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Abiotic Elicitor-Mediated Improvement of Innate Immunity in Camellia sinensis

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Abstract

Elicitor-induced natural defense machinery of plants could be proposed as an alternative, non-conventional, and ecologically-friendly approach for plant protection. In this work, the abiotic elicitor, calcium chloride (CaCl2), was used for inducing resistance in tea plants against blister blight disease caused by Exobasidium vexans. Foliar application of elicitor resulted in around 80 % disease inhibition over the control set, during the peak time of blister blight incidence at the experimental garden of Darjeeling Tea Research and Development Centre. A significant increase in the activities of defense enzymes like phenylalanine ammonia lyase (PAL), peroxidase, polyphenol oxidase, and β-1,3-glucanase along with higher accumulation of total phenolics was observed. Treated plants also had elevated transcript levels of thaumatin, catalase, PAL, cinnamate 4-hydroxylase, and flavonoid 3′-hydroxylase genes compared to control plants. Further, the treatment-induced nitric oxide (NO) production was confirmed by real-time visualization of the NO burst using a fluorescent probe and spectrophotometric analysis. The result suggested that CaCl2 induced an array of plant defense responses making this compound a potential phytosanitary product with a challenging issue and a rather attractive option for sustainable organic tea cultivation practice.

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References

  • Acharya R, Acharya K (2007) Evaluation of nitric oxide synthase status during disease progression in resistant and susceptible varieties of Sesamum indicum against Macrophomina phaseolina. Asian Australas J Plant Sci Biotechnol 1:40–44

    Google Scholar 

  • Acharya R, Mukhia M, Sen S, Acharya K (2005) Nitric oxide: a common antipathogenic factor of plants. Indian J Exp Biol 43:100–103

    CAS  PubMed  Google Scholar 

  • Acharya K, Chakraborty N, Dutta AK, Sarkar S, Acharya R (2011a) Signaling role of nitric oxide in the induction of plant defense by exogenous application of abiotic inducers. Arch Phytopathol Plant Prot 44:1501–1511

    Article  CAS  Google Scholar 

  • Acharya K, Chandra S, Chakraborty N, Acharya R (2011b) Nitric oxide functions as a signal in induced systemic resistance. Arch Phytopathol Plant Prot 44:1335–1342

    Article  CAS  Google Scholar 

  • Ajay D, Baby UI (2010) Induction of systemic resistance to Exobasidium vexans in tea through SAR elicitors. Phytoparasitica 38:53–60

    Article  CAS  Google Scholar 

  • Anand T, Chandrasekaran A, Raguchander T, Prakasam V, Samiyappan R (2009) Chemical and biological treatments for enhancing resistance in chilli against Colletotrichum capsici and Leveillula taurica. Arch Phytopathol Plant Prot 42:533–551

    Article  CAS  Google Scholar 

  • Anttonen M, Hukkanen A, Tiilikkala K, Karjalainen R (2003) Benzothiadiazole induces defense responses in berry crops. Acta Hortic 567:177–182

    Article  Google Scholar 

  • Ardi R, Kobiler I, Jacoby B, Keen NT, Prusky D (1998) Involvement of epicatechin biosynthesis in the activation of the mechanism of resistance of avocado fruits to Colletotrichum gloeosporioides. Physiol Mol Plant Pathol 53:269–285

    Article  CAS  Google Scholar 

  • Arulpragasam PV (1992) Disease control in Asia. In: Wilson KC, Clifford MN (eds) Tea cultivation to consumption. Chapman & Hall, London, pp 353–374

    Google Scholar 

  • Aziz A, Trotel-Aziz P, Dhuicq L, Jeandet P, Couderchet M, Vernet G (2006) Chitosan oligomers and copper sulfate induce grapevine defense reactions and resistance to gray mold and downy mildew. Phytopathology 96:1188–1194

    Article  CAS  PubMed  Google Scholar 

  • Bartha B, Kolbert Z, Erdei L (2005) Nitric oxide production induced by heavy metals in Brassica juncea L. Czern. and Pisum sativum L. Acta Biol Szeged 49:9–12

    Google Scholar 

  • Baudouin E (2011) The language of nitric oxide signalling. Plant Biol 13:233–242

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Chen WP, Chen PD, Liu DJ, Kynast R, Friebe B, Velazhahan R, Muthukrishnan S, Gill BS (1999) Development of wheat scab symptoms is delayed in transgenic wheat plants that constitutively express a rice thaumatin-like protein gene. Theor Appl Genet 99:755–760

    Article  CAS  Google Scholar 

  • Cho S, Chen W, Muehlbauer FJ (2005) Constitutive experssion of the flavanone 3-hydroxylase gene related to pathotype-specific ascochyta blight resistance in Cicer arietinum L. Physiol Mol Plant Pathol 67:100–107

    Article  CAS  Google Scholar 

  • Coquoz JL, Buchala AJ, Meuwly Ph, Métraux JP (1995) Arachidonic acid induces local but not systemic synthesis of salicylic acid and confers systemic resistance in potato plants to Phytophthora infestans and Alternaria solani. Phytopathol 85:1219–1224

    Article  CAS  Google Scholar 

  • Dangl JL, Dietrich RA, Richberg MH (1996) Death don’t have no mercy: cell death programs in plant–microbe interactions. Plant Cell 8:1793–1807

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • del Rίo LA, Corpas FJ, Barroso JB (2004) Nitric oxide and nitric oxide synthase activity in plants. Phytochemistry 65:783–792

    Article  Google Scholar 

  • Delledonne M, Xia Y, Dixon RA, Lamb C (1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394:585–588

    Article  CAS  PubMed  Google Scholar 

  • Delledonne M, Zeier J, Marocco A, Lamb C (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci USA 98:13454–13459

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Desender S, Andrivon D, Val F (2007) Activation of defence reactions in Solanaceae: where is the specificity? Cell Microbiol 9:21–30

    Article  CAS  PubMed  Google Scholar 

  • Dickerson DP, Pascholati SF, Hagerman AE, Butler LG, Nicholson RL (1984) Phenylalanine ammonia-lyase and hydroxycinnamate: CoA ligase in maize mesocotyls inoculated with Helminthosporium maydis or Helminthosporium carbonum. Physiol Plant Pathol 25:111–123

    Article  CAS  Google Scholar 

  • Dong J, Wan G, Liang Z (2010) Accumulation of salicylic acid-induced phenolic compounds and raised activities of secondary metabolic and antioxidative enzymes in Salvia miltiorrhiza cell culture. J Biotechnol 148:99–104

    Article  CAS  PubMed  Google Scholar 

  • Dos Santos NST, Athayde Aguiar AJA, de Oliveira CEV, Verissimo de Sales C, de Melo E, Silva S, Sousa da Silva R, Stamford TCM, de Souza EL (2012) Efficacy of the application of a coating composed of chitosan and Origanum vulgare L. essential oil to control Rhizopus stolonifer and Aspergillus niger in grapes (Vitis labrusca L.). Food Microbiol 32:345–353

    Article  PubMed  Google Scholar 

  • El Modafar C, Elgadda M, El Boutachfaiti R, Abouraicha E, Zehhar N, Petit E, El Alaoui-Talibi Z, Courtois B, Courtois J (2012) Induction of natural defense accompanied by salicylic acid-dependant systemic acquired resistance in tomato seedlings in response to bioelicitors isolated from green algae. Sci Hort 138:55–63

    Article  Google Scholar 

  • Giovanini MP, Puthoff DP, Nemacheck JA, Mittapalli O, Saltzmann KD, Ohm HW, Shukle RH, Williams CE (2006) Gene-for-gene defense of wheat against the Hessian fly lacks a classical oxidative burst. Mol Plant-Microbe Interact 19:1023–1033

    Article  CAS  PubMed  Google Scholar 

  • Gould KS, Lister C (2006) Flavonoid functions in plants. In: Andersen ØM, Markham KR (eds) Flavonoids: chemistry, biochemistry and applications. CRC Press, Boca Raton, pp 397–411

    Google Scholar 

  • Goupil P, Benouaret R, Charrier O, ter Halle A, Richard C, Eyheraguibel B, Thiery D, Ledoigt G (2012) Grape marc extract acts as elicitor of plant defence responses. Ecotoxicology 21:1541–1549

    Article  CAS  PubMed  Google Scholar 

  • Grover A, Gowthaman R (2003) Strategies for development of fungus-resistant transgenic plants. Curr Sci 84:330–340

    Google Scholar 

  • Gupta NS, Banerjee M, Basu SK, Acharya K (2013) Involvement of nitric oxide signal in Alternaria alternata toxin induced defense response in Rauvolfia serpentina Benth. ex Kurz calli. Plant Omics J 6:157–164

    CAS  Google Scholar 

  • Hammerschmidt R (1999) Induced disease resistance: how do induced plants stop pathogens? Physiol Mol Plant Pathol 55:77–84

    Article  CAS  Google Scholar 

  • Hammerschmidt R, Nuckels EM, Kuć J (1982) Association of enhanced peroxidase activity with induced systemic resistance of cucumber in Colletotrichum lagenarium. Physiol Plant Pathol 20:73–82

    Article  CAS  Google Scholar 

  • Harm A, Kassemeyer H–H, Seibicke T, Regner F (2011) Evaluation of chemical and natural resistance inducers against downy mildew (Plasmopara viticola) in grapevine. Am J Enol Vitic 62:184–192

    Article  Google Scholar 

  • Hong JK, Hwang BK, Kim CH (1999) Induction of local and systemic resistance to Colletotrichum coccodes in pepper plants by dl-β-amino-n-butyric acid. J Phytopathol 147:193–198

    Article  CAS  Google Scholar 

  • Hong JK, Yun BW, Kang JG, Raja MU, Kwo E, Sorheagn K, Chu C, Wang Y, Loake GJ (2008) Nitric oxide function and signaling in plant resistance. J Exp Bot 59:147–154

    Article  CAS  PubMed  Google Scholar 

  • Jayaraj J, Rahman M, Wan A, Punja ZK (2009) Enhanced resistance to foliar fungal pathogens in carrot by application of elicitors. Ann Appl Biol 155:71–80

    Article  CAS  Google Scholar 

  • Khlestkina EK, Salina EA, Matthies IE, Leonova IN, Börner A, Röder MS (2011) Comparative molecular marker-based genetic mapping of flavanone 3-hydroxylase genes in wheat, rye and barley. Euphytica 179:333–341

    Article  CAS  Google Scholar 

  • Kuć J (2006) What’s old and what’s new in concepts of induced systemic resistance in plants and its application. In: Tuzun S, Bent E (eds) Multigenic and induced systemic resistance in plants, vol 20. Springer, New York, pp 9–20

    Google Scholar 

  • Lin JH, Gong DQ, Zhu SJ, Zhang LJ, Zhang LB (2011) Expression of PPO and POD genes and contents of polyphenolic compounds in harvested mango fruits in relation to benzothiadiazole-induced defense against anthracnose. Sci Hortic 130:85–89

    Article  CAS  Google Scholar 

  • Lum HK, Butt YK, Lo SC (2002) Hydrogen peroxide induces a rapid production of nitric oxide in mung bean (Phaseolus aureus). Nitric Oxide 6:205–213

    Article  CAS  PubMed  Google Scholar 

  • Maxson-Stein K, He SY, Hammerschmidt R, Jones AS (2002) Effect of treating apple trees with acibenzolar-S-methyl on fire blight and expression of pathogenesis-related protein genes. Plant Dis 8:785–790

    Article  Google Scholar 

  • Mayer AM, Harel E, Shaul RB (1965) Assay of catechol oxidase, a critical comparison of methods. Phytochemistry 5:783–789

    Article  Google Scholar 

  • Michael O, Walter K, Bob D, Theodor S (2001) Induced disease resistance in plants by chemicals. Eur J Plant Pathol 107:19–28

    Article  Google Scholar 

  • Modolo LV, Augusto O, Almeida IM, Magalhaes JR, Salgado I (2005) Nitrite as the major source of nitric oxide production by Arabidopsis thaliana in response to Pseudomonas syringae. FEBS Lett 579:3814–3820

    Article  CAS  PubMed  Google Scholar 

  • Montesano M, Brader G, Palva ET (2003) Pathogen derived elicitors: searching for receptors in plants. Mol Plant Pathol 4:73–79

    Article  CAS  PubMed  Google Scholar 

  • Moreno FD, Blanch GP, del Castillo MLR (2010) (+)-Methyl jasmonate-induced bioformation of myricetin, quercetin and kaempferol in red raspberries. J Agric Food Chem 58:11639–11644

    Article  Google Scholar 

  • Nicholson RL, Hammerschmidt R (1992) Phenolic-compounds and their role in disease resistance. Annu Rev Phytopathol 30:369–389

    Article  CAS  Google Scholar 

  • Pal TK, Bhattacharya S, Chakraborty K (2011) Induction of systemic resistance in rice by leaf extract of Cymbopogan citrus and Ocimum sanctum against seath blight disease. Arch Appl Sci Res 3:392–400

    CAS  Google Scholar 

  • Pan S, Ye XS, Kuć J (1991) Association of β-1,3-glucanase activity and isoform pattern with systemic resistance to blue mold in tobacco induced by stem injection with Peronospora tabacina or leaf inoculation with tobacco mosaic virus. Physiol Mol Plant Pathol 39:25–39

    Article  CAS  Google Scholar 

  • Perchepied L, Balague C, Riou C, Claudel-Renard C, Riviere N, Grezes-Besset B, Roby D (2010) Nitric oxide participates in the complex interplay of defense-related signaling pathways controlling disease resistance to Sclerotinia sclerotiorum in Arabidopsis thaliana. Mol Plant-Microbe Interact 23:846–860

    Article  CAS  PubMed  Google Scholar 

  • Prithiviraj B, Perry LG, Badri DV, Vivanco JM (2007) Chemical facilitation and induced pathogen resistance mediated by a root-secreted phytotoxin. New Phytol 173:852–860

    Article  CAS  PubMed  Google Scholar 

  • Prusky D (1996) Pathogen quiescence in post harvest diseases. Annu Rev Phytopathol 34:413–434

    Article  CAS  PubMed  Google Scholar 

  • Prusky D, Hamadan H, Ardi R, Keen NT (1996) Induction of biosynthesis of epicatechin in avocado suspension cells treated with an enriched CO2 atmosphere. Physiol Mol Plant Pathol 48:171–178

    Article  CAS  Google Scholar 

  • Punja ZK (2005) Transgenic carrots expressing a thaumatin-like protein display enhanced resistance to several fungal pathogens. Can J Plant Pathol 27:291–296

    Article  CAS  Google Scholar 

  • Punyasiri PAN, Tanner GJ, Abeysinghe ISB, Kumar V, Campbell PM, Pradeepa NHL (2004) Exobasidium vexans infection of Camellia sinensis increased 2,3-cis isomerisation and gallate esterification of proanthocyanidins. Phytochemistry 65:2987–2994

    Article  CAS  Google Scholar 

  • Reddy ASN (2001) Calcium: silver bullet in signalling. Plant Sci 160:381–404

    Article  CAS  PubMed  Google Scholar 

  • Rudd JJ, Franklin-Tong VE (2001) Unravelling response-specificity in Ca2+ signalling pathways in plant cells. New Phytol 151:733–749

    Article  Google Scholar 

  • Salter M, Knowles GR (1998) Assay of NOS activity by the measurement of conversion of oxyhemoglobin to methemoglobin by NO. In: Titheradge MA (ed) Nitric oxide protocols. Humana Press, Totowa, pp 61–65

    Google Scholar 

  • Sánchez-Estrada A, Tiznado-Hernández ME, Ojeda-Contreras AJ, Valenzuela-Quintanar AI, Troncoso-Rojas R (2009) Induction of enzymes and phenolic compounds related to the natural defence response of netted melon fruit by a bio-elicitor. J Phytopathol 157:24–32

    Article  Google Scholar 

  • Saravanakumara D, Vijayakumar C, Kumar N, Samiyappan R (2007) PGPR-induced defense responses in the tea plant against blister blight disease. Crop Prot 26:556–565

    Article  Google Scholar 

  • Scalbert A (1991) Antimicrobial properties of tannins. Phytochemistry 30:3875–3883

    Article  CAS  Google Scholar 

  • Seeram NP, Henning SM, Niu Y, Lee R, Scheuller HS, Heber D (2006) Catechin and caffeine content of green tea dietary supplements and correlation with antioxidant capacity. J Agric Food Chem 54:1599–1603

    Article  CAS  PubMed  Google Scholar 

  • Singh K, Rani A, Kumar S, Sood P, Mahajan M, Yadav SK, Singh B, Ahuja PS (2008) An early gene of the flavonoid pathway, flavanone 3-hydroxylase, exhibits a positive relationship with the concentration of catechins in tea (Camellia sinensis). Tree Physiol 28:1349–1356

    Article  CAS  PubMed  Google Scholar 

  • Singh K, Kumar S, Rani A, Gulati A, Ahuja PS (2009) Phenylalanine ammonia-lyase (PAL) and cinnamate 4-hydroxylase (C4H) and catechins (flavan-3-ols) accumulation in tea. Funct Integr Genomics 9:125–134

    Article  CAS  PubMed  Google Scholar 

  • Sowndhararajan K, Marimuthu S, Manianl S (2012) Biocontrol potential of phylloplane bacterium Ochrobactrum anthropi BMO-111 against blister blight disease of tea. J Appl Microbiol 114:209–218

    Article  PubMed  Google Scholar 

  • Sticher L, Mauch-Mani B, Metraux JP (1997) Systemic acquired resistance. Ann Rev Phytopathol 35:235–270

    Article  CAS  Google Scholar 

  • Tanner GJ, Franki KT, Abrahams S, Watson JM, Larkin PJ, Ashton AR (2003) Purification, properties and cloning of leucoanthocyanidin NADPH reductase from Desmodium uncinatum. J Biol Chem 278:31647–31656

  • Taşgin E, Atici O, Nalbantoğlu B, Popova LP (2006) Effects of salicylic acid and cold treatments on protein levels and on the activities of antioxidant enzymes in the apoplast of winter wheat leaves. Phytochemistry 67:710–715

    Article  PubMed  Google Scholar 

  • Tian SP, Qin GZ, Xu Y (2006) Induction of defense responses against Alternaria rot by different elicitors in harvested pear fruit. Appl Microbiol Biotechnol 70:729–734

    Article  CAS  PubMed  Google Scholar 

  • Treutter D, Feucht W (1990) The pattern of flavan-3-ols in relation to scab resistance of apple cultivars. J Hortic Sci 65:511–517

    CAS  Google Scholar 

  • Treutter D, Feucht W (1999) The role of flavan-3-ols and proanthocyanidin in plant defense. In: Dakshini KMM, Foy CL (eds) Principles and practices of plant ecology. CRC Press, Boca Raton, pp 307–338

    Google Scholar 

  • Velazhahan R, Muthukrishnan S (2003/2004) Transgenic tobacco plants constitutively overexpressing a rice thaumatin-like protein (PR-5) show enhanced resistance to Alternaria alternata. Biol Plant 47:347–54

  • Vivekananthan R, Ravi M, Ramanathan A, Samiyappan R (2004) Lytic enzymes induced by Pseudomonas fluorescens and other biocontrol organisms mediate defence against the anthracnose pathogen in mango. World J Microbiol Biotechnol 20:235–244

    Article  CAS  Google Scholar 

  • Walling LL (2001) Induced resistance: from the basic to the applied. Trends Plant Sci 6:445–447

    Article  CAS  Google Scholar 

  • Walters D, Walsh D, Newton A, Lyon G (2005) Induced resistance for plant disease control: maximizing the efficacy of resistance elicitors. Phytopathol 95:1368–1373

    Article  CAS  Google Scholar 

  • White PJ, Broadley MR (2003) Calcium in plants. Ann Bot (London) 92:487–511

    Article  CAS  Google Scholar 

  • Xie DY, Sharma SB, Pavia NL, Ferreira D, Dixon R (2003) Role of anthocyanidin reductase, encoded by BANYULS in plant flavonoid biosynthesis. Science 299:396–399

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi T, Ueki J, Minami E, Shibuya N (2005) Elicitor-induced activation of phospholipases plays an important role for the induction of defense responses in suspension-cultured rice cells. Plant Cell Physiol 46:579–587

    Article  CAS  PubMed  Google Scholar 

  • Yan JQ, Cao JK, Jiang WB, Zhao YM (2012) Effects of preharvest oligochitosan sprays on portharvest fungal disease, storage quality, and defense responses in jujube (Zizyphus jujuba Mill. cv. Dongzao) fruit. Sci Hortic 142:196–204

    Article  CAS  Google Scholar 

  • Yang SY, Chen YL, Feng LY, Yang E, Su XG, Jiang YM (2011) Effect of Methyl jasmonate on pericarp browning of postharvest lychees. J Food Process Preserv 35:417–422

    Article  CAS  Google Scholar 

  • Yao L, Jiang Y, Datta N, Singanusong R, Liu X, Duan J, Raymont K, Lisle A, Xu Y (2004) HPLC analyses of flavanols and phenolic acids in the fresh young shoots of tea (Camellia sinensis) grown in Australia. Food Chem 84:253–263

    Article  CAS  Google Scholar 

  • Zago E, Morsa S, Dat JF, Alard P, Ferrarini A, Inze D, Delledonne M, Van Breusegem F (2006) Nitric oxide- and hydrogen peroxide-responsive gene regulation during cell death induction in tobacco. Plant Physiol 141:404–411

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhao MG, Zhao X, Wu YX, Zhang LX (2007) Enhanced sensitivity to oxidative stress in an Arabidopsis nitric oxide synthase mutant. J Plant Physiol 164:737–745

    Article  CAS  PubMed  Google Scholar 

  • Zieslin N, Ben Zaken R (1993) Peroxidase activity and presence of phenolic substances in peduncles of rose flowers. Plant Physiol Biochem 31:333–339

    CAS  Google Scholar 

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Acknowledgments

Financial support for the research work and fellowship by the Tea Board of India, Ministry of Commerce is gratefully acknowledged.

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Authors and Affiliations

  1. Molecular and Applied Mycology and Plant Pathology Laboratory, Department of Botany, University of Calcutta, 35, Ballygunge Circular Road, Kolkata, 700019, West Bengal, India

    Swarnendu Chandra, Nilanjan Chakraborty & Krishnendu Acharya

  2. Darjeeling Tea Research & Development Centre, Tea Board of India, Acharya Bhanu Path, Kurseong, 734203, West Bengal, India

    Amrita Chakraborty & Ripen Rai

  3. Directorate of Research, Tea Board of India, 14, B.T.M. Sarani, Kolkata, 700001, West Bengal, India

    Swarnendu Chandra & Biswajit Bera

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  1. Swarnendu Chandra
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  2. Nilanjan Chakraborty
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Chandra, S., Chakraborty, N., Chakraborty, A. et al. Abiotic Elicitor-Mediated Improvement of Innate Immunity in Camellia sinensis . J Plant Growth Regul 33, 849–859 (2014). https://doi.org/10.1007/s00344-014-9436-y

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