Hostname: page-component-7c8c6479df-r7xzm Total loading time: 0 Render date: 2024-03-28T09:08:48.880Z Has data issue: false hasContentIssue false

Induced resistance in rice against insects

Published online by Cambridge University Press:  24 July 2007

R. Karban*
Affiliation:
Department of Entomology, University of California, Davis, CA 95616, USA
Y. Chen
Affiliation:
International Rice Research Institute, DAPO Box 7777, Metro Manila, Philippines
*
*Fax: 530-752-1537 E-mail: rkarban@ucdavis.edu

Abstract

Vaccinations are the mainstay of western preventive medicine, and they have been used to protect some crops against disease and insect pests. We consider rice as a model for protection using induced resistance since it is one of the most important staple crops and there have been significant new developments in: cross-resistance among rice insects, chemical pathways involved in induced resistance, sequencing the rice genome and expression of genes conferring resistance against rice insect pests. Insect attack has been found to cause lesions that kill planthopper eggs and early stages of gall midges. Damaged plants released volatiles that made them less likely to be chosen by planthoppers and more attractive to parasitoids. Chemical elicitors have been developed for dicotyledonous plants and these can induce resistance in rice, although rice does not fit models developed to explain signalling in dicots. For example, salicylic acid did not increase in rice after infection by pathogens and did not appear to be the mobile signal for induced resistance against pathogens although it was involved in induced responses to phloem-feeding insects. Jasmonic acid acted as a signal in some induced responses to pathogens as well as chewing insects. Many of the genes associated with induced resistance in rice have recently been mapped, and techniques are being developed to incorporate them into the genome of cultivated varieties. Attempts to control insect pests of rice will affect interactions with pathogens, predators and parasites, and other organisms in this agroecosystem.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Babu, R.M., Sajeena, A., Samundeeswari, A.V., Sreedhar, A., Vidhyasekaran, P., Seetharaman, K. & Reddy, M.S. (2003a) Induction of systemic resistance to Xanthomonas oryzae pv. oryzae by salicylic acid in Oryza sativa (L.). Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz 110, 419431.Google Scholar
Babu, R.M., Sajeena, A., Samundeeswarf, A.V., Sreedhar, A., Vidhyasekeran, P. & Reddy, M.S. (2003b) Induction of bacterial blight (Xanthomonas oryzae pv. oryzae) resistance in rice by treatment with acibenzolar-S-methyl. Annals of Applied Biology 143, 333340.CrossRefGoogle Scholar
Bandong, J.P. & Litsinger, J.A. (2005) Rice crop stage susceptibility to the rice yellow stemborer Scirpophaga incertulas (Walker) (Lepidoptera: Pyralidae). International Journal of Pest Management 51, 3743.CrossRefGoogle Scholar
Barrion, A.T., Litsinger, J.A., Medina, E.B., Aguda, R.M., Bandong, J.P., Pantua, P.C. Jr., Viajante, V.D., de la Cruz, C.G. & Vega, C.R. (1991) The rice Cnaphalocrocis and Marasmia (Lepidoptera: Pyralidae) leaffolder complex in the Philippines: taxonomy, bionomics and control. Philippine Entomologist 8, 9871074.Google Scholar
Beauverie, J. (1901) Essais d'immunization des vegetaux contre les maladies cryptogamiques. Comptes Rendus Hebdomadaires des Seances de l'Acadamie des Sciences, Paris 133, 107110.Google Scholar
Bentur, J.S. & Kalode, M.B. (1996) Hypersensitive reaction and induced resistance in rice against the Asian rice gall midge Orseolia oryzae. Entomologia Experimentalis et Applicata 78, 7781.CrossRefGoogle Scholar
Broadway, R.M. & Duffey, S.S. (1986) Plant proteinase inhibitors: mechanism of action and effect on the growth and digestive physiology of larval Heliothis zea and Spodoptera exigua. Journal of Insect Physiology 32, 827833.CrossRefGoogle Scholar
Campbell, R. (1989) The use of microbial inoculants in the biological control of plant diseases. pp. 6777in Campbell, R. & Macdonald, R.M. (Eds) Microbial inoculation of crop plants. Oxford, Oxford University Press.Google Scholar
Cartwright, D., Langcake, P., Pryce, R.J., Leworthy, D.P. & Ride, J.P. (1977) Chemical activation of host defence mechanisms as a basis for crop protection. Nature 267, 511513.CrossRefGoogle Scholar
Chatterjee, P.B. (1979) Rice leaf folder attacks in India. International Rice Research Newsletter 4 (3), 21.Google Scholar
Chern, M.S., Fitzgerald, H.A., Canlas, P.E., Navarre, D.A. & Ronald, P.C. (2005) Over-expression of a rice NPR1 homologue leads to constitutive activation of defense response and hypersensitivity to light. Molecular Plant–Microbe Interactions 18, 511520.CrossRefGoogle Scholar
Chester, K.S. (1933) The problem of acquired physiological immunity in plants. Quarterly Review of Biology 8, 129154. 275–324.CrossRefGoogle Scholar
Dale, D. (1994) Insect pests of the rice plant – their biology and ecology. pp. 363485in Heinrichs, E.A. (Ed.) Biology and management of rice insects. New York, Wiley.Google Scholar
Deacon, J.W. (1988) Biocontrol of soil-borne plant pathogens with introduced inocula. Philosophical Transactions of the Royal Society of London B 318, 249264.Google Scholar
Dhaliwal, G.S., Shahi, H.N., Gill, P.S. & Maskina, M.S. (1979) Field reaction of rice varieties to leaf folder at various nitrogen levels. International Rice Research Newsletter 4, 7.Google Scholar
Dixon, R.A., Achine, L., Kota, P., Liu, C.J., Reddy, M.S.S. & Wang, L.J. (2002) The phenylpropanoid pathway and plant defence – a genomics perspective. Molecular Plant Pathology 3, 371390.CrossRefGoogle ScholarPubMed
Farmer, E.E., Johnson, R.R. & Ryan, C.A. (1992) Regulation of expression of proteinase inhibitor genes by methyl jasmonate and jasmonic acid. Plant Physiology 98, 9951002.CrossRefGoogle ScholarPubMed
Gallagher, K.D., Kenmore, P.E. & Sogawa, K. (1994) Judicial use of insecticides deters planthopper outbreaks and extends the life of resistant varieties in Southeast Asian rice. pp. 599614in Perfect, T. (Ed.) Planthoppers: their ecology and management. New York, Chapman & Hall.CrossRefGoogle Scholar
Gorlach, J., Volrath, S., Knauf-Bleter, G., Hengy, G., Beckhove, U., Kogel, K.H., Oostendorp, M., Staub, T., Ward, E., Kessmann, H. & Ryals, J. (1996) Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell 8, 629643.Google ScholarPubMed
Green, T.R. & Ryan, C.A. (1972) Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175, 776777.CrossRefGoogle ScholarPubMed
Hait, G.M. & Sinha, A.K. (1987) Biochemical changes associated with induction of resistance in rice seedlings to Helminthosporium oryzae by seed treatment with chemicals. Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz 94, 360368.Google Scholar
Harris, M.O., Stuart, J.J., Mohan, M., Nair, S., Lamb, R.J. & Rohfritsch, O. (2003) Grasses and gall midges: plant defense and insect adaptation. Annual Review of Entomology 48, 549577.CrossRefGoogle ScholarPubMed
Haukioja, E. & Hakala, T. (1975) Herbivore cycles and periodic outbreaks. Formulation of a general hypothesis. Report of the Kevo Subarctic Research Station 12, 19.Google Scholar
Hedin, P.A. (1990) Bioregulator-induced changes in allelochemicals and their effects on plant resistance to pests. Critical Reviews in Plant Sciences 9, 371379.CrossRefGoogle Scholar
Huan, N.H., Thiet, L.V., Chien, H.V. & Heong, K.L. (2005) Farmer's participatory evaluation of reducing pesticides, fertilizers and seed rates in rice farming in the Mekong Delta, Vietnam. Crop Protection 24, 457464.CrossRefGoogle Scholar
Hu-Qi, Y., Li-Yue, R., Zheng-Yu, Hu-Xi B., Zhang-Xaio, J. & Li-Ben, J. (2005) Insecticidal activity of transgenic rice expressing CpTI or CpTI+Bt against Chilo suppressalis Walker. Journal of Fujian Agriculture and Forestry University, Natural Science Edition 34, 185188.Google Scholar
Isman, M.B. (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and the increasingly regulated world. Annual Review of Entomology 51, 4566.CrossRefGoogle ScholarPubMed
Jongsma, M.A., & Bolter, C. (1997) The adaptation of insects to plant protease inhibitors. Journal of Insect Physiology 43, 885895.CrossRefGoogle Scholar
Kagale, S., Marimuthu, T., Thayumanavan, B., Nandakumar, R. & Samiyappan, R. (2004) Antimicrobial activity and induction of systemic resistance in rice by leaf extract of Datura metel against Rhizoctonia solani and Xanthomonas oryzae pv. oryzae. Physiological and Molecular Plant Pathology 65, 91100.CrossRefGoogle Scholar
Kanno, H. & Fujita, Y. (2003) Induced systemic resistance to rice blast fungus in rice plants infested by white-backed planthopper. Entomologia Experimentalis et Applicata 107, 155158.CrossRefGoogle Scholar
Kanno, H., Satoh, M., Kimura, T. & Fujita, Y. (2005) Some aspects of induced resistance to rice blast fungus, Magnaporthe grisea, in rice plant infested by white-backed planthopper, Sogatella furcifera. Applied Entomology and Zoology 40, 9197.CrossRefGoogle Scholar
Karban, R. & Baldwin, I.T. (1997) Induced responses to herbivory. 319 pp. Chicago, University of Chicago Press.CrossRefGoogle Scholar
Karban, R. & Carey, J.R. (1984) Induced resistance of cotton seedlings to mites. Science 225, 5354.CrossRefGoogle ScholarPubMed
Kenmore, P.E., Cariño, F.O., Perez, C.A., Dyck, V.A. & Gutierrez, A.P. (1984) Population regulation of the rice brown planthopper (Nilaparvata lugens Stål) within rice fields in the Philippines. Journal of Plant Protection in the Tropics 1, 1937.Google Scholar
Khan, Z.R., Barrion, A.T., Litsinger, J.A., Castilla, N.P. & Joshi, R.C. (1988) Mini review: a bibliography of rice leaffolders (Lepidoptera: Pyralidae). Insect Science and Its Application 9, 129174.Google Scholar
Khan, Z.R., Litsinger, J.A., Barrion, A.T., Villaneuva, F.F.D., Fernandez, N.J. & Taylor, B. (1991) World bibliography of rice stem borers, 1794–1990. 415 pp. Los Banos, Philippines, International Rice Research Institute.Google Scholar
Kogel, K.H. & Langen, G. (2005) Induced disease resistance and gene expression in cereals. Cellular Microbiology 7, 15551564.CrossRefGoogle ScholarPubMed
Kuc, J. (1982) Induced immunity to plant disease. BioScience 32, 854860.Google Scholar
Kuc, J. (1995) Induced systemic resistance – an overview. pp. 169175in Hammerschmidt, R. & Kuc, J. (Eds) Induced resistance to diseases in plants. Amsterdam, Kluwer.CrossRefGoogle Scholar
Lee, A., Cho, K., Jang, S., Rakwal, R., Iwahashi, H., Agrawal, G.K., Shim, J. & Han, O. (2004) Inverse correlation between jasmonic acid and salicylic acid during early wound response in rice. Biochemical and Biophysical Research Communications 318, 734738.CrossRefGoogle ScholarPubMed
Lee, M.W., Qi, M. & Yang, Y. (2001) A novel jasmonic acid-inducible rice myb gene associates with fungal infection and host cell death. Molecular Plant-Microbe Interactions 14, 527535.CrossRefGoogle ScholarPubMed
Li-Yue, R., Hu-Qi, Y., Zheng-Yu, Hu-Xi B., Zhang-Xiao, J. & Li-Ben, J. (2005) Field evaluation of the resistance of transgenic rice expressing CpTI or CpTI+Bt to lepidopterous pests. Journal of Fujian Agriculture and Forestry University, Natural Science Edition 34, 181184.Google Scholar
Lou, Y., Cheng, J., Ping, X., Tang, F., Ru, S. & Du, M. (2002) Mechanisms on host discrimination between two hosts Nilaparvata lugens and Sogatella furcifera by the egg parasitoid Anagrus nilaparvatae. Acta Entomologica Sinica 45, 770776.Google Scholar
Lou, Y., Du, M., Turlings, T.C.J., Cheng, J. & Shan, W. (2005) Exogenous application of jasmonic acid induces volatile emissions in rice and enhances parasitism of Nilaparvata lugens eggs by the parasitoid Anagrus nilaparvatae. Journal of Chemical Ecology 31, 19852002.CrossRefGoogle ScholarPubMed
Malamy, J., Carr, J.P., Klesig, D.F. & Raskin, I. (1990) Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250, 10021004.CrossRefGoogle ScholarPubMed
Matsumura, M. & Suzuki, Y. (2003) Direct and feeding-induced interactions between two rice planthoppers, Sogatella furcifera and Nilaparvata lugens: effects on dispersal capability and performance. Ecological Entomology 28, 174182.CrossRefGoogle Scholar
Matteson, P.C. (2000) Insect pest management in tropical Asian irrigated rice. Annual Review of Entomology 45, 549574.CrossRefGoogle ScholarPubMed
Mei, C., Qi, M., Sheng, G. & Yang, Y. (2006) Inducible overexpression of a rice allene oxide synthase gene increases the endogenous jasmonic acid level, PR gene expression and host resistance to fungal infection. Molecular Plant–Microbe Interactions 19, 11271137.CrossRefGoogle ScholarPubMed
Métraux, J.P., Signer, H., Ryals, J., Ward, E., Wyss-Benz, M., Gaudin, J., Raschdorf, K., Schmid, E., Blum, W. & Inverardi, B. (1990) Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250, 10041006.CrossRefGoogle ScholarPubMed
Miyashita, T. (1985) Estimation on the economic injury level in the rice leafroller Cnaphalocrocis medinalis Guenée (Lepidoptera: Pyralidae). I. Relation between yield loss and injury of rice leaves at heading or in the grain filling period. Japanese Journal of Applied Entomology and Zoology 29, 7376.CrossRefGoogle Scholar
Munusamy, M., Selvaraj, P., Murugaiyan, S., Sundaram, S., Chung, H.Y., Yang, J.C., Subbiah, S. & Sa, T.M. (2004) Growth promotion and induction of systemic resistance in rice cultivar Co-47 (Oryza sativa L.) by Methylobacterium spp. Botanical Bulletin of Academia Sinica 45, 315324.Google Scholar
Nagadhara, D., Ramesh, S., Pasalu, I.C., Kondala Rao, Y., Sarma, N.P., Reddy, V.D. & Rao, K.V. (2004) Transgenic rice plants expressing the snowdrop lectin gene (gna) exhibit high-level resistance to the whitebacked planthopper (Sogatella furcifera). Theoretical and Applied Genetics 109, 13991405.CrossRefGoogle Scholar
Rath, L.K. & Misra, D.S. (1998) Induced resistance in rice through certain micronutrient fertilizer application to whitebacked planthopper, Sogatella furcifera (Horvath). Journal of Insect Science 11, 2629.Google Scholar
Ray, J. (1901) Les maladies cryptogamiques des vegetaux. Revue Generale de Botanique 13, 145151.Google Scholar
Repellin, A., Baga, M., Jauhar, P.P., & Chibbar, R.N. (2001) Genetic enrichment of cereal crops via alien gene transfer: new challenges. Plant Cell, Tissue and Organ Culture 64, 159183.CrossRefGoogle Scholar
Ross, A.F. (1961) Systemic acquired resistance induced by localized virus infections in plants. Virology 14, 340358.CrossRefGoogle ScholarPubMed
Sardesai, N., Rajyashri, K.R., Behura, S.K., Nair, S. & Mohan, M. (2001) Genetic, physiological and molecular interactions of rice and its major dipteran pest, gall midge. Plant Cell, Tissue and Organ Culture 64, 115131.CrossRefGoogle Scholar
Satoh, M., Nakajima, T. & Kanno, H. (2005) Induced resistance to rice blast disease in rice plants infested with the white-backed planthopper, Sogatella furcifera, in a paddy field. Japanese Journal of Applied Entomology and Zoology 49, 105111.CrossRefGoogle Scholar
Schuler, G., Gorls, H. & Boland, W. (2001) 6-substituted indanoyl isoleucine conjugates mimic the biological activity of coronatine. European Journal of Organic Chemistry 2001, 16631668.3.0.CO;2-I>CrossRefGoogle Scholar
Schweizer, P., Buchala, A. & Metraux, J.P. (1997) Gene-expression patterns and levels of jasmonic acid in rice treated with the resistance inducer 2,6–dichloroisonicotinic acid. Plant Physiology 115, 6170.CrossRefGoogle Scholar
Schweizer, P., Buchala, A., Budler, R. & Metraux, J.P. (1998) Induced systemic resistance in wounded rice plants. Plant Journal 14, 475481.CrossRefGoogle Scholar
Schweizer, P., Schlagenhauf, E., Schaffrath, U. & Dudler, R. (1999) Different patterns of host genes are induced in rice by Pseudomonas syringae, a biological inducer of resistance, and the chemical inducer benzothiadiazole (BTH). European Journal of Plant Pathology 105, 659665.CrossRefGoogle Scholar
Seino, Y., Suzuki, Y. & Sogawa, K. (1996) An ovicidal substance produced by rice plants in response to oviposition by the whitebacked planthopper, Sogatella furcifera (Horvath) (Homoptera: Delphacidae). Applied Entomology and Zoology 31, 467473.CrossRefGoogle Scholar
Shepard, B.M., Barrion, A.T. & Litsinger, J.A. (1995) Rice-feeding insects of tropical Asia. Manila, Philippines, International Rice Research Institute.Google Scholar
Silverman, P., Seskar, M., Kanter, D., Schweizer, P., Metraux, J.P. & Raskin, I. (1995) Salicylic acid in rice. Biosynthesis, conjugation, and possible role. Plant Physiology 108, 633639.CrossRefGoogle ScholarPubMed
Sinha, A.K. & Hait, G.N. (1982) Host sensitization as a factor in induction of resistance in rice against Drechslera by seed treatment with phytoalexin inducers. Transactions of the British Mycological Society 79, 213219.CrossRefGoogle Scholar
Stout, M.J., Thaler, J.S. & Thomma, B.P.H.J. (2006) Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods. Annual Review of Entomology 51, 663689.CrossRefGoogle ScholarPubMed
Suzuki, Y., Sogawa, K. & Seino, Y. (1996) Ovicidal reaction of rice plants against the whitebacked planthopper, Sogatella furcifera Horvath (Homoptera: Delphacidae). Applied Entomology and Zoology 32, 530532.Google Scholar
Thaler, J.S. & Bostock, R.M. (2004) Interactions between abscisic-acid mediated responses and plant resistance to pathogens and insects. Ecology 85, 4858.CrossRefGoogle Scholar
Walling, L.L. (2000) The myriad plant responses to herbivores. Journal of Plant Growth Regulation 19, 195216.CrossRefGoogle ScholarPubMed
Wang, X., Ren, X., Zhu, L. & He, G. (2004) OsBi1, a rice gene, encodes a novel protein with a CBS-like domain and its expression is induced in responses to herbivore feeding. Plant Science 166, 15811588.CrossRefGoogle Scholar
Wang, X.L., He, R.F. & He, G.C. (2005) Construction of suppression subtractive hybridization libraries and identification of brown planthopper-induced genes. Journal of Plant Physiology 162, 12541262.CrossRefGoogle ScholarPubMed
Way, M.J. & Heong, K.L. (1994) The role of biodiversity in the dynamics and management of insect pests of tropical irrigated rice – a review. Bulletin of Entomological Research 84, 567587.CrossRefGoogle Scholar
Wu, J., Xu, J., Yuan, S., Liu, J., Jiang, Y. & Xu, J. (2001) Pesticide-induced susceptibility of rice to brown planthopper Nilaparvata lugens. Entomologia Experimentalis et Applicata 100, 119126.CrossRefGoogle Scholar
Wu, J., Hui-Min, H., Yang, G., Liu, J., Liu, G. & Wilkins, R.M. (2004) Effective duration of pesticide-induced susceptibility of rice to brown planthopper (Nilaparvata lugens Stål, Homoptera: Delphacidae), and physiological and biochemical changes in rice plants following pesticide application. International Journal of Pest Management 50, 5562.CrossRefGoogle Scholar
Xu, T., Zhou, Q., Xia, Q., Zhang, W.Q. & Gu, D.X. (2002) Effects of herbivore-induced rice volatiles on the host selection behavior of brown planthopper, Nilaparvata lugens. Chinese Science Bulletin 47, 13551360.CrossRefGoogle Scholar
Xu, T., Zhou, Q., Chen, W., Zhang, G., He, G., Gu, D. & Zhang, W. (2003) Involvement of jasmonate-signaling pathway in the herbivore-induced rice plant defense. Chinese Science Bulletin 48, 19821987.CrossRefGoogle Scholar
Yadava, C.P., Santaram, G., Israel, P. & Kalode, M.B. (1972) Life history of rice leaf-roller, Cnaphalocrocis medinalis Guenee (Lepidoptera: Pyralidae) and its rection to some rice varieties and grasses. Indian Journal of Agricultural Science 42, 520523.Google Scholar
Yamasaki, M., Yoshimura, A. & Yasui, H. (2000) Mapping of quantitative trait loci of ovicidal response to brown planthopper (Nilaparvata lugens Stål) in rice (Oryza sativa L.) Breeding Science 50, 291296.CrossRefGoogle Scholar
Yamasaki, M., Yoshimura, A. & Yasui, H. (2003) Genetic basis of ovicidal response to whitebacked planthopper (Sogatella furcifera Horvath) in rice (Oryza sativa L.) Molecular Breeding 12, 133143.CrossRefGoogle Scholar
Yang, Y.N., Qi, M. & Mei, C.S. (2004) Endogenous salicylic acid protects rice plants from oxidative damage caused by aging as well as biotic and abiotic stress. Plant Journal 40, 909919.CrossRefGoogle ScholarPubMed
Yuan, H.Y., Chen, X.P., Zhu, L. & He, G.C. (2004) Isolation and characterization of a novel rice gene encoding a putative insect-inducible protein homologous to wheat Wir1. Journal of Plant Physiology 161, 7985.CrossRefGoogle Scholar
Zhang, F., Zhu, L. & He, G. (2004) Differential gene expression in response to brown planthopper feeding in rice. Journal of Plant Physiology 161, 5362.CrossRefGoogle ScholarPubMed
Zhou, Q., Xu, T., Zhang, G.R., Gu, D.X. & Zhang, W.Q. (2003) Repellent effects of herbivore-induced rice volatiles on the brown planthopper, Nilaparvata lugens Stål. Acta Emotomologica Sinica 46, 739744.Google Scholar