Enzyme induction as a possible mechanism for latex-mediated insect resistance in romaine lettuce

Journal of Chemical Ecology

Volumn 35, Issue 2, 2009, Pages 190-200

  Sethi, Amit ^a   McAuslane, Heather J ^a   Rathinasabapathi, Bala ^a   Nuessly, Gregg S ^b   Nagata, Russell T ^b  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

Banded cucumber beetle; Chrysomelidae; Coleoptera; Diabrotica balteata; Enzymes; Induced defense; Lactuca sativa; Latex; Laticifers; Oxidative browning; Peroxidase; Phenylalanine ammonia lyase; Plant defense; Polyphenol oxidase

Indexed keywords

ADULT; BEETLE; CLIMBING PLANT; CULTIVAR; DIET; ENZYME ACTIVITY; FITNESS; FUNCTIONAL MORPHOLOGY; LEAFY VEGETABLE; PEST RESISTANCE; PLANT DEFENSE; SECONDARY METABOLITE;

CHRYSOMELIDAE; COLEOPTERA; CUCUMIS SATIVUS; DIABROTICA BALTEATA; HEXAPODA; LACTUCA; LACTUCA SATIVA;

CATECHOL OXIDASE; LATEX; PEROXIDASE; PHENYLALANINE AMMONIA LYASE; VEGETABLE PROTEIN;

ANIMAL; ARTICLE; BEETLE; ENZYME INDUCTION; ENZYMOLOGY; FEMALE; GENE EXPRESSION REGULATION; LETTUCE; METABOLISM; PHYSIOLOGY;

ANIMALS; BEETLES; CATECHOL OXIDASE; ENZYME INDUCTION; FEMALE; GENE EXPRESSION REGULATION, PLANT; LATEX; LETTUCE; PEROXIDASE; PHENYLALANINE AMMONIA-LYASE; PLANT PROTEINS;

EID: 67449136268     PISSN: 00980331     EISSN: 15731561     Source Type: Journal    
DOI: 10.1007/s10886-009-9596-6     Document Type: Article

References (62)

1. 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.
2. AZARKANA, M., WINTJENS, R., LOOZE, Y., and BAEYENS-VOLANT, D. 2004. Detection of three wound-induced proteins in papaya latex. Phytochemistry 65:525-534.
3. 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.
4. 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.
5. 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.
6. 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.
7. COLE, R. A. 1984. Phenolic acids associated with the resistance of lettuce cultivars to the lettuce root aphid. Ann. Appl. Biol. 105:129-145.
8. 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.
9. DIXON, R. A., and PAIVA, N. L. 1995. Stress induced phenylpropanoid metabolism. Plant Cell 7:1085-1097.
10. 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.
11. 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.
12. 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.
13. DUFFEY, S. S., and STOUT, M. J. 1996. Antinutritive and toxic components of plant defense against insects. Arch. Insect Biochem. Physiol. 32:3-37.
14. 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.
15. 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.
16. ESAU, K. 1965. Plant Anatomy. Wiley, Hoboken, New Jersey.
17. EVANS, F. J., and SCHMIDT, R. J. 1976. Two new toxins from the latex of Euphorbia poissonii. Phytochemistry 15:333-335.
18. 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.
19. FOX, M. G., and FRENCH, J. C. 1988. Systematic occurrence of sterols in latex of Araceae: subfamily Colocasioideae. Am. J. Bot. 75:132-137.
20. 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.
21. 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.
22. 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.
23. 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.
24. HAHLBROCK, K., and SCHEEL, D. 1989. Physiology and molecular biology of phenylpropanoid metabolism. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40:347-369.
25. 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.
26. 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.
27. 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.
28. 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.
29. 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.
30. 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.
31. 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.
32. 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.
33. 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.
34. 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.
35. 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.
36. 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.
37. MASKAN, M. 2001. Kinetics of color change of kiwi fruit during hot air and microwave drying. J. Food Eng. 48:169-176.
38. MATILE, P. 1976. Localizations of alkaloids and mechanism of their accumulation in vacuoles of Chelidonium majus laticifers. Nova Acta Leopold. Suppl. 7:65-73.
39. 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.
40. 2+/calmodulin-binding peroxidase from Euphorbia latex: novel aspects of calcium-hydrogen peroxide cross-talk in the regulation of plant defenses. Biochemistry 44:14120-14130.
41. 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.
42. 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.
43. NISHIO, S., BLUM, M. S., and TAKAHASHI, S. 1983. Intraplant distribution of cardenolides in Asclepias humistrata (Asclepiada-ceae) with additional notes on their fates in Tetraopes melanurus (Coleoptera: Cerambycidae) and Rhyssomatus lineaticollis (Co-leoptera: Curculionidae). Mem. Coll. Agric. Kyoto Univ.122:43-52.
44. 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.
45. 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/.
46. 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.
47. PICKARD, W. F. 2008. Laticifers and secretory ducts: two other tube systems in plants. New Phytol. 177:877-888.
48. 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.
49. 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.
50. RIBEREAU-GAYON, P. 1972. Plant Phenolics. Oliver and Boyd, Edinburgh, UK.
51. RYDER, E. J. 1998. Lettuce, Endive and Chicory. CABI, Cambridge, UK.
52. SAS INSTITUTE. 2003. Guide for Personal Computers, version 9.1.3. SAS Institute, Cary, North Carolina.
53. 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.
54. SETHI, A. 2007. Biochemical Mode of Multiple Insect Resistance in Romaine Lettuce Cultivar. Ph.D. dissertation. University of Florida, Gainesville, Florida.
55. 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.
56. 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.
57. 2 on total phenolics, phenylalanine ammonia lyase and polyphenol oxidase in lettuce tissue. J. Am. Soc. Hort. Sci. 110:249-253.
58. 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.
59. 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.
60. VAN DIE, J. 1955. A comparative study of the particle fraction from Apocynaceae latices. Annal. Bogor. 2:1-124.
61. WANG, J., and CONSTABEL, C. P. 2004. Polyphenol oxidase over-expression in transgenic Populus enhances resistance to herbivory by forest tent caterpillar (Malacosoma disstria). Planta 220:87-96.
62. WITITSUWANNAKUL, D., CHAREONTHIPHAKORN, N., PACE, M., and WITITSUWANNAKUL, R. 2002. Polyphenol oxidases from Hevea brasiliensis: purification and characterization. Phytochemistry 61:115-121.