Nutritive Quality of Plant Protein: Sources of Variation and Insect Herbivore Responses

Archives of Insect Biochemistry and Physiology

Volumn 32, Issue 1, 1996, Pages 107-130

  Felton, Gary W ^a  

^a UNIVERSITY OF ARKANSAS   (United States)

Author keywords

Herbivore performance; Host plant suitability; Phytochemicals; Plant protein quality

Indexed keywords

EID: 0000551928     PISSN: 07394462     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1520-6327(1996)32:1<107::AID-ARCH7>3.0.CO;2-X     Document Type: Article

References (109)

1. Aggarwal KK, Saluja D, Sachar RC (1993): Phosphorylation of RUBISCO in Cicer arientinum: Non-phosphoprotein nature of RUBISCO in Nicotiana tabacum. Phytochemistry 34:329-335.
2. Appel HM (1994): The chewing herbivore gut lumen: Physicochemical conditions and their impact on plant nutrients, allelochemicals, and insect pathogens. In Bernays EA (ed): Insect-Plant Interactions, vol. 5. Boca Raton: CRC Press, Inc., pp 210-223.
3. Appel HM, Maines LW (1995): The influence of host plant on gut conditions of gypsy moth caterpillars. J Insect Physiol 41:241-246.
4. Appel HM, Martin MM (1990): Gut redox conditions in herbivorous lepidopteran larvae. J Chem Ecol 16:3277-3290.
5. Berenbaum MR (1995): Turnabout is fair play: Secondary roles for primary compounds. J Chem Ecol 21:925-940.
6. Bernays EA, Chapman RF (1994): Host-Plant Selection by Phytophagous Insects. New York: Chapman & Hall.
7. Bi JL, Felton GW (1995): Foliar oxidative stress and insect herbivory: Primary compounds, secondary metabolites and reactive oxygen species as components of induced resistance. J Chem Ecol 21:1511-1530.
8. Bi JL, Felton GW, Mueller AJ (1994): Induced resistance in soybean to Helicoverpa zea: Role of plant protein quality. J Chem Ecol 20:183-198.
9. Blakemore D, Williams S, Lehane MJ (1995): Protein stimulation of trypsin secretion from the opaque zone midgut cells of Stomyx calcitrans. Comp Biochem Physiol 110B:301-307.
10. Bloem KA, Duffey SS (1990): Effect of protein type and quantity on growth and development of larval Heliothis zea and Spodoptera exigua and the endoparasitoid Hyposter exiguae. Entomol Exp Appl 54:141-148.
11. Boulter D, Derbyshire E (1978): The general properties, classification and distribution of plant proteins. In Norton G (ed): Plant Proteins. London: Butterworths, pp 3-24.
12. Bradley DJ, Kjellbom P, Lamb CJ (1992): Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: A novel, rapid defense response. Cell 70:21-30.
13. Brisson LF, Tenhaken R, Lamb C (1994): Function of oxidative cross-linking of cell wall structural proteins in plant disease resistance. Plant Cell 6:1703-1712.
14. Broadway RM (1995): Are insects resistant to plant proteinase inhibitors? J Insect Physiol 41:107-116.
15. Broadway RM (1996): Dietary proteinase inhibitors alter complement of midgut proteases. Arch Insect Biochem Physiol 32:39-54.
16. Broadway RM, Duffey SS (1986a): The effect of dietary protein on the growth and digestive physiology of larval Heliothis zea and Spodoptera exigua. J Insect Physiol 32:673-680.
17. Broadway RM, Duffey SS (1986b): Plant proteinase inhibitors: Mechanism of action and effect on the growth and digestive physiology of larval Heliothis zea and Spodoptera exigua. J Insect Physiol 32:827-833.
18. Broadway RM, Duffey SS (1988): The effect of plant protein quality on insect digestive physiology and the toxicity of plant proteinase inhibitors. J Insect Physiol 34:1111-1117.
19. Brodbeck BV, Andersen PC, Mizell III RF (1996): Utilization of primary nutrients by the polyphagous xylophage, Homalodisca coagulata, reared on single host species. Arch Insect Biochem Physiol 32:65-84.
20. Browne LB (1993): Physiologically induced changes in resource-oriented behavior. Ann Rev Entomol 38:1-25.
21. Brugger KE (1992): Anatomical adaptation of the gut to diet in red-winged blackbirds (Agelaius phoeniceous). Auk 108:562-567.
22. Campos F, Atkinson J, Arnason JT, Philogene BJR, Morand P, Werstiuk NH, Timmins G (1988): Toxicity and toxicokinetics of 6-methoxybenzoxazolinone (MBOA) in the European corn borer, Ostrinia nubilalis (Hubner). J Chem Ecol 14:989-1002.
23. Campos F, Atkinson J, Arnason JT, Philogene BJR, Morand P, Werstiuk NH, Timmins G (1989): Toxicokinetics of 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) in the European corn borer, Ostrinia nubilalis (Hubner). J Chem Ecol 15:1989-2001.
24. Christeller JT, Laing WA, Markwick NP, Burgess EPJ (1992): Midgut protease activities in 12 phytophagous lepidopteran larvae: Dietary and protease inhibitor interactions. Insect Biochem Mol Biol 22:735-746.
25. Christeller JT, Gatehouse AMR, Laing WA (1994a): The interaction of the elastase inhibitor, elgin C, with insect digestive endopeptidases: The effect of pH on the dissociation constants. Insect Biochem Mol Biol 24:103-109.
26. Christeller JT, Markwick NP, Burgess EPJ (1994b): Midgut proteinase activities of three keratinolytic larvae, Hofmannophila pseudospretella, Tineola bisselliella, and Anthrenocerus australis, and the effect of proteinase inhibitors on proteolysis. Arch Insect Biochem Physiol 25:159-173.
27. Cooper RA, Schal C (1992): Effect of protein type and concentration on development and reproduction of the German cockroach, Blatella germanica. Entomol Exp Appl 63:123-134.
28. Crafts-Brander SJ, Salvucci ME, Egli DB (1991): Fruit removal in soybean induces the formation of an insoluble form of ribulose-1,5-biphosphate carboxylase/oxygenase in leaf extracts. Planta 183:300-306.
29. Culvenor CCJ, Dann AT, Dick AT (1962): Alkylation as the mechanism by which the hepatotoxic pyrrolizidine alkaloids act on cell nuclei. Nature 195:570-573.
30. De Sales MP, Macedo MLR, Xavier-Filho JX (1992): Digestibility of cowpea (Vigna unguiculata) vicilins by pepsin, papain, and bruchid (insect) midgut proteinases. Comp Biochem Physiol 103B:945-950.
31. Duffey SS, Felton GW (1989): Plant enzymes in resistance to insects. In Whitaker JR, Sonnet PE (eds): Biocatalysis in Agricultural Biotechnology. Washington, DC: American Chemical Society, pp 288-313.
32. Duffey SS, Felton GW (1991): Enzymatic antinutritive defenses of the tomato plant against insects. In Hedin PA (ed): Naturally Occurring Pest Bioregulators. Washington, DC: American Chemical Society, pp 166-197.
33. Ehrlich PH, Raven PR (1964): Butterflies and plants: A study of coevolution. Evolution 18: 586-608.
34. Enyedi AJ, Yalpani N, Silverman P, Raskin I (1992): Signal molecules in systemic plant resistance to pathogens and pests. Cell 70:879-886.
35. Felix CR, Betschart B, Billingsley PF, Freyvogel TA (1991): Post-feeding induction of trypsin in the midgut of Aedes aegypti L. (Diptera: Culicidae) is separable into two cellular phases. Insect Biochem 21:197-203.
36. Feller U, Fischer A (1994): Nitrogen metabolism in senescing leaves. Crit Rev Plant Sci 13: 241-273.
37. Felton GW, Duffey SS (1991): Reassessment of the role of gut alkalinity and detergency in insect herbivory. J Chem Ecol 17:1821-1836.
38. Felton GW, Summers CB (1993): Potential role of ascorbate oxidase as a plant defense protein against insect herbivory. J Chem Ecol 19:1553-1568.
39. Felton GW, Donato K, Del Vecchio RJ, Duffey SS (1989): Activation of plant foliar oxidases by insect feeding reduces the nutritional quality of foliage for herbivores. J Chem Ecol 15: 2667-2694.
40. Felton GW, Donato KK, Broadway RM, Duffey SS (1992): Impact of oxidized plant phenolics on the nutritional quality of dietary protein to a noctuid herbivore, Spodoptera exigua. J Insect Physiol 38:277-285.
41. Felton GW, Summers CB, Mueller AJ (1994a): Oxidative responses in soybean foliage to herbivory by bean leaf beetle and three-cornered alfalfa hopper. J Chem Ecol 20: 639-650.
42. Felton GW, Bi JL, Summers CB, Mueller AJ, Duffey SS (1994b): Potential role of lipoxygenases in defense against insect herbivory. J Chem Ecol 20:651-666.
43. Fraenkel GS (1959): The raison d'etre of secondary plant substances. Science 129:1466-1470.
44. Garcia-Ferris C, Moreno J (1994): Oxidative modification and breakdown of ribulose-1,5-bisphosphate carboxylase/oxygenase in Euglena gracilis by nitrogen starvation. Planta 193:208-215.
45. Gardner HW (1979): Lipid hydroperoxide reactivity with proteins and amino acids: A review. J Agric Food Chem 27:220-228.
46. Gershenzon J, Croteau R (1991): Terpenoids. In Rosenthal GA, Berenbaum MR (eds): Herbivores: Their Interactions with Secondary Metabolites, vol. 1. San Diego: Academic Press, pp 165-220.
47. Giulivi C, Davies KJA (1993): Dityrosine and tyrosine oxidation products are endogenous markers for the selective proteolysis of oxidatively modified red blood cell hemoglobin by (the 19 S) proteosome. J Biol Chem 268:8752-8759.
48. Harding JJ (1985): Nonenzymatic covalent posttranslational modification of proteins in vivo. Adv Protein Chem 37:247-334.
49. Haukioja E, Ruohomaki K, Suomela J, Vuorisalo T (1991): Nutritional quality as a defense against herbivores. Forest Ecol Manag 39:237-245.
50. Hedin PA, Parrott WL, Jenkins JN (1991): Effects of cotton plant allelochemicals and nutrients on behavior and development of tobacco budworm. J Chem Ecol 17:1107-1121.
51. Hinks CF, Hupka D, Olfert O (1993): Nutrition and the protein economy in grasshoppers and locusts. Comp Biochem Physiol 104A:133-142.
52. Hinson JA, Roberts DW (1992): Role of covalent and noncovalent interactions in cell toxicity: Effects on proteins. Ann Rev Pharmacol Toxicol 32:471-510.
53. Horie Y, Watanabe K (1983): Effect of various kinds of dietary protein and supplementation with limiting amino acids on growth, haemolymph components and uric acid excretion in the silkworm, Bombyx mori. J Insect Physiol 29:187-199.
54. Houseman JG, Campos F, Thie NMR, Philogene BJR, Atkinson J, Morand P, Arnason JT (1992): Effect of maize-derived compounds DIMBOA and MBOA on growth and digestive processes of European corn borer (Lepidoptera: Pyralidae). J Econ Entomol 85: 669-674.
55. Jackson S (1992): Do seabird gut sizes and mean retention times reflect adaptation to diet and foraging method? Physiol Zool 65:674-697.
56. Johnson KS, Felton GW (1996): Potential influence of midgut pH and redox potential on protein utilization in insect herbivores. Arch Insect Biochem Physiol 32:85-106.
57. Johnson KS, Felton GW (1996): Physiological and dietary influences on midgut redox conditions in generalist lepidopteran larvae. J Insect Physiol (in press).
58. Karasov WH, Diamond JM (1988): Interplay between physiology and ecology in digestion. BioSci 38:602-611.
59. Karasov WH, Levey DJ (1990): Digestive system trade-offs and adaptations of frugivorous passerine birds. Physiol Zool 63:1248-1270.
60. Karasov WH, Solberg DH, Chang SD, Hughes M, Stein ED, Diamond JM (1985): Is intestinal transport of sugars and amino acids subject to critical-period programming? Am J Physiol 249:G770-G785.
61. Karowe DN, Martin MM (1989): The effects of quantity and quality of diet nitrogen on the growth, efficiency of food utilization, nitrogen budget, and metabolic rate of fifth-instar Spodoptera eridania larvae (Lepidoptera: Noctuidae). J Insect Physiol 35:699-708.
62. Kawakishi S, Kaneko T (1987): Interaction of proteins with allyl isothiocyanate. J Agric Food Chem 35:85-88.
63. Larocque AM, Houseman JG (1990): Effect of ingested soybean, ovomucoid and corn protease inhibitors on digestive processes of the European corn borer, Ostrinia nubilalis (Lepidoptera: Pyralidae). J Insect Physiol 36:691-697.
64. Lehane MJ, Blakemore D, Williams S, Moffat MR (1995): Mini review: Regulation of digestive enzyme levels in insects. Comp Biochem Physiol 110B:285-289.
65. Lhoste EF, Fiszlewicz M, Gueugneau A-M, Corring T (1994): Adaptation of exocrine pancreas to dietary proteins: Effect of the nature of protein and rat strain on enzyme activities and messenger RNA levels. J Nutr Biochem 5:84-94.
66. Lundberg P, Palo RT (1993): Resource use, plant defenses, and optimal digestion in ruminants. Oikos 68:224-228.
67. Matheis G, Whitaker JR (1987): A review: Enzymatic cross-linking of proteins applicable to foods. J Food Biochem 11:309-327.
68. Mattson WA (1980): Herbivory in relation to plant nitrogen content. Ann Rev Ecol 11:19-38.
69. McNeill S, Southwood TRE (1978): The role of nitrogen in the development of insect plant relationships. In Harborne J (ed): Biochemical Aspects of Plant and Animal Coevolution. London: Academic Press, pp 77-98.
70. Mehta RA, Fawcett TW, Portah D, Mato AK (1992): Oxidative stress causes rapid membrane translocation and in vivo degradation of ribulose-1,5-bisphosphate carboxylase/oxygenase. J Biol Chem 267:2810-2816.
71. Montandon R, Stipanovich RD, Williams HJ, Sterling WL, Vinson SB (1987): Nutritional indices and excretion of gossypol by Alabama argillacea (Hubner) and Heliothis virescens (F.) (Lepidoptera: Noctuidae) fed glanded and glandless cotyledonary cotton leaves. J Econ Entomol 80:32-36.
72. Moore RF (1983): Effect of dietary gossypol on the boll weevil (Coleoptera: Curculionidae). J Econ Entomol 76:696-699.
73. Neal JJ (1996): The brush border membrane and amino acid transport. Arch Insect Biochem Physiol 32:55-64.
74. Nelson SD, Pearson PG (1990): Covalent and noncovalent interactions in acute lethal cell injury caused by chemicals. Ann Rev Pharmacol Toxicol 30:169-195.
75. O'Brien PJ (1991): Molecular mechanisms of quinone cytotoxicity. Chem Biol Interact 80:1-41.
76. Ohgushi T (1992): Resource limitation on insect herbivore populations. In Hunter MD, Ohgushi T, Prie PW (eds): Effects of Resource Distribution on Animal-Plant Interactions. San Diego: Academic Press, Inc., pp 199-241.
77. Pacifici RE, Davies KJA (1990): Protein degradation as an index of oxidative stress. Methods Enzymol 186:485-502.
78. Perez FJ, Niemeyer HM (1985): The reduction of 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one by thiols. Phytochemistry 24:2963-2966.
79. Potter SM, Jimenez-Flores R, Pollack SM, Lone TA, Berber-Jiminez MD (1993): Protein-saponin interaction and its influence on blood lipids. J Agric Food Chem 41:1287-1291.
80. Raubenheimer D (1992): Tannic acid, protein, and digestible carbohydrate: Dietary imbalance and nutritional compensation in locusts. Ecology 73:1012-1027.
81. Reuveni M, Hong YS, Dunn PE, Neal JJ (1993): Leucine transport into brush border membrane vesicles from guts of Leptinotarsus decemlineata and Manduca sexta. Comp Biochem Physiol 104A:267-272.
82. Richard RC, Goupy PM, Nicolas JJ, Lacombe J-M, Pavia AA (1991): Cysteine as an inhibitor of enzymatic browning. 1. Isolation and characterization of addition compounds formed during oxidation of phenolics by apple polyphenol oxidase. J Agric Food Chem 39:841-847.
83. Rojas MG, Stipanovich RD, Williams HJ, Vinson SB (1992): Metabolism of gossypol by Heliothis virescens (F.) (Lepidoptera: Noctuidae). Environ Entomol 21:518-526.
84. Roy DM, Schneeman BO (1981): Effect of soyprotein, casein, and trypsin inhibitor on cholesterol, bile acids, and pancreatic enzymes in mice. J Nutr 111:878-885.
85. Scharrer E (1989): Regulation of intestinal amino acid transport. In Friedman M (ed): Absorption and Utilization of Amino Acids. Boca Raton, FL: CRC Press, Inc., pp 57-68.
86. Schultz JC, Lechowicz MJ (1986): Hostplant, larval age, and feeding behavior influence midgut pH in the gypsy moth (Lymantria dispar). Oecologia 71:133-137.
87. Scriber JM, Slansky Jr F (1981): The nutritional ecology of immature insects. Ann Rev Entomol 26:183-211.
88. Sheen SJ (1991): Comparison of chemical and functional properties of soluble leaf proteins from four plant species. J Agric Food Chem 39:681-685.
89. Simpson SJ, Simpson CL (1990): The mechanisms of compensation by phytophagous insects. In Bernays EA (ed): Insect-Plant Interactions, vol. 2. Boca Raton, FL: CRC Press Inc., pp 112-160.
90. Slansky F Jr (1993): Nutritional ecology: The fundamental quest for nutrients. In Stamp NE, Casey TM (eds): Caterpillars-Ecological and Evolutionary Constraints on Foraging. New York: Chapman & Hall, pp 29-91.
91. Slansky F Jr, Feeny P (1977): Stabilization of the rate of nitrogen accumulation by larvae of the cabbage butterfly on wild and cultivated foodplants. Ecol Monogr 47:209-228.
92. Slansky F Jr, Wheeler GS (1991): Food consumption and utilization responses to dietary dilution with cellulose and water by velvetbean caterpillars, Anticarsia gemmnatalis. Physiol Entomol 16:99-116.
93. Slansky F Jr, Wheeler GS (1992): Caterpillars' compensatory feeding response to diluted nutrients leads to a toxic allelochemical dose. Entomol Exp Appl 65:171-186.
94. Stadtman ER (1993): Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions. Ann Rev Biochem 62:797-821.
95. Stockhoff BA (1993): Ontogenetic change in dietary selection for protein and lipid by gypsy moth larvae. J Insect Physiol 39:677-686.
96. Thomas H, Stoddart JL (1980): Leaf senescence. Ann Rev Plant Physiol 31:83-111.
97. Thompson D, Constantin-Teodosiu D, Egestad B, Mickos H, Moldeus P (1990): Formation of glutathione conjugates during oxidation of eugenol by microsomal fractions of rat liver and lung. Biochem Pharmacol 39:1587-1595.
98. Uchida K, Stadtman ER (1992): Modification of histidine residues in proteins by reaction with 4-hydroxynonenal. Proc Natl Acad Sci USA 89:4544-4548.
99. Waldbauer GP, Friedman S (1991): Self-selection of optimal diets by insects. Ann Rev Entomol 36:43-63.
100. Waldbauer GP, Cohen RW, Friedman S (1984): Self-selection of an optimal nutrient mix from defined diets by larvae of the corn earworm, Heliothis zea (Boddie). Physiol Zool 57: 590-597.
101. Whitaker JR (1986): Covalent attachment of essential amino acids to proteins to improve their nutritional and functional properties. In Feeney RE, Whitaker JR (eds): Protein Tailoring for Food and Medical Uses. New York: Marcel Dekker, Inc., pp 41-74.
102. Wittenbach VA (1983): Effect of pod removal on leaf photosynthesis and soluble protein composition of field-growth soybeans. Plant Physiol 73:121-124.
103. Wolfersberger MG (1993): Preparation and partial characterization of amino acid transporting brush border membrane vesicles from the larval midgut of the gypsy moth (Lymantria dispar). Arch Insect Biochem Physiol 24:139-147.
104. Yang Y, Joern A (1994a): Gut size changes in relation to variable food quality and body size in grasshoppers. Functional Ecol 8:36-45.
105. Yang Y, Joern A (1994b): Compensatory feeding in response to variable food quality by Melanoplus differentialis. Physiol Entomol 19:75-82.
106. Yeoh H-H, Watson L (1982): Taxonomic variation in total leaf protein amino acid compositions of grasses. Phytochemistry 21:615-626.
107. Yeoh H-H, Wee Y-C, Watson L (1986): Taxonomic variation in total leaf protein amino acid compositions of monocotyledonous plants. Biochem Syst Ecol 14:91-96.
108. Yeoh H-H, Wee Y-C, Watson L (1992): Leaf protein contents and amino acid patterns of dicotyledonous plants. Biochem Syst Ecol 20:657-663.
109. Young VR, Marchini JS (1990): Mechanisms and nutritional significance of metabolic responses to altered intakes of protein and amino acids, with reference to nutritional adaptations in humans. Am J Clin Nutr 51:270-289.