Abstract
Amaranthus hypochondriacus is a C4 pseudocereal crop capable of producing reasonable grain yields in adverse environmental conditions that limit cereal performance. It accumulates trypsin inhibitors and α-amylase inhibitors in seeds and leaves that are considered to act as insect feeding deterrents. Foliar trypsin and α-amylase inhibitors also accumulate by treatment with exogenous jasmonic acid (JA) in controlled laboratory conditions. Three field experiments were performed in successive years to test if two nonphytotoxic dosages of JA were capable of inducing inhibitor activity in A. hypochondriacus in agronomical settings, and if this induced response reduced insect herbivory and insect abundance in foliage and seed heads. The performance of JA-treated plants was compared to insecticide-treated plants and untreated controls. The effect of exogenous JA on the foliar levels of six additional putatively defence proteins was also evaluated. Possible adverse effects of JA induction on productivity were evaluated by measuring grain yield, seed protein content, and germination efficiency. The results present a complex pattern and were not consistent from year to year. To some extent, the yearly variability observed could have been consequence of growth under drought versus nondrought conditions. In a drought year, JA-treated plants had lower levels of insect herbivory-derived damage in apical leaves and panicle than control plants, whereas in nondrought years, there was an inconsistent effect on aphids, with no effect on lepidopteran larvae. JA treatments reduced the size of the insect community in seed heads. The effect varied with year. Exogenous JA did not adversely affect productivity, and in the absence of drought stress, the higher dosage enhanced grain yield. Induction of defensive proteins by JA, although sporadic, was more effective in nondrought conditions. The patterns of foliar protein accumulation observed suggest that they may be part of a constitutive, rather than inducible, chemical defense mechanism that is developmentally regulated and critically dependent on the environment. The results emphasize the difficulties that are often encountered when evaluating the performance of chemical elicitors of induced resistance in field settings.
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REFRENCES
Agrawal, A. 2000. Overcompensation of plants in response to herbivory and the by-product benefits of mutualism. Trends Plant Sci. 5:309–313.
Alarcon, J. J. and Malone, M. 1995. The influence of plant age on wound induction of proteinase inhibitors in tomato. Physiol. Plant 95:423–427.
AOAC 2000. Official Methods of Analysis. Association of Official Analytical Chemists, 17th edn. Washington, DC.
Appel, W. 1974. Amino acid arylamidases (“Leucine-nitroanilidase”). Determination with l-Leucine-p-nitroanilide as substrate, pp. 958–963, in H. U. Bergmeyer (ed.). Methods of Enzymatic Analysis, 2nd English edn., Vol. 2. Verlag Chemie International, Florida.
Aragón-García, A. and López-Olguín, J. F. 2001. Descripción y Control de las Plagas de Amaranto. Benemérita Universidad Autónoma de Puebla, México, pp. 1–30.
Baldwin, I. T., 1999. The jasmonate cascade and the complexity of induced defence against herbivore attack, pp. 155–186, in M. Wink (ed.). Functions of Plant Secondary Metabolites and Their Exploitation in Biotechnology. Annual Plant Reviews, Vol. 3. Sheffield Academic Press, England.
Becker, R., Wheeler, E. L., Lorenz, K., Stafford, A. E., Rosjean, O. K., Betschart, A. A., and Saunders, R. M. 1981. A compositional study of amaranth grain. J. Food Sci. 46:1175–1180.
Bewley, J. D. 1997. Seed germination and dormancy. Plant Cell 9:1055–1066.
Bird, R. and Hopkins, R. H. 1954. The action of some α-amylases on amylose. Biochem. J. 56:86–96.
Blechert, S., Brodshelm, W., Hölder, S., Kammerer, L., Kutchan, T. M., Mueller, M. J., Xia, Z.-Q., and Zenk, M. H. 1995. The octadecanoid pathway: Signal molecules for the regulation of secondary pathways. Proc. Natl. Acad. Sci. U.S.A. 92:4099–4105.
Bradford, M. 1976. A rapid and sensitive method for the determination of microgram quantities of protein utilizing the principle of protein dye-binding. Anal. Biochem. 72:248–254.
Chagolla-López, A., Blanco-Labra, A., Patthy, A., Sánchez, R., and Pongor, S. 1994. A novel α-amylase inhibitor from amaranth (Amaranthus hypochondriacus) seeds. J. Biol. Chem. 269:23675–23680.
Cipollini, D. F., Jr. 1997. Wind-induced mechanical stimulation increases pest resistance in common bean. Oecologia 111:84–90.
Cipollini, D. F., Jr. and Redman, A. M. 1999. Age-dependent effects of jasmonic acid treatment and wind exposure on foliar oxidase activity and insect resistance in tomato. J. Chem. Ecol. 25:271–281.
Corcuera, L. J. 1993. Biochemical basis for the resistance of barley to aphids. Phytochemistry 33:741–747.
Cordero, M. J., Raventós, D., and San Segundo, B. 1994. Differential expression and induction of chitinases and β-glucanases in response to fungal infection during germination of maize seeds. Mol. Plant-Microbe Interact. 7:23–31.
Dean, S. 1986. High-tech crop breeding may ease world hunger. Agric. Inf. Dev. Bull. U.N. 8:19.
Dombrowski, J. E. 2003. Salt stress activation of wound-related genes in tomato plants. Plant Physiol. 132:2098–2107.
Downton, W. J. S. 1973. Amaranthus edulis: A high lysine grain amaranth. World Crops 25:20.
English-Loeb, G., Stout, M. J., and Duffey, S. S. 1997. Drought stress in tomatoes: Changes in plant chemistry and potential non-linear consequences for insect herbivores. Oikos 79:456–468.
Erlanger, B., Kokowsky, N., and Cohen, W. 1961. The preparation and properties of two new chromogenic substrates of trypsin. Arch. Biochem. Biophys. 95:271–278.
Espitia-Rangel, E. 1990. Situación actual y problemática del cultivo de amaranto en México, pp. 101–109, in A. Trinidad-Santos, F. Gómez-Lorence, and G. Suárez-Ramos (eds.). El Amaranto Amaranthus spp. Su Cultivo y Aprovechamiento. Colegio de Postgraduados, Chapingo, México.
Farmer, E. E., Johnson, R. R., and Ryan, C. A. 1992. Regulation of expression of proteinase inhibitor genes by methyl jasmonate and jasmonic acid. Plant Physiol. 98:995–1002.
Felton, G. W., Summers, C. B., and Mueller, A. J. 1994. Oxidative responses in soybean foliage to herbivory by bean leaf beetle and three-cornered alfalfa hopper. J. Chem. Ecol. 20:639–650.
Flint, H. M., Wilson, F. D., Hendrix, D., Leggett, J., Naranjo, S., Henneberry, T. J., and Radin, J. W. 1994. The effect of plant water stress on beneficial and pest insects including the pink bollworm and the sweetpotato whitefly in two short season cultivars of cotton. Southwestern Entomol. 19:11–22.
Gatehouse, J. A. 2002. Plant resistance toward insect herbivores: A dynamic interaction. New Phytol. 156:145–169.
Gervaix, A., Kessels, G., Suter, S., Lew, P., and Verhoeven, A. 1991. The chymotrypsin inhibitor carbobenzyloxy-leucine-tyrosine-chloromethylketone interferes with the neutrophyl respirator burst mediated by a signaling pathway independent of PtdIns P2 breakdown and cytosolic free calcium. J. Immunol. 47:1912–1919.
Gross, K. C. 1982. A rapid and sensitive spectrophotometric method for assaying polygalacturonase using 2-cyanoacetamide. Horticult. Sci. 17:933–934.
Holdsworth, M., Kurup, S., and McKibbin, R. 1999. Molecular and genetic mechanisms regulating the transition from embryo development to germination. Trends Plant Sci. 4:275–280.
Karban, R. 1999. Future use of plant signals in agricultural and industrial crops, pp. 223-238, in Insect-Plant Interactions and Induced Plant Defence (Novartis Foundation Symposium 223). Wiley, Chichester.
Kauffman, C. S. and Weber, L. E. 1990. Grain amaranth, pp. 127–139, in J. Janick and J. E. Simon (eds.). Advances in New Crops. Proceedings of the First National Symposium on New Crops, Research Development, Economics. Timber Press, Portland, OR.
Lam, J.-M., Pwee, K.-H., Sun, W. Q., Chua, Y.-L., and Wang, X.-J. 1999. Enzyme-stabilizing activity of seed trypsin inhibitors during desiccation. Plant Sci. 142:209–218.
Lehman, J., Atzorn, R., Brückner, C., Reinbothe, S., Leopold, J., Wasternack, C., and Parthier, B. 1995. Accumulation of jasmonate, abscisic acid, specific transcripts and proteins in osmotically stressed barley leaf segments. Planta 197:156–162.
Lopez, F., Vansuyt, G., Derancourt, J., Fourcroy, P., and Casse-Delbart, F. 1994. Identification by 2D-PAGE analysis of salt-stress induced proteins in radish (Raphanus sativus). Cell Mol. Biol. 40:85–90.
Lyon, G. D. and Newton, A. C. 1999. Implementation of elicitor mediated resistance in agriculture, pp. 299–318, in A. A. Agrawal, S. Tuzun, and E. Bent (eds.). Induced Plant Defenses Against Pathogens and Herbivores: Biochemistry, Ecology and Agriculture. The American Phytopathological Society, St. Paul, MN.
Maldonado, U. and Estrada, A. 1986. Amaranth genetic variation and utilization in Mexico, pp. 120–124, in Proceedings of the Third Amaranth Conference. Grain Amaranth: Expanding Consumption Through Improved Cropping, Marketing and Crop Development. Rodale Press Inc., Emmaus, PA.
Memelink, J., Verpoorte, R., and Kijne, J. W. 2001. ORCAnization of jasmonate-responsive gene expression in alkaloid metabolism. Trends Plant Sci. 6:212–219.
Nagamatsu-López, Y. 2004. Efecto de la luz sobre la acumulación de inhibidores de proteasas en Amaranthus hypochondriacus. MSc dissertation. Cinvestav I.P.N. at Irapuato, México. Biologia Plantorium 47:633–634.
Omer, A. D., Thaler, J., Granett, J., and Karban, R. 2000. Jasmonic acid induced resistance in grapevines to a root and leaf feeder. J. Econ. Entomol. 93:840–845.
Orozco-Cardenas, M., McGurl, B., and Ryan, C. A. 1993. Expression of an antisense prosystemin gene in tomato reduces resistance toward Manduca sexta larvae. Proc. Natl. Acad. Sci. U.S.A. 90:8273–8276.
Rawate, P. D., 1983. Amaranth (pigweed): A crop to help solve the world protein shortage, pp. 287–298, in A. W. Lockeretz (ed.). Environmentally Sound Agriculture: Selected Papers from the Fourth International Conference of the International Federation of Organic Agriculture Movements, Praeger, New York.
Reinbothe, S., Mollenhauer, B., and Reinbothe, C. 1994. JIPs and RIPs: The regulation of plant gene expression by jasmonates in response to environmental cues and pathogens. Plant Cell 6:1197–1209.
Reviron, M.-P., Vartanian, N., Sallantin, M., HHuet, J.-C., Pernollet, J.-C., and De Vienne, D. 1992. Characterization of a novel protein induced by progressive or rapid drought and salinity in Brassica napus leaves. Plant Physiol. 100:1486–1493.
Salas-Araiza, M. D. 1999. Insectos asociados con el Amaranthus spp. (Amaranthaceae) en Irapuato, Gto., México, pp. 471–477, in Memorias del XXXIV Congreso Nacional de Entomología. Sociedad Mexicana de Entomología A.C. Aguascalientes, Mexico.
Sánchez-Hernández, C. 2001. Caracterización de la actividad inhibitoria contra α-amilasa presente en amaranto y su inducción por distintos evocadores relacionados con defensa, daño mecánico y herbivoría. MSc dissertation. Cinvestav I.P.N. at Irapuato, México.
Sandoval-Cardoso, M. L. 1991. Purificación y caracterización de enzimas larvales de 4 insectos que atacan maíz durante el almacenamiento. BSc dissertation. Universidad de Guanajuato, Mexico.
Segura-Nieto, M., Vázquez-Sánchez, N., Rubio-Velázquez, H., Olguín-Martínez, L., Rodríguez-Nester, C., and Herrera-Estrella, L. 1992. Characterization of amaranth (Amaranthus hypochondriacus L.) seed proteins. J. Agric. Food Chem. 40:1553–1558.
Sokal, R. R. and Rohlf, F. J. 1969. BIOMETRY: The Principles and Practice of Statistics in Biological Research. W. H. Freeman, San Francisco, CA.
Staswick, P. E. and Lehman, C. C. 1999. Jasmonic acid-signaled responses in plants, pp. 117–136, in A. A. Agrawal, S. Tuzun, and E. Bent (eds.). Induced Plant Defenses Against Pathogens and Herbivores: Biochemistry, Ecology and Agriculture. The American Phytopathological Society, St. Paul, MN.
Stout, M. J., Workman, J., and Duffey, S. S. 1994. Differential induction of tomato foliar proteins by arthropod herbivores. J. Chem. Ecol. 20:2575–2594.
Teutonico, R. A. and Knorr, D. 1985. Amaranth: Composition, properties and applications of a rediscovered food crop. Food Technol. 39:49–61.
Thaler, J. S. 1999a. Induced resistance in agricultural crops: Effects of jasmonic acid on herbivory and yield in tomato plants. Environ. Entomol. 28:30–37.
Thaler, J. S. 1999b. Jasmonic acid mediated interactions between plants, herbivores, parasitoids, and pathogens: A review of field experiments in tomato, pp. 319–334, in A. A.Agrawal, eds.Tuzun, and E.Bent (eds.). Induced Plant Defenses Against Pathogens and Herbivores: Biochemistry, Ecology and Agriculture. The American Phytopathological Society, St. Paul, MN.
Thaler, J. S. 1999c. Jasmonate-inducible plant defences cause increased parasitism of herbivores. Nature 399:686–688.
Thaler, J. S., Stout, M. J., Karban, R., and Duffey, S. S. 1996. Exogenous jasmonates simulate insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and field. J. Chem. Ecol. 22:1767–1781.
Thaler, J. S., Stout, M. J., Karban, R., and Duffey, S. S. 2001. Jasmonate-mediated induced plant resistance affects a community of herbivores. Ecol. Entomol. 26:312–324.
ValdésRodríguez, S., Segura-Nieto, M., Chagolla-Lopez, A., Verver, Y. Vargas-Cortina, A., Martínez-Gallardo, N., and Blanco-Labra, A. 1993. Purification, characterization, and complete amino acid sequence of a trypsin inhibitor from amaranth (Amaranthus hypochondriacus) seeds. Plant Physiol. 103:1407–1412.
van Dam, N. M., Horn, M., Mareš, M., and Baldwin, I. T. 2001. Ontogeny constrains systemic protease inhibitor response in Nicotiana attenuata. J. Chem. Ecol. 27:547–568.
Vera, P., Hernández Yago, J., and Conejero, V. 1988. Immunocytochemical localization of the major “pathogenesis-related” (PR) protein of tomato plants. Plant Sci. 55:223–230.
Villagómez-Castro, J. C., Calvo-Mendez, C., and López-Romero, E. 1992. Chitinase activity in encysting Entamoeba invadens and its inhibition by allosamidin. Mol. Biochem. Parasitol. 52:55–62.
Welham, T., O'Neill, M., Johnson, S., Wang, T. L., and Domoney, C. 1998. Expression patterns of genes encoding seed trypsin inhibitors in Pisum sativum. Plant Sci. 131:13–24.
Wittstock, U. and Gershenzon, J. 2002. Constitutive plant toxins and their role in defense against herbivores and pathogens. Curr. Opin. Plant Biol. 5:300–307.
Wolson, J. L. and Murdock, L. L. 1990. Growth of Manduca sexta on wounded tomato: Role of induced proteinase inhibitors. Entomol. Exp. Appl. 54:257–264.
Xu, Y., Chang, P.-F. L., Liu, D., Narasimhan, M. L., Raghothama, K. G., Hasegawa, P. M., and Bressan, R. A. 1994. Plant defense genes are synergistically induced by ethylene and methyl jasmonate. Plant Cell 6:1077–1085.
Xu, D., Duan, X., Wang, B., Hong, B., Ho, D. T., and Wu, R. 1996. Expression of a late embryogenesis abundant protein gene, HVA1 from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol. 110:249–257.
Zheng, Y. and Wozniak, C. A. 1997. Adaptation of a β-1,3-glucanase assay to microplate format. BioTechniques 22:922–926.
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Délano-Frier, J.P., Martínez-Gallardo, N.A., Martínez-de La Vega, O. et al. The Effect of Exogenous Jasmonic Acid on Induced Resistance and Productivity in Amaranth (Amaranthus hypochondriacus) Is Influenced by Environmental Conditions. J Chem Ecol 30, 1001–1034 (2004). https://doi.org/10.1023/B:JOEC.0000028464.36353.bb
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DOI: https://doi.org/10.1023/B:JOEC.0000028464.36353.bb