Skip to main content
Log in

Jasmonic Acid-Mediated-Induced Resistance in Groundnut (Arachis hypogaea L.) Against Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae)

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Jasmonic acid (JA) acts as a signal molecule to induce resistance in plants against herbivores and its levels are elevated in plants after wounding or insect damage. Groundnut is an important crop in many tropical and subtropical regions worldwide, but there is surprisingly little knowledge on its induced defenses against herbivores. The effect of JA as a spray on induced resistance in three groundnut genotypes, namely, ICGV 86699 (resistant), NCAc 343 (resistant), and TMV 2 (susceptible), against Helicoverpa armigera was studied. The activity of oxidative enzymes [peroxidase (POD) and polyphenol oxidase (PPO)] and the amounts of other host plant defense components [total phenols, hydrogen peroxide (H2O2), malondialdehyde (MDA), and protein content] were recorded at 24, 48, 72, and 96 h after pretreatment (1 day) with JA followed by infestation with H. armigera (PJA + HIN) and H. armigera infestation with simultaneous JA application (HIN + JA) to understand the consequences of induced resistance in groundnut. The plant damage, larval survival, and larval weights were also recorded. There was a significant increase in POD and PPO activities and in the amounts of total phenols, H2O2, MDA, and proteins in PJA + HIN- and JA + HIN-treated plants as compared to the plants treated with JA and infested with H. armigera individually and to untreated control plants. Among all the genotypes, the strongest induction of defense was observed in the ICGV 86699 genotype. It is concluded that pretreatment with JA and its application during low levels of insect infestation can increase the levels of host plant resistance against herbivorous insects and reduce the pest-associated losses in groundnut.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Agrawal AA (2000) Benefits and costs of induced plant defense for Lepidium virginicum (Brassicaceae). Ecology 81:1804–1813

    Google Scholar 

  • Allison SD, Schultz JC (2004) Differential activity of peroxidase isozyme in response to wounding, gypsy moth and plant hormones in northern red oak (Quercus rubra L.). J Chem Ecol 30:1363–1379

    Article  PubMed  CAS  Google Scholar 

  • Arimura G, Matsui K, Takabayashi J (2009) Chemical and molecular ecology of herbivore-induced plant volatiles: proximate factors and their ultimate functions. Plant Cell Physiol 50:911–923

    Article  PubMed  CAS  Google Scholar 

  • Ballhorn DJ (2011) Constraints of simultaneous resistance to a fungal pathogen and an insect herbivore in lima bean (Phaseolus lunatus L.). J Chem Ecol 37:141–144

    Article  PubMed  CAS  Google Scholar 

  • Ballhorn DJ, Pietrowski A, Lieberei R (2010) Direct trade-off between cyanogenesis and resistance to a fungal pathogen in lima bean (Phaseolus lunatus L.). J Ecol 98:226–236

    Article  CAS  Google Scholar 

  • Barbehenn R, Dukatz C, Holt C, Reese A, Martiskainen O, Salminen JP, Yip L, Tran L, Constable CP (2010) Feeding on poplar leaves by caterpillars potentiates foliar peroxidase action in their guts and increase plant resistance. Oecologia 164:993–1004

    Article  PubMed  Google Scholar 

  • Bhonwong A, Stout MJ, Attajarusit J, Tantasawat P (2009) Defensive role of tomato polyphenol oxidase against cotton bollworm (Helicoverpa armigera) and Beet armyworm (Spodoptera exigua). J Chem Ecol 35:28–38

    Article  PubMed  CAS  Google Scholar 

  • Boka K, Orban N, Kristof Z (2007) Dynamics and localization of H2O2 production in elicited plant cells. Protoplasma 230:89–97

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Bruinsma M, Dicke M (2008) Herbivore-induced indirect defense: from induction mechanisms to community ecology. In: Schaller A (ed) Induced plant resistance to herbivory. Springer Verlag, Berlin, pp 31–60

    Chapter  Google Scholar 

  • Carmak I, Horst JH (1991) Effects of aluminum on lipid peroxidation, superoxide dismutase, catalase and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468

    Article  Google Scholar 

  • Chaman ME, Corcuera LJ, Zuniga GE, Cardemil L, Argandona VH (2001) Induction of soluble and cell wall peroxidases by aphid infestation in barley. J Agric Food Sci 49:2249–2253

    Article  CAS  Google Scholar 

  • Chen Y, Ni X, Buntin GD (2009) Physiological, nutritional and biochemical bases of corn resistance to foliage-feeding fall armyworm. J Chem Ecol 35:297–306

    Article  PubMed  Google Scholar 

  • Cipollini DF, Enright S, Traw MB, Bergelson J (2004) Salicylic acid inhibits jasmonic acid-induced resistance of Arabidopsis thaliana to Spodoptera exigua. Mol Ecol 13:1643–1653

    Article  PubMed  CAS  Google Scholar 

  • Food and Agriculture Organization (2007) FAOSTAT database. http://www/FAO.org. Accessed 5 Jan 2011

  • Franceschi V, Krokene P, Christiansen E, Krekling T (2005) Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytol 167:353–376

    Article  PubMed  CAS  Google Scholar 

  • Gechev T, Gadjev I, Van Breusegem F, Inze D, Dukiandjiev S, Toneva V, Minkov I (2002) Hydrogen peroxide protects tobacco from oxidative stress by inducing a set of antioxidant enzymes. Cell Mol Life Sci 59:708–714

    Article  PubMed  CAS  Google Scholar 

  • Gould N, Reglinski T, Northcott GL, Spiers M, Taylor JT (2009) Physiological and biochemical responses in Pinus radiata seedlings associated with methyl jasmonate-induced resistance to Diplodia pinea. Physiol Mol Plant Pathol 74:121–128

    Article  CAS  Google Scholar 

  • Gulsen O, Eickhoff T, Heng-Moss T, Shearman R, Baxendale F, Sarath G, Lee D (2010) Characterization of peroxidase changes in resistant and susceptible warm-season turf grasses challenged by Blissus occiduus. Arthropod Plant Interact 4:45–55

    Article  Google Scholar 

  • Guo XX, Yang XQ, Yang RY, Zeng QP (2010) Salicylic acid and methyl jasmonate but not Rose Bengal enhance artemisinin production through invoking burst of endogenous singlet oxygen. Plant Sci 178:390–397

    Article  CAS  Google Scholar 

  • Halitschke R, Baldwin IT (2005) Jasmonates and related compounds in plant–insect interactions. J Plant Growth Regul 23:238–245

    Google Scholar 

  • Hamm JC, Stout MJ, Riggio RM (2010) Herbivore- and elicitor-induced resistance in rice to the rice water weevil (Lissorhoptrus oryzophilus Kuschel) in the laboratory and field. J Chem Ecol 36:192–199

    Article  PubMed  CAS  Google Scholar 

  • Han Y, Wang Y, Bi JL, Yang XQ, Huang Y, Zhao X, Hu Y, Cai QN (2009) Constitutive and induced resistance in aphid-resistant and aphid-susceptible cultivars of wheat. J Chem Ecol 35:176–182

    Article  PubMed  CAS  Google Scholar 

  • He J, Chen F, Chen S, Lv G, Deng Y, Fang Z, Guan Z, He C (2010) Chrysanthemum leaf epidermal surface morphology and antioxidant and defense enzyme activity in response to aphid infestation. J Plant Physiol 168:687–693

    Article  PubMed  Google Scholar 

  • Heng-Moss TM, Sarath G, Baxendale F, Novak D, Bose S, Ni X, Quisenberry S (2004) Characterization of oxidative enzyme changes in buffalograsses challenged by Blissus occiduus. J Econ Entomol 97:1086–1095

    Article  PubMed  CAS  Google Scholar 

  • Huang W, Zhikuan J, Qingfang H (2007) Effects of herbivore stress by Aphis medicaginis Koch on the malondialdehyde contents and activities of protective enzymes in different alfalfa varieties. Acta Ecol Sin 27(6):2177–2183

    Article  CAS  Google Scholar 

  • Johnson KS, Felton GW (2001) Plant phenolics as dietary antioxidants for herbivorous insects: a test with genetically modified tobacco. J Chem Ecol 27:2579–2597

    Article  PubMed  CAS  Google Scholar 

  • Karban R (2011) The ecology and evolution of induced resistance against herbivores. Func Ecol 25:339–347

    Article  Google Scholar 

  • Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299–328

    Article  PubMed  CAS  Google Scholar 

  • Kranthi KR, Jadhav DR, Kranthi S, Wanjari RR, Ali SS, Russel DA (2002) Insecticide resistance in five major insect pests of cotton in India. Crop Prot 21:449–460

    Article  CAS  Google Scholar 

  • Lawrence PK, Koundal KR (2002) Plant protease inhibitors in control of phytophagous insects EJB Electron. J Biotechnol 5:93–109

    Google Scholar 

  • Maffei ME, Mithofer A, Arimura GI, Uchtenhagen H, Bossi S, Bertea CM, Cucuzza LS, Novero M, Volpe V, Quadro S, Boland W (2006) Effects of feeding Spodoptera littoralis on lima bean leaves. III. Membrane depolarization and involvement of hydrogen peroxide. Plant Physiol 140:1022–1035

    Article  PubMed  CAS  Google Scholar 

  • Maffei ME, Mithofer A, Boland W (2007) Insects feeding on plants: Rapid signals and responses preceding the induction of phytochemical release. Phytochemistry 68:2946–2959

    Article  PubMed  CAS  Google Scholar 

  • Mahanil S, Attajarusit J, Stout MJ, Thipyapong P (2008) Overexpression of tomato polyphenol oxidase increases resistance to common cutworm. Plant Sci 174:456–466

    Article  CAS  Google Scholar 

  • Mayer AM, Harel E (1979) Polyphenol oxidases in plant. Phytochemistry 18:193–215

    Article  CAS  Google Scholar 

  • Miranda M, Ralph SG, Mellway R, White R, Heath MC, Bohlmann J, Constabel CP (2007) The transcriptional response of hybrid poplar (Populus trichocarpa × P. deltoides) to infection by Melampsora medusae leaf rust involves induction of flavonoid pathway genes leading to the accumulation of proanthocyanidins. Mol Plant Microbe Interact 20:816–831

    Article  PubMed  CAS  Google Scholar 

  • Moloi MJ, van der Westhuizen AJ (2006) The reactive oxygen species are involved in resistance responses of wheat to the Russian wheat aphid. J Plant Physiol 163:1118–11125

    Article  PubMed  CAS  Google Scholar 

  • Moreira X, Sampedro L, Zas R (2009) Defensive responses of Pinus pinaster seedlings to exogenous application of methyl jasmonate: concentration effect and systemic response. Environ Exp Bot 67:94–100

    Article  CAS  Google Scholar 

  • Noreen Z, Ashraf M (2009) Change in antioxidant enzymes and some key metabolites in some genetically diverse cultivars of radish (Raphanus sativus L.). Environ Exp Bot 67:395–402

    Article  CAS  Google Scholar 

  • Orozco-Cárdenas ML, Narvaez-Vasquez J, Ryan CA (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin and methyl jasmonate. Plant Cell 13:179–191

    Article  PubMed  Google Scholar 

  • Piotrowska A, Bajgu A, Czerpak R, Kot K (2010) Changes in the growth, chemical composition, and antioxidant activity in the aquatic plant Wolffia arrhiza (L.) Wimm. (Lemnaceae) exposed to jasmonic acid. J Plant Growth Regul 29:53–62

    Article  CAS  Google Scholar 

  • Raj SN, Sarosh BR, Shetty HS (2006) Induction and accumulation of polyphenol oxidase activities as implicated in development of resistance against pearl millet downy mildew disease. Func Plant Biol 33:563–571

    Article  CAS  Google Scholar 

  • Ramiro DA, Guerreiro-Filho O, Mazzafera P (2006) Phenol contents, oxidase activities, and the resistance of coffee to the leaf miner Leucoptera coffeella. J Chem Ecol 32:1977–1988

    Article  PubMed  CAS  Google Scholar 

  • Reymond P, Farmer EE (1998) Jasmonate and salicylate as global signals for defense gene expression. Curr Opin Plant Biol 5:404–411

    Article  Google Scholar 

  • Scott MI, Thaler SJ, Scott GF (2010) Response of a generalist herbivore Trichoplusia ni to jasmonate-mediated induced defense in tomato. J Chem Ecol 36:490–499

    Article  PubMed  CAS  Google Scholar 

  • Senthil-Nathan S, Kalaivani K, Choi MY, Paik CH (2009) Effects of jasmonic acid-induced resistance in rice on the plant brownhopper, Nilaparvata lugens Stal (Homoptera: Delphacidae). Pestic Biochem Physiol 95:77–84

    Article  CAS  Google Scholar 

  • Sethi A, McAuslane HJ, Rathinasabapathi B, Nuessly GS, Nagata RT (2009) Enzyme induction as a possible mechanism for latex-mediated insect resistance in romaine lettuce. J Chem Ecol 35:190s–200s

    Article  Google Scholar 

  • Shannon LM, Kay E, Lew JY (1966) Peroxidase isozymes from horseradish roots. Isolation and physical properties. J Biol Chem 241:2166–2172

    PubMed  CAS  Google Scholar 

  • Sharma HC, Pampathy G, Dwivedi SL, Reddy LJ (2003) Mechanism and diversity of resistance to insect pests in wild relatives of groundnut. J Econ Entomol 96:1886–1897

    Article  PubMed  CAS  Google Scholar 

  • Sharma HC, Pampathy G, Dhillon MK, Ridsdill-Smith JT (2005) Detached leaf assay to screen for host plant resistance to Helicoverpa armigera. J Econ Entomol 98(2):568–576

    Article  PubMed  Google Scholar 

  • Sharma HC, Sujana G, Rao DM (2009) Morphological and chemical components of resistance to pod borer, Helicoverpa armigera in wild relatives of pigeonpea. Arthropod Plant Interact 3(3):151–161

    Article  Google Scholar 

  • Shivaji R, Camas A, Ankala A, Engelberth J, Tumlinson JH, Williams WP, Wilkinson JR, Luthe DS (2010) Plants on constant alert: elevated levels of jasmonic acid and jasmonate-induced transcripts in caterpillar-resistant maize. J Chem Ecol 36:179–191

    Article  PubMed  CAS  Google Scholar 

  • Stout MJ, Fidantsef AL, Duffey SS, Bostock RM (1999) Signal interactions in pathogen and insect attack: systemic plant-mediated interactions between pathogens and herbivores of the tomato, Lycopersicon esculentum. Physiol Mol Plant Pathol 54:97–114

    Article  Google Scholar 

  • Thaler JS, Stout MJ, Karban R, Duffey SS (2001) Jasmonate-mediated induced plant resistance affects a community of herbivores. Ecol Entomol 216:312–324

    Article  Google Scholar 

  • Thipyapong P, Mahanil S, Bhonwong A, Attajarusit J, Stout MJ, Steffens JC (2006) Increasing resistance of tomato to lepidopteran insects by overexpression of polyphenol oxidase. In: Ashcroft WJ (ed), Proceedings of the ninth international symposium on processing the tomato. November 15–18, 2004, Australia: Melbourne. Acta Hortic 724:29–38

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Usha Rani P, Jyothsna Y (2010) Biochemical and enzymatic changes in rice as a mechanism of defense. Acta Physiol Plant 32:695–701

    Article  Google Scholar 

  • Venu RC, Madhav MS, Sreerekha MV, Nobuta K, Zhang Y, Carswell P, Boehm MJ, Meyers BC, Korth KL, Wang GL (2010) Deep and comparative transcriptome analysis of rice plants infested by the beet armyworm (Spodoptera exigua) and water weevil (Lissorhoptrus oryzophilus). Rice 3:22–35

    Article  Google Scholar 

  • Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216

    PubMed  CAS  Google Scholar 

  • Wang JH, Constabel CP (2004) Three polyphenol oxidases from hybrid poplar are differentially expressed during development and after wounding and elicitor treatment. Physiol Plant 122:344–353

    Article  CAS  Google Scholar 

  • Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697

    Article  PubMed  CAS  Google Scholar 

  • Wu G, Jiang S, Miyata T (2004) Effects of synergists on toxicity of six insecticides in parasitoid Diaeretiella rapae (Hymenoptera: Aphidiidae). J Econ Entomol 97:2057–2066

    Article  PubMed  CAS  Google Scholar 

  • Zavala JA, Patankar AG, Gase K, Hui D, Baldwin IT (2004) Manipulation of endogenous trypsin proteinase inhibitor production in Nicotiana attenuata demonstrates their function as antiherbivore defenses. Plant Physiol 134:1181–1190

    Article  PubMed  CAS  Google Scholar 

  • Zhang SZ, Hau BZ, Zhang F (2008) Induction of the activities of antioxidative enzymes and the levels of malondialdehyde in cucumber seedlings as a consequence of Bemisia tabaci (Hemiptera: Aleyrodidae) infestation. Arthropod Plant Interact 2:209–213

    Article  Google Scholar 

  • Zhao LY, Chen JL, Cheng DF, Sun JR, Liu Y, Tian Z (2009) Biochemical and molecular characterizations of Sitobion avenae-induced wheat defense responses. Crop Prot 28:435–442

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

Download references

Acknowledgments

We are thankful to Dr. H. C. Sharma (Principal Scientist, Entomology, ICRISAT, India) for providing the seeds and for his valuable comments and suggestions. We also thank Dr. Abeshiekh Rathore and Mr. Anil Kumar of the Biometrics Laboratory, ICRISAT, for their assistance with the data analysis. The first author is grateful to the corresponding author for providing financial assistance and necessary laboratory facilities, and also for his valuable and enthusiastic discussions during the work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Savarimuthu Ignacimuthu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

War, A.R., Paulraj, M.G., War, M.Y. et al. Jasmonic Acid-Mediated-Induced Resistance in Groundnut (Arachis hypogaea L.) Against Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae). J Plant Growth Regul 30, 512–523 (2011). https://doi.org/10.1007/s00344-011-9213-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-011-9213-0

Keywords

Navigation