 13(5):465–491

    Article  CAS  PubMed  Google Scholar 

  • Barth C, Moeder W, Klessig DF, Conklin PL (2004) The timing of senescence and response to pathogens is altered in the ascorbate deficient Arabidopsis mutant vitamin c-1. Plant Physiol 134:1784–1792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Botanga CJ, Bethke G, Chen Z, Gallie DR, Fiehn O, Glazebrook J (2012) Metabolite profiling of Arabidopsis inoculated with Alternaria brassicicola reveals that ascorbate reduces disease severity. Mol Plant Microbe Interact 25(12):1628–1638

    Article  CAS  PubMed  Google Scholar 

  • Boubakri H, Gargouri M, Mliki A, Brini F, Chong J, Jbara M (2016) Vitamins for enhancing plant resistance. Planta 244(3):529–543

    Article  CAS  PubMed  Google Scholar 

  • Boubakri H, Poutaraud A, Wahab MA, Clayeux C, Baltenweck-Guyot R, Steyer D, Marcic C, Mliki A, Soustre-Gacougnolle I (2013a) Thiamine modulates metabolism of the phenylpropanoid pathway leading to enhanced resistance to Plasmopara viticola in grapevine. BMC Plant Biol 13:31

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boubakri H, Wahab MA, Chong J, Bertsch C, Mliki A, Soustre-Gacougnolle I (2012) Thiamine induced resistance to Plasmopara viticola in grapevine and elicited host-defense responses, including HR like-cell death. Plant Physiol Biochem 57:120–133

    Article  CAS  PubMed  Google Scholar 

  • Boubakri H, Wahab MA, Chong J, Gertz C, Gandoura S, Mliki A, Bertsch C, Soustre-Gacougnolle I (2013b) Methionine elicits H2O2 generation and defense gene expression in grapevine and reduces Plasmopara viticola infection. J Plant Physiol 170(18):1561–1568

    Article  CAS  PubMed  Google Scholar 

  • Colvile L, Smirnoff N (2008) Antioxidant status, peroxidase activity, and PR protein transcript levels in ascorbate-deficient Arabidopsis thaliana vtc mutants. J Exp Bot 59:1–12

    Google Scholar 

  • Conklin PL, Gatzek S, Wheeler GL, Dowdle J, Raymond MJ, Rolinski S, Isupov M, Littlechild JA, Smirnoff N (2006) Arabidopsis thaliana VTC4 encodes L galactose-1-P phosphatase, a plant ascorbic acid biosynthetic enzyme. J Biol Chem 281:15662–15670

    Article  CAS  PubMed  Google Scholar 

  • Conklin PL, Norris SR, Wheeler GL, Williams EH, Smirnoff N, Last RL (1999) Genetic evidence for the role of GDP-mannose in plant ascorbic acid (vitamin C) biosynthesis. Proc Natl Acad Sci U S A 96:4198–4203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conklin PL, Saracco SA, Norris SR, Last RL (2000) Identification of ascorbic acid-deficient Arabidopsis thaliana mutants. Genetics 154:847–856

    CAS  PubMed  PubMed Central  Google Scholar 

  • de Pinto MC, Tommasi F, De Gara L (2002) Changes in the antioxidant systems as part of the signaling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species in tobacco bright-yellow 2 cells. Plant Physiol 130:1–11

    Article  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Despres C, Chubak C, Rochon A, Clark R, Bethune T, Desveaux D, Fobert PR (2003) The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1. Plant Cell 15:2181–2191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dias CV, Mendes JS, Dos Santos AC, Pirovani CP, da Silva Gesteira A, Micheli F, Gramacho KP, Hammerstone J, Mazzafera P, de Mattos Cascardo JC (2011) Hydrogen peroxide formation in cacao tissues infected by the hemibiotrophic fungus Moniliophthora perniciosa. Plant Physiol Biochem 49:917–922

    Article  CAS  PubMed  Google Scholar 

  • Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ, Reid JB, Fitt GP, Sewelam N, Schenk PM, Manners JM, Kazan K (2007) MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 19:2225–2245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dowdle J, Ishikawa T, Gatzek S, Rolinski S, Smirnoff N (2007) Two genes in Arabidopsis thaliana encoding GDP-L-galactose phosphorylase are required for ascorbate biosynthesis and seedling viability. Plant J 52:673–689

    Article  CAS  PubMed  Google Scholar 

  • Egan MJ, Wang ZY, Jones MA, Smirnoff N, Talbot NJ (2007) Generation of reactive oxygen species by fungal NADPH oxidases is required for rice blast disease. Proc Natl Acad Sci U S A 104:11772–11777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fobert PR, Despres C (2005) Redox control of systemic acquired resistance. Curr Opin Plant Biol 8:378–382

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071

    Article  CAS  Google Scholar 

  • Fujiwara A, Shimura H, Masuta C, Sano S, Inukai T (2013) Exogenous ascorbic acid derivatives and dehydroascorbic acid are effective antiviral agents against Turnip mosaic virus in Brassica rapa. J Gen Plant Pathol 79:198–204

    Article  CAS  Google Scholar 

  • Gallie DR (2013) The role of l-ascorbic acid recycling in responding to environmental stress and in promoting plant growth. J Exp Bot 64:433–443

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Brugger A, Lamotte O, Vandelle E, Bourque S, Lecourieux D, Poinssot B, Wendehenne D, Pugin A (2006) Early signaling events induced by elicitors of plant defenses. Mol Plant Microbe Interact 19(7):711–724

    Article  CAS  PubMed  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    Article  CAS  PubMed  Google Scholar 

  • Hagemeier J, Schneider B, Oldham NJ, Hahlbrock K (2001) Accumulation of soluble and wall-bound indolic metabolites in Arabidopsis thaliana leaves infected with virulent or avirulent Pseudomonas syringae pathovar tomato strains. Proc Natl Acad Sci U S A 98:53–58

    Article  Google Scholar 

  • Huckelhoven R (2007) Cell wall-associated mechanisms of disease resistance and susceptibility. Annu Rev Phytopathol 45:101–127

    Article  PubMed  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444(7117):323–329

    Article  CAS  PubMed  Google Scholar 

  • Khan TA, Mazid M, Mohammad F (2012) Potential of Ascorbic acid against oxidative burst in plants under biotic stress: a review. J Ind Res Technol 2(2):72–80

    Google Scholar 

  • Kus JV, Zaton K, Sarkar R, Cameron RK (2002) Age-related resistance in Arabidopsis is a developmentally regulated defense response to Pseudomonas syringae. Plant Cell 14(2):479–490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuzniak E (2010) The ascorbate–gluathione cycle and related redox signals in plant–pathogen interactions. In: Anjum NA et al (eds) Ascorbate-glutathione pathway and stress tolerance in plants. Springer, Dordrecht, pp 115–136

    Chapter  Google Scholar 

  • Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251–275

    Article  CAS  PubMed  Google Scholar 

  • Li J, Trivedi O, Wang N (2016) Field evaluation of plant defense inducers for the control of citrus Huanglongbing. Plant Pathol 6:37–46

    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  CAS  PubMed  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Müller-Moulé P, Havaux M, Niyogi KK (2003) Zeaxanthin deficiency enhances the high light sensitivity of an ascorbate-deficient mutant of Arabidopsis. Plant Physiol 133:748–760

    Article  PubMed  PubMed Central  Google Scholar 

  • Mukherjee M, Larrimore KE, Ahmed NJ, Bedick TS, Barghouthi NT, Traw MB, Barth C (2010) Ascorbic acid deficiency in Arabidopsis induces constitutive priming that is dependent on hydrogen peroxide, salicylic acid, and the NPR1 gene. Mol Plant Microbe Interact 23(3):340–351

    Article  CAS  PubMed  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  CAS  PubMed  Google Scholar 

  • Noctor G, Gomez L, Vanacker H, Foyer CH (2002) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signalling. J Exp Bot 53:1283–1304

    Article  CAS  PubMed  Google Scholar 

  • Pastor V, Luna E, Ton J, Cerezo M, Garcia-Agustin P, Flors V. Fine tuning of reactive oxygen species homeostasis regulates primed immune responses in Arabidopsis. Mol Plant Microbe Interact. 2013; 11:1334–1344.

    Google Scholar 

  • Pastori GM, Kiddle G, Antoniw J, Bernard S, Veljovic-Jovanovic S, Verrier PJ, Noctor G, Foyer CH (2003) Leaf vitamin C contents modulate plant defense transcripts and regulate genes that control development through hormone signalling. Plant Cell 15:939–951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pavet V, Olmos E, Kiddle G, Mowla S, Kumar S, Antoniw J, Alvarez ME, Foyer CH (2005) Ascorbic acid deficiency activates cell death and disease resistance responses in Arabidopsis. Plant Physiol 139:1291–1303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pieterse CMJ, Poelman EH, Van Wees SCM, Dicke M (2013) Induced plant responses to microbes and insects. Front Plant Sci 4:475

    Article  PubMed  PubMed Central  Google Scholar 

  • Pieterse CMJ, Van Loon LC (2004) NPR1: the spider in the web of induced resistance signalling pathways. Curr Opin Plant Biol 7:456–464

    Article  CAS  PubMed  Google Scholar 

  • Pignocchi C, Fletcher JM, Wilkinson JE, Barnes JD, Foyer CH (2003) The function of ascorbate oxidase in tobacco. Plant Physiol 132:1631–1641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY, Hunt MD (1996) Systemic acquired resistance. Plant Cell 8(10):1809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanmartin M, Drogoudi PD, Lyons T, Pateraki I, Barnes J, Kanellis AK (2003) Over-expression of ascorbate oxidase in the apoplast of transgenic tobacco results in altered ascorbate and glutathione redox states and increased sensitivity to ozone. Planta 216:918–928

    CAS  PubMed  Google Scholar 

  • Sasaki-Sekimoto Y, Taki N, Obayashi T, Aono M, Matsumoto F, Sakurai N, Suzuki H, Hirai MY, Noji M, Saito K, Masuda T, Takamiya K, Shibata D, Ohta H (2005) Coordinated activation of metabolic pathways for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis. Plant J 44(4):653–668

    Article  CAS  PubMed  Google Scholar 

  • Smirnoff N, Wheeler GL (2000) Ascorbic acid in plants: biosynthesis and function. Crit Rev Biochem Mol Biol 35:291–314

    Article  CAS  PubMed  Google Scholar 

  • Sudhamony M, Nirupama M, Adinpunya M (2009) Salicilic acid-induced resistance to Fusarium oxysporum f. sp. Lycopersici in tomato. Plant Physiol Biochem 47:642–649

    Article  Google Scholar 

  • Suza WP, Rowe ML, Hamberg M, Staswick PE (2010) A tomato enzyme synthesizes (+)-7-isojasmonoyl-L-isoleucine in wounded leaves. Planta 231:717–728

    Article  CAS  PubMed  Google Scholar 

  • Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Wang C, Zuo J, Dong X (2008) Plant immunity requires conformational charges of NPR1 via S-nitrosylation and thioredoxins. Science 321:952–956

    Article  CAS  PubMed  Google Scholar 

  • Takahama U, Oniki T (1992) Regulation of peroxidase dependent oxidation of phenolics in the apoplast of spinach leaves by ascorbate. Plant Cell Physiol 33:379–387

    CAS  Google Scholar 

  • Tamogami S, Rakwal R, Kodama O (1997) Phytoalexin production elicited by exogenously applied jasmonic acid in rice leaves (Oryza sativa L.) is under the control of cytokinins and ascorbic acid. FEBS Lett 412:61–64

    Article  CAS  PubMed  Google Scholar 

  • Torres MA, Jones JDG, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141:373–378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsuda K, Kosaka Y, Kobori T, Shiomi H, Musumi K, Kataoka M (2005) Effects of fertilizer application on yield and vitamin C content of tomato inoculated with the attenuated isolate CM95 of Cucumber mosaic virus. Jpn J Phytopathol 71:1–5

    Article  Google Scholar 

  • Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. Plant Cell 14(suppl 1):S153–S164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Wees SCM, Van der Ent S, Pieterse CMJ (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11(4):443–448

    Article  PubMed  Google Scholar 

  • Vanacker H, Carver TLW, Foyer C (1998) Pathogen-induced changes in the antioxidant status of the apoplast in barley leaves. Plant Physiol 117:1103–1114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vanacker H, Carver TLW, Foyer CH (2000) Early H2O2 accumulation in mesophyll cells leads to induction of glutathione during the hyper-sensitive response in the barley powdery mildew interaction. Plant Physiol 123:1289–1300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Veljovic-Jovanovic SD, Pignocchi C, Noctor G, Foyer CH (2001) Low ascorbic acid in the vtc-1 mutant of Arabidopsis is associated with decreased growth and intracellular redistribution of the antioxidant system. Plant Physiol 127:426–435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walsh JA, Jenner CE (2002) Turnip mosaic virus and the quest for durable resistance. Mol Plant Pathol 13(5):289–300

    Article  Google Scholar 

  • Walters DR, Ratsep J, Havis ND (2013) Controlling crop diseases using induced resistance: challenges for the future. J Exp Bot 64(5):1263–1280

    Article  CAS  PubMed  Google Scholar 

  • Wheeler GL, Jones MA, Smirnoff N (1998) The biosynthetic pathway of vitamin C in higher plants. Nature 393:365–369

    Article  CAS  PubMed  Google Scholar 

  • Wolucka BA, Goossens A, Inzé D (2005) Methyl jasmonate stimulates the de novo biosynthesis of vitamin C in plant cell suspensions. J Exp Bot 56(419):2527–2538

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Xing D (2008) Methyl jasmonate induces production of reactive oxygen species and alterations in mitochondrial dynamics that precede photosynthetic dysfunction and subsequent cell death. Plant Cell Physiol 49:1092–1111

    Article  CAS  PubMed  Google Scholar 

  • Zipfel C (2009) Early molecular events in PAMP-triggered immunity. Curr Opin Plant Biol 12(4):414–420

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The author would like to thank the Tunisian Ministry of Higher Education and Scientific Research for the support.

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Correspondence to Hatem Boubakri .

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Boubakri, H. (2017). The Role of Ascorbic Acid in Plant–Pathogen Interactions. In: Hossain, M., Munné-Bosch, S., Burritt, D., Diaz-Vivancos, P., Fujita, M., Lorence, A. (eds) Ascorbic Acid in Plant Growth, Development and Stress Tolerance. Springer, Cham. https://doi.org/10.1007/978-3-319-74057-7_10

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