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Enzyme Induction as a Possible Mechanism for Latex-Mediated Insect Resistance in Romaine Lettuce

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Abstract

Plant latex is a known storehouse of various secondary metabolites with demonstrated negative impact on insect fitness. A romaine lettuce cultivar, “Valmaine”, possesses a high level of latex-mediated resistance against the banded cucumber beetle, Diabrotica balteata LeConte (Coleoptera: Chrysomelidae), compared to a closely related cultivar “Tall Guzmaine”. Latex from damaged Valmaine plants was much more deterrent to adult D. balteata feeding than latex from undamaged plants when applied to the surface of artificial diet under choice conditions; no such difference was found in choice tests with latex from damaged and undamaged Tall Guzmaine plants. The intensities of whiteness and browning were significantly higher in Valmaine latex than in Tall Guzmaine latex. The activities of three enzymes (phenylalanine ammonia lyase, polyphenol oxidase, and peroxidase) significantly increased over time in latex from damaged Valmaine plants (i.e., 1, 3, and 6 days after feeding initiation), but they remained the same in Tall Guzmaine latex. The constitutive levels of phenylalanine ammonia lyase and polyphenol oxidase also were significantly higher in Valmaine latex than in Tall Guzmaine latex. These studies suggest that Valmaine latex chemistry may change after plant damage due to increased activity of inducible enzymes and that inducible resistance appears to act synergistically with constitutive resistance against D. balteata.

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References

  • Archer, B. L., Audley, B. G., McSweeney, G. P., and Hong, T. C. 1969. Studies on composition of latex serum and ‘bottom fraction’ particles. J. Rubber Res. Inst. Malaysia 21:560–569.

    CAS  Google Scholar 

  • Azarkana, M., Wintjens, R., Looze, Y., and Baeyens-Volant, D. 2004. Detection of three wound-induced proteins in papaya latex. Phytochemistry 65:525–534.

    Article  CAS  Google Scholar 

  • Bennett, M. H., Gallagher, M., Bestwich, C., Rossiter, J., and Mansfield, J. 1994. The phytoalexin response of lettuce to challenge by Botrytis cinerea, Bremia lactucae and Pseudomonas syringae pv. phaseolicola. Physiol. Mol. Plant Pathol. 44:321–333.

    Article  CAS  Google Scholar 

  • Campos-Vargas, R., and Saltveit, M. E. 2002. Involvement of putative chemical wound signals in the induction of phenolic metabolism in wounded lettuce. Physiol. Plant. 114:73–84.

    Article  PubMed  CAS  Google Scholar 

  • Chaman, M. E., Corcuera, L. J., Zuniga, G. E., Cardemil, L., and Argandona, V. H. 2001. Induction of soluble and cell wall peroxidases by aphid infestation in barley. J. Agric. Food Sci. 49:2249–2253.

    Article  CAS  Google Scholar 

  • Chaman, M. E., Copaja, S. V., and Argandon, V. H. 2003. Relationships between salicylic acid content, phenylalanine ammonia-lyase (PAL) activity, and resistance of barley to aphid infestation. J. Agric. Food Sci. 51:2227–2231.

    Article  CAS  Google Scholar 

  • Cole, R. A. 1984. Phenolic acids associated with the resistance of lettuce cultivars to the lettuce root aphid. Ann. Appl. Biol. 105:129–145.

    Article  CAS  Google Scholar 

  • Constabel, C. P., and Ryan, C. A. 1998. A survey of wound and methyl jasmonate-induced leaf polyphenol oxidase in crop plants. Phytochemistry 47:507–511.

    Article  CAS  Google Scholar 

  • Dixon, R. A., and Paiva, N. L. 1995. Stress induced phenylpropanoid metabolism. Plant Cell 7:1085–1097.

    Article  PubMed  CAS  Google Scholar 

  • Dowd, P. F. 1994. Enhanced maize (Zea mays L.) pericarp browning: associations with insect resistance and involvement of oxidizing enzymes. J. Chem. Ecol. 20:2777–2803.

    Article  CAS  Google Scholar 

  • Dowd, P. F., and Norton, R. A. 1995. Browning-associated mechanisms of resistance to insects in corn callus tissue. J. Chem. Ecol. 21:583–600.

    Article  CAS  Google Scholar 

  • Duffey, S. S., and Felton, G. W. 1991. Enzymatic antinutritive defenses of the tomato plant against insects, pp. 167–197, in P. A. Hedin (ed.). Naturally Occurring Pest BioregulatorsACS, Washington, DC.

    Google Scholar 

  • Duffey, S. S., and Stout, M. J. 1996. Antinutritive and toxic components of plant defense against insects. Arch. Insect Biochem. Physiol. 32:3–37.

    Article  CAS  Google Scholar 

  • Dupont, M. S., Mondin, Z., Williamson, G., and Price, K. R. 2000. Effect of variety, processing and storage on the flavonoid glycoside content and composition of lettuce and endive. J. Agric. Food Chem. 48:3957–3964.

    Article  PubMed  CAS  Google Scholar 

  • El Moussaoui, A., Nijs, M., Paul, C., Wintjens, R., Vincentelli, J., Azarkan, M., and Looze, Y. 2001. Revisiting the enzymes stored in the laticifers of Carica papaya in the context of their possible participation in the plant defense mechanism. Cell Mol. Life Sci. 58:556–570.

    Article  PubMed  CAS  Google Scholar 

  • Esau, K. 1965. Plant Anatomy. Wiley, Hoboken, New Jersey.

    Google Scholar 

  • Evans, F. J., and Schmidt, R. J. 1976. Two new toxins from the latex of Euphorbia poissonii. Phytochemistry 15:333–335.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Fox, M. G., and French, J. C. 1988. Systematic occurrence of sterols in latex of Araceae: subfamily Colocasioideae. Am. J. Bot. 75:132–137.

    Article  CAS  Google Scholar 

  • Freitas, C. D. T., Oliveira, J. S., Miranda, M. R. A., Macedo, N. M. R., Sales, M. P., Villas-Boas, L. A., and Viana, R. M. 2007. Enzymatic activities and protein profile of latex from Calotropis procera. Plant Physiol. Biochem. 45:781–789.

    Article  PubMed  CAS  Google Scholar 

  • Gregory, P. and Tingey, W. M. 1981. Chemical mechanisms of potato resistance to the leafhopper. Breeding for resistance to insects and mites, pp. 95–99, in Proceedings of 2nd Eucarpia/IOBC Meeting of the Working Group Breeding for Resistance to Insects and Mites. Canterbury, UK.

  • Groeneveld, H. W. 1976. Some morphological and chemical characteristics of the purified terpenoid particles of the latex of Hoya australis R.B. ex Traill. Acta Bot. Neer. 25:1–13.

    CAS  Google Scholar 

  • Guzman, V. L. 1986. Short Guzmaine, Tall Guzmaine and Florigade, three cos lettuce cultivars resistant to lettuce mosaic virus. Agricultural Experiment Station Circular S-326. IFAS University of Florida, FL, USA.

    Google Scholar 

  • Hahlbrock, K., and Scheel, D. 1989. Physiology and molecular biology of phenylpropanoid metabolism. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40:347–369.

    Article  CAS  Google Scholar 

  • Hedin, P. A., Jenkins, J. N., Collum, D. H., White, W. H., Parrott, W. L., M, and Gown, M. W. 1983. Cyanidin-3-glucoside, a newly recognized basis for resistance in cotton to the tobacco budworm Heliothis virescens (Fab.) (Lepidoptera: Noctuidae). Experientia 39:799–801.

    Article  CAS  Google Scholar 

  • Huang, J., Nuessly, G. S., McAuslane, H. J., and Slansky, F. 2002. Resistance to adult banded cucumber beetle, Diabrotica balteata (Coleoptera: Chrysomelidae), in romaine lettuce. J. Econ. Entomol. 95:849–855.

    PubMed  Google Scholar 

  • Huang, J., McAuslane, H. J., and Nuessly, G. S. 2003. Resistance in lettuce to Diabrotica balteata (Coleoptera: Chrysomelidae): the roles of latex and inducible defense. Environ. Entomol. 32:9–16.

    Google Scholar 

  • Inoue, M., Sezaki, S., Sorin, T., and Sugiura, T. 1985. Change of phenylalanine ammonia-lyase activity in strawberry leaves infested with the two-spotted spider mite, Tetranychus urticae KOCH (Acarina: Tetranychidae). Appl. Entomol. Zool. 20:348–349.

    CAS  Google Scholar 

  • Ke, D., and Saltveit, M. E. 1986. Effects of calcium and auxin on russet spotting and phenylalanine ammonia-lyase activity in iceberg lettuce. HortScience 21:1169–1171.

    CAS  Google Scholar 

  • Kim, J. H., and Mullin, C. A. 2003. Antifeedant effects of proteinase inhibitors on feeding behaviors of adult western corn rootworm (Diabrotica virgifera virgifera). J. Chem. Ecol. 29:795–810.

    Article  PubMed  CAS  Google Scholar 

  • Konno, K., Hirayama, C., Nakamura, M., Tateishi, K., Tamura, Y., Hattori, M., and Kohno, K. 2004. Papain protects papaya trees from herbivorous insects: role of cysteine proteases in latex. Plant J. 37:370–378.

    Article  PubMed  CAS  Google Scholar 

  • Konno, K., Ono, H., Nakamura, M., Tateishi, K., Hirayama, C., Tamura, Y., Hattori, M., Koyama, A., and Kohno, K. 2006. Mulberry latex rich in antidiabetic sugar-mimic alkaloids forces dieting on caterpillars. Proc. Nat. Acad. Sci. U.S.A. 103:1337–1341.

    Article  CAS  Google Scholar 

  • Kush, A., Goyvarets, E., Chye, M. L., and Chua, N. H. 1990. Laticifer-specific gene expression in Hevea brasiliensis (Rubber tree). Proc. Nat. Acad. Sci. U.S.A. 87:1787–1790.

    Article  CAS  Google Scholar 

  • Loaiza-Velarde, J. G., Tomás-Barberán, F. A., and Saltveit, M. E. 1997. Effect of intensity and duration of heat-shock treatments on wound-induced phenolic metabolism in iceberg lettuce. J. Am. Soc. Hort. Sci. 122:873–877.

    CAS  Google Scholar 

  • Lohman, M. H., and Hartel, R. W. 1994. Effect of milk fat fractions on fat bloom in dark chocolate. J. Am. Oil Chem. Soc. 71:267–275.

    Article  CAS  Google Scholar 

  • Malcolm, S. B., and Zalucki, M. P. 1996. Milkweed latex and cardenolide induction may resolve the lethal plant defence paradox. Entomol. Exp. Appl. 80:193–196.

    Article  CAS  Google Scholar 

  • Maskan, M. 2001. Kinetics of color change of kiwi fruit during hot air and microwave drying. J. Food Eng. 48:169–176.

    Article  Google Scholar 

  • Matile, P. 1976. Localizations of alkaloids and mechanism of their accumulation in vacuoles of Chelidonium majus laticifers. Nova Acta Leopold. Suppl. 7:65–73.

    Google Scholar 

  • Moss, J. R., and Otten, L. 1989. A relationship between color development and moisture content during roasting of peanut. Can. Inst. Food Sci. Tech. J. 22:34–39.

    Google Scholar 

  • Mura, A., Medda, R., Longu, S., Floris, G., Rinaldi, A. C., and Padiglia, A. 2005. A Ca2+/calmodulin-binding peroxidase from Euphorbia latex: novel aspects of calcium-hydrogen peroxide cross-talk in the regulation of plant defenses. Biochemistry 44:14120–14130.

    Article  PubMed  CAS  Google Scholar 

  • Mura, A., Pintus, F., Medda, R., Floris, G., Rinaldi, A. C., and Padiglia, A. 2007. Catalase and antiquitin from Euphorbia characias: two proteins involved in plant defense? Biochemistry 72:501–508.

    PubMed  CAS  Google Scholar 

  • Ni, X., Quisenberry, S. S., Heng-Moss, T., Markwell, J., Sarath, G., Klucas, R., and Baxendale, F. 2001. Oxidative responses of resistant and susceptible cereal leaves to symptomatic and nonsymptomatic cereal aphid (Hemiptera: Aphididae) feeding. J. Econ. Entomol. 94:743–751.

    PubMed  CAS  Google Scholar 

  • Nishio, S., Blum, M. S., and Takahashi, S. 1983. Intraplant distribution of cardenolides in Asclepias humistrata (Asclepiadaceae) with additional notes on their fates in Tetraopes melanurus (Coleoptera: Cerambycidae) and Rhyssomatus lineaticollis (Coleoptera: Curculionidae). Mem. Coll. Agric. Kyoto Univ. 122:43–52.

    CAS  Google Scholar 

  • Nuessly, G. S., and Nagata, R. T. 1994. Differential probing response of serpentine leafminer, Liriomyza trifolii (Burgess), on cos lettuce. J. Entomol. Sci. 29:330–338.

    Google Scholar 

  • Palumbo, J., Fournier, A., Ellsworth, P., Nolte, K., and Clay, P. 2006. Insect crop losses and insecticide usage for head lettuce in Arizona: 2004–2006. College of Agriculture 2006 Vegetable Report. AZ, USA: University of Arizona. http://cals.arizona.edu/pubs/crops/az1419/.

  • Peterson, G. L. 1977. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Ann. Biochem. 83:346–356.

    Article  CAS  Google Scholar 

  • Pickard, W. F. 2008. Laticifers and secretory ducts: two other tube systems in plants. New Phytol. 177:877–888.

    Article  PubMed  Google Scholar 

  • Ramos, M. V., Freitas, C. D. T., Staniscuaski, F., Macedo, L. L. P., Sales, M. P., Sousa, D. P., and Carlini, C. R. 2007. Performance of distinct crop pests reared on diets enriched with latex proteins from Calotropis procera: Role of laticifer proteins in plant defense. Plant Sci. 173:349–357.

    Article  CAS  Google Scholar 

  • Rees, S. B., and Harborne, J. B. 1985. The role of sesquiterpene lactones and phenolics in the chemical defense of the chicory plant. Phytochemistry 24:2225–2231.

    Article  CAS  Google Scholar 

  • Ribereau-Gayon, P. 1972. Plant Phenolics. Oliver and Boyd, Edinburgh, UK.

    Google Scholar 

  • Ryder, E. J. 1998. Lettuce, Endive and Chicory. CABI, Cambridge, UK.

    Google Scholar 

  • SAS Institute. 2003. Guide for Personal Computers, version 9.1.3. SAS Institute, Cary, North Carolina.

  • Sessa, R. A., Bennett, M. H., Lewis, M. J., Mansfield, J. W., and Beale, M. H. 2000. Metabolite profiling of sesquiterpene lactones from Lactuca species. J. Biol. Chem. 275:26877–26884.

    PubMed  CAS  Google Scholar 

  • Sethi, A. 2007. Biochemical Mode of Multiple Insect Resistance in Romaine Lettuce Cultivar. Ph.D. dissertation. University of Florida, Gainesville, Florida.

  • Sethi, A., McAuslane, H. J., Nagata, R. T., and Nuessly, G. S. 2006. Host plant resistance in romaine lettuce affects feeding behavior and biology of Trichoplusia ni and Spodoptera exigua (Lepidoptera: Noctuidae). J. Econ. Entomol. 99:2156–2163.

    Article  PubMed  Google Scholar 

  • Sethi, A., McAuslane, H. J., Nagata, R. T., and Nuessly, G. S. 2008. Romaine lettuce latex deters banded cucumber beetle (Coleoptera: Chrysomelidae) feeding: A vehicle for deployment of biochemical defenses. Entomol. Exp. Appl. 128:410–420.

    Article  Google Scholar 

  • Sirinphanic, J., and Kader, A. A. 1985. Effects of total CO2 on total phenolics, phenylalanine ammonia lyase and polyphenol oxidase in lettuce tissue. J. Am. Soc. Hort. Sci. 110:249–253.

    Google Scholar 

  • Stout, M. J., Fidantsef, A. L., Duffey, S. S., and Bostock, R. M. 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 

  • Valentines, M. C., Vilaplana, R., Usall, J., and Larrigaudiere, C. 2005. Involvement of enzymatic browning and peroxidase activity as resistance mechanisms in ‘Golden Delicious’ apples. Acta Hort. 682:2041–2048.

    CAS  Google Scholar 

  • Van Die, J. 1955. A comparative study of the particle fraction from Apocynaceae latices. Annal. Bogor. 2:1–124.

    CAS  Google Scholar 

  • Wang, J., and Constabel, C. P. 2004. Polyphenol oxidase overexpression in transgenic Populus enhances resistance to herbivory by forest tent caterpillar (Malacosoma disstria). Planta 220:87–96.

    Article  PubMed  CAS  Google Scholar 

  • Wititsuwannakul, D., Chareonthiphakorn, N., Pace, M., and Wititsuwannakul, R. 2002. Polyphenol oxidases from Hevea brasiliensis: purification and characterization. Phytochemistry 61:115–121.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Jennifer Hogsette (Department of Entomology and Nematology, University of Florida, Gainesville, FL, USA) and Julia Meredith (Center for Medical, Agricultural and Veterinary Entomology, United States Department of Agriculture, Gainesville, FL, USA) for help with insect rearing and lettuce growing, respectively. We also thank Murugesan Rangasamy (Department of Entomology and Nematology, University of Florida, Gainesville, FL, USA) for valuable suggestions on enzyme assays and Marty Marshall (Department Food Science and Food Nutrition, University of Florida, Gainesville, FL, USA) for use of his spectrophotometer. We are grateful to Ramandeep Kaur (Department of Entomology and Nematology, University of Florida, Gainesville, FL, USA) for help in setting up experiments and conducting enzyme assays. This research was supported by the Florida Agricultural Experiment Station and the USDA/ARS Tropical and Subtropical Agricultural Research Program.

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Authors and Affiliations

  1. Department of Entomology & Nematology, University of Florida, P.O. Box 110620, Gainesville, FL, 32611-0620, USA

    Amit Sethi & Heather J. McAuslane

  2. Horticultural Sciences Department, University of Florida, Gainesville, FL, 32611, USA

    Bala Rathinasabapathi

  3. Everglades Research and Education Center, University of Florida, 3200 East Palm Beach Rd, Belle Glade, FL, 33430-4702, USA

    Gregg S. Nuessly & Russell T. Nagata

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  1. Amit Sethi
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  2. Heather J. McAuslane
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  4. Gregg S. Nuessly
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  5. Russell T. Nagata
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Correspondence to Heather J. McAuslane.

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Sethi, A., McAuslane, H.J., Rathinasabapathi, B. et al. Enzyme Induction as a Possible Mechanism for Latex-Mediated Insect Resistance in Romaine Lettuce. J Chem Ecol 35, 190–200 (2009). https://doi.org/10.1007/s10886-009-9596-6

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