Resistance of plants to herbivorous insects: Can this resistance fail?

References

• Berge , M. A. and Rosenthal , G. A. 1991 . Metabolism of L canavanine and L canaline in the tobacco budworm Heliothis virescens Noctuidae . Chem. Res. Toxicol. , 4 : 237 – 240 .
   PubMed Web of Science ®Google Scholar
• Birk , Y. and Applebaum , S. W. 1960 . Effect of soybean trypsin inhibitors on the development and midgut proteolytic activity of Tribolium castaneum larvae . Enzymologia , 22 : 318 – 326 .
   Google Scholar
• Bleiler , J. A. and Rosenthal , G. A. 1988 . Biochemical ecology of canavanine‐eating seed predators . Ecology , 69 : 427 – 433 .
   Web of Science ®Google Scholar
• Bode , W. and Huber , R. 1992 . Natural protein proteinase inhibitors and their interaction with proteinases . Eur. J. Biochem. , 204 : 433 – 451 .
   PubMedGoogle Scholar
• Broadway , R. M. 1995 . Are insects resistant to plant proteinase inhibitors? . J. Insect Physiol. , 41 : 107 – 116 .
   Web of Science ®Google Scholar
• Broadway , R. M. 1996 . Dietary proteinase inhibitors alter complement of midgut proteases . Arch. Insect Biochem. Physiol. , 32 : 39 – 53 .
   Web of Science ®Google Scholar
• Broadway , R. M. and Duffey , S. S. 1986 . Plant proteinase inhibitors: Mechanism of action and effect on the growth and digestive physiology of larval Heliothis zea and Spodopteraexigua . J. Insect Physiol. , 32 : 827 – 833 .
   Web of Science ®Google Scholar
• Broadway , R. M. and Duffey , S. S. 1988 . The effect of plant protein quality on insect digestive physiology and the toxicity of plant proteinase inhibitors . J. Insect Physiol. , 34 : 1111 – 1117 .
   Web of Science ®Google Scholar
• Broadway , R. M. and Villani , M. G. 1995 . Does host range influence susceptibility of herbivorous insects to novel plant proteinase inhibitors? . Entomol. Exp. Appl. , 76 : 303 – 312 .
   Web of Science ®Google Scholar
• Burgess , E. P. J. , Main , C. A. , Stevens , P. S. , Christeiier , J. T. , Gatehouse , A. M. R. and Laing , W. A. 1994 . Effects of protease inhibitor concentration and combinations on the survival, growth and gut enzyme activities of the black field cricket, Teleogryllus commodus . J. Insect Physiol. , 40 : 803 – 811 .
   Web of Science ®Google Scholar
• Burgess , E. P. J. , Stevens , P. S. , Keen , G. K. , Laing , W. A. and Christeller , J. T. 1991 . Effects of protease inhibitors and dietary protein level on the black field cricket Teleogryllus commodus . Entomol. Exp. Appl. , 61 : 123 – 130 .
   Web of Science ®Google Scholar
• Casu , R. E. , Jarmey , J. M. , Elvin , C. M. and Eisemann , C. H. 1994 . Isolation of a trypsin‐like serine protease gene family from the sheep blowfly Lucilia cuprina . Insect Molec. Biol. , 3 : 159 – 170 .
   PubMedGoogle Scholar
• Chrispeels , M. J. and Raikhel , N. V. 1991 . Lectins, lectin genes, and their role in plant defense . Plant Cell , 3 : 1 – 9 .
   PubMed Web of Science ®Google Scholar
• Deloach , J. R. and Spates , G. E. 1980 . Effect of soybean trypsin inhibitor‐loaded erthrocytes on fecundity and midgut protease and hemolysis activity of stable flies . J. Econ. Entomol. , 73 : 590 – 594 .
   Web of Science ®Google Scholar
• Eigenbrode , S. D. , Espelie , K. E. and Shelton , A. M. 1991a . Behavior of neonate diamondback moth larvae (Plutella xylostella (L.)) on leaves and on extracted leaf waxes of resistantand susceptible cabbages . J. Chem. Ecol. , 17 : 1691 – 1704 .
   PubMed Web of Science ®Google Scholar
• Eigenbrode , S. D. , Stoner , K. A. , Shelton , A. M. and Kain , W. C. 1991b . Characteristics of glossy leaf waxes associated with resistance to diamondback moth (Lepidoptera: Plutellidae) in Brassica oleracea . J. Econ. Entomol. , 84 : 1609 – 1618 .
   Web of Science ®Google Scholar
• Felton , G. W. , Broadway , R. M. and Duffey , S. S. 1989 . Inactivation of proteinase inhibitor activity by plant‐derived quinones: Complications for host‐plant resistance against noctuid herbivores . J. Insect Physiol. , 35 : 981 – 990 .
   Web of Science ®Google Scholar
• Felton , G. W. and Duffey , S. S. 1992 . Ascorbate oxidation reduction in Helicoverpa zea as a scavenging system against dietary oxidants . Arch. Insect Biochem. Physiol. , 19 : 27 – 37 .
   Web of Science ®Google Scholar
• Felton , G. W. , Workman , J. and Duffey , S. S. 1992 . Avoidance of antinutritive plant defense: role of midgut pH in Colorado potato beetle . J. Chem. Ecol. , 18 : 571 – 583 .
   PubMed Web of Science ®Google Scholar
• Fernandes , K. V. S. , Sabelli , P. A. , Barratt , D. H. P. , Richardson , M. , Xavier‐Filho , J. and Shewry , P. R. 1993 . The resistance of cowpea seeds to bruchid beetles is not related to levels of cysteine proteinase inhibitors . Plant Molec. Biol. , 23 : 215 – 219 .
   PubMed Web of Science ®Google Scholar
• Foard , D. E. , Murdock , L. L. and Dunn , P. E. 1983 . Engineering of crop plants with resistance to herbivores and pathogens: an approach using primary gene products . Plant Molec. Biol. , 2 : 223 – 233 .
   Google Scholar
• Gatehouse , A. M. R. and Boulter , D. 1983 . Assessment of the antimetabolic effects of trypsin inhibitors from cowpea (Vigna unguiculata) and other legumes on development of the bruchid beetle Callosobruchus maculatus . J. Sci. Food Agric. , 34 : 345 – 350 .
   Web of Science ®Google Scholar
• Hilder , V. A. , Gatehouse , A. M. R. , Sheerman , S. E. , Barker , R. F. and Boulter , D. 1987 . A novel mechanism of insect resistance engineered into tobacco . Nature , 330 : 160 – 163 .
   Web of Science ®Google Scholar
• Hoffmann , M. P. , Zalom , F. G. , Wilson , L. T. , Smilanick , J. M. , Malyj , L. D. , Kiser , J. , Hilder , V. A. and Barnes , W. M. 1992 . Field evaluation of transgenic tobacco containing genes encoding Bacillus thuringiensis delta‐endotoxin or cowpea trypsin inhibitor: efficacy against Helicoverpa zea (Lepidoptera:Noctuidae) . J. Econ. Entomol. , 85 : 2516 – 2522 .
   Web of Science ®Google Scholar
• Huesing , J. E. , Murdock , L. L. and Shade , R. E. 1991a . Effect of wheat germ isolectins on development of cowpea weevil . Phytochemistry , 30 : 785 – 788 .
   Web of Science ®Google Scholar
• Huesing , J. E. , Shade , R. E. , Chrispeels , M. J. and Murdock , L. L. 1991b . Alpha‐amylase inhibitor, not phytohemagglutinin, explains resistance of common bean seeds to cowpea weevil . Plant Physiol. , 96 : 993 – 996 .
   PubMed Web of Science ®Google Scholar
• Ishimoto , M. and Kitamura , K. 1992 . Tolerance to the seed alpha‐amylase inhibitor by the two insect pests of the common bean, Zabrotes subfaciatus and Acanthoscelides obtectus (Coleoptera: Bruchidae) . Appl. Entomol. Zool. , 27 : 243 – 251 .
   Web of Science ®Google Scholar
• Johnson , R. , Narvaez , J. , An , G. and Ryan , C. 1989 . Expression of proteinase inhibitors 1 and 11 in transgenic tobacco plants: Effects on natural defense against Manduca sexta larvae . Proc. Natl. Acad. Sci. USA , 86 : 9871 – 9875 .
   PubMed Web of Science ®Google Scholar
• Johnston , K. A. , Gatehouse , J. A. and Anstee , J. H. 1993 . Effects of soybean protease inhibitors on the growth and development of larval Helicoverpa armigera . J. Insect Physiol. , 39 : 657 – 664 .
   Web of Science ®Google Scholar
• Juvik , J. A. , Shapiro , J. A. , Young , T. E. and Mutschler , M. A. 1994 . Acylglucoses from wild tomatoes alter behavior and reduce growth and survival of Helicoverpa zea and Spodoptera exigua (Lepidoptera: Noctuidae) . J. Econ. Entomol. , 87 : 482 – 492 .
   Web of Science ®Google Scholar
• Laskowski , M. 1985 . “ Protein inhibitors of serine proteinases ‐ Mechanism and classification ” . In Nutritional and Toxicological Significance of Enzyme Inhibitors in Foods , Edited by: Friedman , M. 1 – 17 . New York : Plenum Press .
   Google Scholar
• Liedl , B. E. , Lawson , D. M. , White , K. K. , Shapiro , J. A. , Cohen , D. E. , Carson , W. G. , Trumble , J. T. and Mutschler , M. A. 1995 . Acylsugars of wild tomato Lycopersicon pennellii alters settling and reduces oviposition of Bemisia argentifolii (Homoptera: Aleyroididae) . J. Econ. Entomol. , 88 : 742 – 748 .
   Web of Science ®Google Scholar
• Lorito , M. , Broadway , R. M. , Hayes , C. K. , Woo , S. L. , Noviello , C. , Williams , D. L. and Harman , G. E. 1994 . Proteinase inhibitors from plants as a novel class of fungicide . Molec. Plant‐Microbe Interact. , 7 : 525 – 527 .
   Web of Science ®Google Scholar
• Martin , J. S. , Martin , M. M. and Bernays , E. A. 1987 . Failure of tannic acid to inhibit digestion or reduce digestibility of plant protein in gut fluids of insect herbivores: Implications for theories of plant defense . J. Chem. Ecol. , 13 : 605 – 621 .
   PubMed Web of Science ®Google Scholar
• McManus , M. T. , White , D. W. R. and McGregor , P. G. 1994 . Accumulation of a chymotrypsin inhibitor in transgenic tobacco can affect the growth of insect pests . Transgen. Res. , 3 : 50 – 58 .
   Web of Science ®Google Scholar
• Oppert , B. , Morgan , T. D. , Culbertson , C. and Kramer , K. J. 1993 . Dietary mixtures of cysteine and serine proteinase inhibitors exhibit synergistic toxicity toward the red flour beetle, Tribolium castaneum . Comp. Biochem. Physiol. , 105C : 379 – 385 .
   Google Scholar
• Orozco‐Cardenas , M. , McGurl , B. and Ryan , C. A. 1993 . Expression of an antisense prosystemin gene in tomato plants reduces resistance toward Manduca sexta larvae . Proc. Natl. Acad. Sci. USA , 90 : 8273 – 8276 .
   PubMed Web of Science ®Google Scholar
• Orr , G. L. , Strickland , J. A. and Walsh , T. A. 1994 . Inhibition of Diabrotica larval growth by a multicystatin from potato tubers . J. Insect Physiol. , 40 : 893 – 900 .
   Web of Science ®Google Scholar
• Peterson , A. M. , Barillas‐Mury , C. V. and Wells , M. A. 1994 . Sequence of three cDNAs encoding an alkaline midgut trypsin from Manduca sexta . Insect Biochem. Molec. Biol. , 24 : 463 – 471 .
   PubMed Web of Science ®Google Scholar
• Purcell , J. P. , Greenplate , J. T. and Sammons , R. D. 1992 . Examination of midgut luminal proteinase activities in six economically important insects . Insect Biochem. Molec. Biol. , 22 : 41 – 47 .
   Web of Science ®Google Scholar
• Rosenthal , G. A. and Dahlman , D. L. 1991 . Incorporation of L canavanine into proteins and the expression of its antimetabolic effects . J. Agric. Food Chem. , 39 : 987 – 990 .
   Web of Science ®Google Scholar
• Rosenthal , G. A. , Dahlman , D. L. and Janzen , D. H. 1978 . LCanaline detoxification: A seed predator's biochemical mechanism . Science , 202 : 528 – 529 .
   PubMed Web of Science ®Google Scholar
• Rosenthal , G. A. , Reichhart , J. M. and Hoffmann , J. A. 1989 . L canavanine incorporation into vitellogenin and macromolecular conformation . J. Biol. Chem. , 264 : 13693 – 13696 .
   PubMed Web of Science ®Google Scholar
• Ryan , C. A. 1981 . Proteinase Inhibitors , New York : Academic Press . 351–370 pp.
   Google Scholar
• Schroeder , H. E. , Gollasch , S. , Moore , A. , Tabe , L. M. , Craig , S. , Hardie , D. C. , Chrispeels , M. J. , Spencer , D. and Higgins , T. J. V. 1995 . Bean alpha‐amylase inhibitor confers resistance to the pea weevil (Bruchus pisorum) in transgenic peas (Pisum sativumL.) . Plant Physiol. , 107 : 1233 – 1239 .
   PubMed Web of Science ®Google Scholar
• Shade , R. E. , Murdock , L. L. , Foard , D. E. and Pomeroy , M. A. 1986 . Artificial seed system for bioassay of cowpea weevil (Coleoptera: Bruchidae) growth and development . Environ. Entomol. , 15 : 1286 – 1291 .
   Web of Science ®Google Scholar
• Shukle , R. H. and Murdock , L. L. 1983 . Lipoxygenase, trypsin inhibitor, and lectin from soybeans: Effects on larval growth of Manduca sexta (Lepidoptera: Sphingidae) . Environ. Entomol. , 12 : 787 – 791 .
   Web of Science ®Google Scholar
• Spates , G. 1979 . Fecundity of the stable fly: effect of soybean trypsin inhibitor and phospholipase A inhibitor on the fecundity . Annals Entomol. Soc. Amer. , 72 : 845 – 849 .
   Web of Science ®Google Scholar
• Steffens , R. , Fox , F. R. and Kassell , B. 1978 . Effect of trypsin inhibitors on growth and metamorphosis of corn borer larvae Ostrinia nubilalis (Hubner) . J. Agric. Food Chem. , 26 : 170 – 174 .
   Web of Science ®Google Scholar
• Summers , C. B. and Felton , G. W. 1994 . Prooxidant effects of phenolic acids on the generalist herbivore Helicoverpa zea (Lepidoptera: Noctuidae): Potential mode of action for phenolic compounds in plant anti‐herbivore chemistry . Insect Biochem. Molec. Biol. , 24 : 943 – 953 .
   Web of Science ®Google Scholar
• Wolfson , J. L. and Murdock , L. L. 1995 . Potential use of protease inhibitors for host plant resistance: A test case . Environ. Entomol. , 24 : 52 – 57 .
   Web of Science ®Google Scholar
• Zhu , K. , Huesing , J. E. , Shade , R. E. and Murdock , L. L. 1994 . Cowpea trypsin inhibitor and resistance to cowpea weevil (Coleoptera: Bruchidae) in cowpea variety TVu2027 . Environ. Entomol. , 23 : 987 – 991 .
   Web of Science ®Google Scholar