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Exogenous Application of Jasmonic Acid Induces Volatile Emissions in Rice and Enhances Parasitism of Nilaparvata lugens Eggs by theParasitoid Anagrus nilaparvatae

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Abstract

Jasmonate signaling pathway plays an important role in induced plant defense against herbivores and pathogens, including the emission of volatiles that serve as attractants for natural enemies of herbivores. We studied the volatiles emitted from rice plants that were wounded and treated with jasmonic acid (JA) and their effects on the host-searching behavior of the rice brown planthopper, Nilaparvata lugens (Stål), and its mymarid egg parasitoid Anagrus nilaparvatae Pang et Wang. Female adults of N. lugens significantly preferred to settle on JA-treated rice plants immediately after release. The parasitoid A. nilaparvatae showed a similar preference and was more attracted to the volatiles emitted from JA-treated rice plants than to volatiles from control plants. This was also evident from greenhouse and field experiments in which parasitism of N. lugens eggs by A. nilaparvatae on plants that were surrounded by JA-treated plants was more than twofold higher than on control plants. Analyses of volatiles collected from rice plants showed that JA treatment dramatically increased the release of volatiles, which included aliphatic aldehydes and alcohols, monoterpenes, sesquiterpenes, methyl salicylate, n-heptadecane, and several as yet unidentified compounds. These results confirm an involvement of the JA pathway in induced defense in rice plants and demonstrate that the egg parasitoid A. nilaparvatae exploits plant-provided cues to locate hosts. We explain the use of induced plant volatiles by the egg parasitoid by a reliable association between planthopper feeding damage and egg presence.

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References

  • A. A. Agrawal (1999) ArticleTitleInduced responses to herbivory in wild radish: Effects on several herbivores and plant fitness Ecology 80 1713–1723

    Google Scholar 

  • A. A. Agrawal (2000) ArticleTitleSpecificity of induced resistance in wild radish: causes and consequences for two specialist and two generalist caterpillars Oikos 89 493–500 Occurrence Handle10.1034/j.1600-0706.2000.890308.x

    Article  Google Scholar 

  • A. A. Agrawal M. F. Sherriffs (2001) ArticleTitleInduced plant resistance and susceptibility to late-season herbivores of wild radish Ann. Entomol. Soc. Am. 94 71–75

    Google Scholar 

  • H. Alborn T. C. J. Turlings T. H. Jones G. Stenhagen J. H. Loughrin J. H. Tumlinson (1997) ArticleTitleAn elicitor of plant volatiles from beet armyworm oral secretion Science 276 945–949 Occurrence Handle10.1126/science.276.5314.945

    Article  Google Scholar 

  • P. Barbosa P. Gross J. Kemper (1991) ArticleTitleInfluence of plant allelochemicals on the tobacco hornworm and its parasitoid, Cotesia congregata Ecology 72 1567–1575

    Google Scholar 

  • C. A. Black R. Karban L. D. Godfery J. Granett W. E. Chaney (2003) ArticleTitleJasmonic acid: a vaccine against leafminers (Diptera: Agromyzidae) in celery Environ. Entomol. 32 1196–1202

    Google Scholar 

  • W. Boland J. Hopke J. Donath J. Nüske F. Bublitz (1995) ArticleTitleJasmonic acid and coronatin induce odor production in plants Angew. Chem., Int. Ed. Engl. 34 1600–1602

    Google Scholar 

  • J. Cheng J. He (1996) Rice Insect Pests China Agricultural Press Beijing

    Google Scholar 

  • M. Dicke (1999) Specificity of herbivore-induced plant defences D. J. Chadwick J. Goode (Eds) Insect–Plant Interactions and Induced Plant Defence. Novartis Foundation Symposium 223 Wiley Chichester, United Kingdom 43–59

    Google Scholar 

  • M. Dicke R. Gols D. Ludeking M. A. Posthumus (1999) ArticleTitleJasmonic acid and herbivory differentially induce carnivore-attracting plant volatiles in lima bean plants J. Chem. Ecol. 25 1907–1922

    Google Scholar 

  • R. Gols M. Roosjen H. Dijkman M. Dicke (2003) ArticleTitleInduction of direct and indirect plant responses by jasmonic acid, low spider mite densities, or a combination of jasmonic acid treatment and spider mite infestation J. Chem. Ecol. 29 2651–2666 Occurrence Handle10.1023/B:JOEC.0000008010.40606.b0 Occurrence Handle14969353

    Article  PubMed  Google Scholar 

  • S. Gouinguene H. Alborn T. C. J. Turlings (2003) ArticleTitleInduction of volatile emissions in maize by different larval instars of Spodoptera littoralis J. Chem. Ecol. 29 145–162 Occurrence Handle10.1023/A:1021984715420 Occurrence Handle12647859

    Article  PubMed  Google Scholar 

  • R. Halitschke I. T. Baldwin (2003) ArticleTitleAntisense LOX expression increases herbivore performance by decreasing defense responses and inhibiting growth-related transcriptional reorganization in Nicotiana attenuata Plant J. 36 794–807 Occurrence Handle10.1046/j.1365-313X.2003.01921.x Occurrence Handle14675445

    Article  PubMed  Google Scholar 

  • R. Halitschke A. Kessler J. Kahl A. Lorenz I. T. Baldwin (2000) ArticleTitleEcophysiological comparison of direct and indirect defenses in Nicotiana attenuata Oecologia 124 408–417 Occurrence Handle10.1007/s004420000389

    Article  Google Scholar 

  • R. Halitschke U. Schittko G. Pohnert W. Boland I. T. Baldwin (2001) ArticleTitleMolecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses Plant Physiol. 125 711–717 Occurrence Handle10.1104/pp.125.2.711 Occurrence Handle11161028

    Article  PubMed  Google Scholar 

  • B. Heath A. Manukian (1994) ArticleTitleAn automated system for use in collecting volatile chemicals released from plants J. Chem. Ecol. 20 593–608 Occurrence Handle10.1007/BF02059600

    Article  Google Scholar 

  • M. Hilker T. Meiners (2002) ArticleTitleInduction of plant responses towards oviposition and feeding of herbivorous arthropods: a comparison Entomol. Exp. Appl. 104 181–192 Occurrence Handle10.1023/A:1021232319226

    Article  Google Scholar 

  • M. Hilker O. Rohfritsch T. Meiners (2002) The plant’s response towards insect egg deposition M. Hilker T. Meiners (Eds) Chemoecology of Insect Eggs and Egg Deposition Blackwell Berlin 61–90

    Google Scholar 

  • J. Hopke J. Donath S. Blechert W. Boland (1994) ArticleTitleHerbivore-induced volatiles: The emission of acyclic homoterpenes from leaves of Phaseolus lunatus and Zea mays can be triggered by a beta-glucosidase and jasmonic acid FEBS Lett. 352 146–150 Occurrence Handle10.1016/0014-5793(94)00948-1 Occurrence Handle7925964

    Article  PubMed  Google Scholar 

  • R. Karban I. T. Baldwin (1997) Induced Responses to Herbivory University of Chicago Press Chicago, IL

    Google Scholar 

  • R. Karban A. A. Agrawal M. Mangel (1997) ArticleTitleThe benefits of induced defences against herbivores Ecology 78 1351–1355

    Google Scholar 

  • A. Kessler I. T. Baldwin (2001) ArticleTitleDefensive function of herbivore-induced plant volatile emissions in nature Science 291 2141–2144 Occurrence Handle10.1126/science.291.5511.2141 Occurrence Handle11251117

    Article  PubMed  Google Scholar 

  • A. Kessler I. T. Baldwin (2002) ArticleTitlePlant responses to insect herbivory: the emerging molecular analysis Annu. Rev. Plant Biol. 53 299–328 Occurrence Handle10.1146/annurev.arplant.53.100301.135207 Occurrence Handle12221978

    Article  PubMed  Google Scholar 

  • S. T. Kim S. Yu K. S. Cho S. G. Kim J. C. Hong H.-D. Han H.-D. Bae M. H. Nam K. Y. Kang (2003) ArticleTitleProteomic analysis of differentially expressed proteins induced by rice blast fungus and elicitor in suspension-cultured rice cells Proteomics 3 2366–2378

    Google Scholar 

  • P. J. Landolt J. H. Tumlinson D. H. Alborn (1999) ArticleTitleAttraction of Colorado potato beetle (Coleoptera: Chrysomelidae) to damaged and chemically induced potato plants Environ. Entomol. 28 973–978

    Google Scholar 

  • F. Liu Y. Lou J. Cheng (2002) ArticleTitleVolatiles-mediated intra- and interspecific interactions of the rice brown planthopper, Nilaparvata lugens, and the white-backed planthopper, Sogatella furcifera Chin. J. Rice Sci. 16 162–166

    Google Scholar 

  • Y. Lou I. T. Baldwin (2003) ArticleTitleManduca sexta recognition and resistance among allopolyploid Nicotiana host plants Proc. Natl. Acad. Sci. USA 100 14581–14586 Occurrence Handle10.1073/pnas.2135348100 Occurrence Handle14530394

    Article  PubMed  Google Scholar 

  • Y. Lou I. T. Baldwin (2004) ArticleTitleNitrogen supply influences herbivore-induced direct and indirect defenses and transcriptional responses in Nicotiana attenuata Plant Physiol. 135 496–506 Occurrence Handle10.1104/pp.104.040360 Occurrence Handle15133153

    Article  PubMed  Google Scholar 

  • Y. Lou J. Cheng (1994) ArticleTitleThe kairomone from Nilaparvata lugens (Stål) and its relation to rice varieties Acta Phytophylacica Sin. 21 327–332

    Google Scholar 

  • Y. Lou J. Cheng (1996) ArticleTitleThe behavioral responses of Anagrus nilaparvatae Pang et Wang to the volatile of rice varieties Entomol. J. East China 5 60–64

    Google Scholar 

  • Y. Lou J. Cheng (2003) ArticleTitleRole of rice volatiles in the foraging behaviour of the predator Cyrtorhinus lividipennis Reuter for the rice brown planthopper Nilaparvata lugens (Stål) Biocontrol 48 73–86 Occurrence Handle10.1023/A:1021291427256

    Article  Google Scholar 

  • Lou, Y., Cheng, J., and Du, M. 1999. Role of rice volatiles in the host selection behavior of the parasitoid, Anagrus nilaparvatae Pang et Wang: isolation and identification of volatile rice synomone, p. 608, in G. Zhou (ed.). First Annual Meeting of Science Society of China: Science and Technology Progress and Society and Economy Development Beyond 2000. Science and Technology Press of China, Beijing, China.

  • Y. Lou J. Cheng X. Ping F. Tang S. Ru M. Du (2002) ArticleTitleMechanisms on host discrimination between two hosts Nilaparvata lugens and Sogatella furcifera by the egg parasitoid Anagrus nilaparvatae Acta Entomol. Sin. 45 770–776

    Google Scholar 

  • L. Mattiacci M. Dicke M. A. Posthumus (1995) ArticleTitleBeta-glucosidase: an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps Proc. Natl. Acad. Sci. USA 92 2036–2040 Occurrence Handle11607516

    PubMed  Google Scholar 

  • T. Meiners M. Hilker (2000) ArticleTitleInduction of plant synomones by oviposition of a phytophagous insect J. Chem. Ecol. 26 221–232 Occurrence Handle10.1023/A:1005453830961

    Article  Google Scholar 

  • N. Obara M. Hasegawa O. Kodama (2002) ArticleTitleInduced volatiles in elicitor-treated rice blast fungus-inoculated rice leaves Biosci. Biotechnol. Biochem. 66 2549–2559 Occurrence Handle10.1271/bbb.66.2549 Occurrence Handle12596847

    Article  PubMed  Google Scholar 

  • R. Ozawa K. Shiojiri M. W. Sabelis G.-I. Arimura T. Nishioka J. Takabayashi (2004) ArticleTitleCorn plants treated with jasmonic acid attract more specialist parasitoids, thereby increasing parasitization of the common armyworm J. Chem. Ecol. 30 1797–1808 Occurrence Handle10.1023/B:JOEC.0000042402.04012.c7 Occurrence Handle15586675

    Article  PubMed  Google Scholar 

  • R. Rakwal S. Komatsu (2000) ArticleTitleRole of jasmonate in the rice (Oryza sativa L.) self-defense mechanism using proteome analysis Electrophoresis 21 2492–2500 Occurrence Handle10.1002/1522-2683(20000701)21:12<2492::AID-ELPS2492>3.0.CO;2-2 Occurrence Handle10939463

    Article  PubMed  Google Scholar 

  • R. Rakwal G. K. Agrawal N.-S. Jwa (2001) ArticleTitleCharacterization of a rice (Oryza sativa L.) Bowman-Birk proteinase inhibitor: tightly light regulated induction in response to cut, jasmonic acid, ethylene and protein phosphatase 2A inhibitors Gene 263 189–198 Occurrence Handle10.1016/S0378-1119(00)00573-4 Occurrence Handle11223257

    Article  PubMed  Google Scholar 

  • E. Rubia-Sanchez Y. Suzuki K. Miyamoto T. Watanabe (1999) ArticleTitleThe potential for compensation of the effects of the brown planthopper Nilaparvata lugens (Stål) (Homoptera: Delphacidae) feeding on rice Crop Prot. 18 39–45 Occurrence Handle10.1016/S0261-2194(98)00087-8

    Article  Google Scholar 

  • M. Sabelis A. Janssen A. Pallini M. Venzon J. Bruin B. Drukker P. Scutareanu (1999) Behavioral responses of predatory and herbivorous arthropods to induced plant volatiles: from evolutionary ecology to agricultural applications A. A. Agrawal S. Tuzun E. Bent (Eds) Induced Plant Defenses Against Pathogens and Herbivores APS Press Saint Paul, MN 269–296

    Google Scholar 

  • E. A. Schmelz H. T. Alborn J. H. Tumlinson (2001) ArticleTitleThe influence of intact-plant and excised-leaf bioassay designs on volicitin- and jasmonic acid-induced sesquiterpene volatile release in Zea mays Planta 214 171–179 Occurrence Handle11800380

    PubMed  Google Scholar 

  • E. A. Schmelz H. T. Alborn E. Banchio J. H. Tumlinson (2003) ArticleTitleQuantitative relationships between induced jasmonic acid levels and volatile emission in Zea mays during Spodoptera exigua herbivory Planta 216 665–673 Occurrence Handle12569409

    PubMed  Google Scholar 

  • Y. Suzuki K. Sogawa Y. Seino (1996) ArticleTitleOvicidal reaction of rice plants against the whitebacked planthopper, Sogatella furcifera Horváth (Homoptera: Delphacidae) Appl. Entomol. Zool. 31 111–118

    Google Scholar 

  • B. Sznajder J. A. Harvey (2003) ArticleTitleSecond and third trophic level effects of differences in plant species reflect dietary specialisation of herbivores and their endoparasitoids Entomol. Exp. Appl. 109 73–82 Occurrence Handle10.1046/j.1570-7458.2003.00096.x

    Article  Google Scholar 

  • S. Tamogamia R. Rakwalb O. Kodamaa (1997) ArticleTitlePhytoalexin 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 Occurrence Handle10.1016/S0014-5793(97)00743-6 Occurrence Handle9257690

    Article  PubMed  Google Scholar 

  • J. S. Thaler (1999) ArticleTitleJasmonate-inducible plant defences cause increased parasitism of herbivores Nature 399 686–688 Occurrence Handle10.1038/21420

    Article  Google Scholar 

  • T. C. J. Turlings F. L. Wäckers (2004) Recruitment of predators and parasitoids by herbivore-damaged plants R. T. Cardé J. Millar (Eds) Advances in Insect Chemical Ecology Cambridge University Press Cambridge 21–75

    Google Scholar 

  • T. C. J. Turlings U. B. Lengwiler M. L. Bernasconi D. Wechsler (1998) ArticleTitleTiming of induced volatile emissions in maize seedlings Planta 207 146–152 Occurrence Handle10.1007/s004250050466

    Article  Google Scholar 

  • L. E. M. Vet M. Dicke (1992) ArticleTitleEcology of infochemicals use by natural enemies in a tritrophic context Annu. Rev. Entomol. 37 141–172 Occurrence Handle10.1146/annurev.en.37.010192.001041

    Article  Google Scholar 

  • Wang, X., Du, M., Lou, Y., and Cheng, J. 2005. Jasmonates signaling pathway is not involved in the production of Nilaparvata lugens-induced rice volatiles. J. Zhejiang Uni. (Agri. and Life Sci.) (in press).

  • T. Watanabe H. Kitagawa (2000) ArticleTitlePhotosynthesis and translocation of assimilates in rice plants following phloem feeding by the planthopper Nilaparvata lugens (Homoptera: Delphacidae) J. Econ. Entomol. 93 1192–1198 Occurrence Handle10985030

    PubMed  Google Scholar 

  • M. Yamasaki A. Yoshimura H. Yasui (2003) ArticleTitleGenetic basis of ovicidal response to whitebacked planthopper (Sogatella furcifera Horváth) in rice (Oryza sativa L.) Mol. Breed. 12 133–143 Occurrence Handle10.1023/A:1026018821472

    Article  Google Scholar 

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Acknowledgments

We thank Sandrine Gouinguené, Maria Elena Hoballah, Thomas Degen, Zhou Guoxin, and Wang Xia for their invaluable assistance with laboratory work and the Ministry of Science and Technology of China (973) (G2000016208) and the National Natural Science Foundation of China (30270233) for funding.

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Authors and Affiliations

  1. Institute of Applied Entomology, Zhejiang University, Hangzhou, 310029, China

    Yong-Gen Lou, Meng-Hao Du, Jia-An Cheng & Wei-Fang Shan

  2. Institute of Zoology, University of Neuchâtel, Neuchâtel, Switzerland

    Yong-Gen Lou & Ted C. J. Turlings

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  1. Yong-Gen Lou
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  2. Meng-Hao Du
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Correspondence to Yong-Gen Lou.

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Lou, YG., Du, MH., Turlings, T.C.J. et al. Exogenous Application of Jasmonic Acid Induces Volatile Emissions in Rice and Enhances Parasitism of Nilaparvata lugens Eggs by theParasitoid Anagrus nilaparvatae. J Chem Ecol 31, 1985–2002 (2005). https://doi.org/10.1007/s10886-005-6072-9

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