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Annual Review of Entomology

Volume 60, 2015

Insect Response to Plant Defensive Protease Inhibitors

Abstract

Plant protease inhibitors (PIs) are natural plant defense proteins that inhibit proteases of invading insect herbivores. However, their anti-insect efficacy is determined not only by their potency toward a vulnerable insect system but also by the response of the insect to such a challenge. Through the long history of coevolution with their host plants, insects have developed sophisticated mechanisms to circumvent antinutritional effects of dietary challenges. Their response takes the form of changes in gene expression and the protein repertoire in cells lining the alimentary tract, the first line of defense. Research in insect digestive proteases has revealed the crucial roles they play in insect adaptation to plant PIs and has brought about a new appreciation of how phytophagous insects employ this group of molecules in both protein digestion and counterdefense. This review provides researchers in related fields an up-to-date summary of recent advances.

Keyword(s): adaptation, counterdefense, digestion, phytophagous insects, protease, transcription regulation
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2015-01-07
2024-04-27
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Literature Cited

  1. Abdeen A, Virgos A, Olivella E, Villanueva J, Aviles X. 1.  et al. 2005. Multiple insect resistance in transgenic tomato plants over-expressing two families of plant proteinase inhibitors. Plant Mol. Biol. 57:189–202 [Google Scholar]
  2. Ahn JE, Guarino LA, Zhu-Salzman K. 2.  2007. Seven-up facilitates insect counter-defense by suppressing cathepsin B expression. FEBS J. 274:2800–14 [Google Scholar]
  3. Ahn JE, Guarino LA, Zhu-Salzman K. 3.  2010. Coordination of hepatocyte nuclear factor 4 and Seven-up controls insect counter-defense cathepsin B expression. J. Biol. Chem. 285:6573–84 [Google Scholar]
  4. Ahn JE, Salzman RA, Braunagel SC, Koiwa H, Zhu-Salzman K. 4.  2004. Functional roles of specific bruchid protease isoforms in adaptation to a soybean protease inhibitor. Insect Mol. Biol. 13:649–57 [Google Scholar]
  5. Ahn JE, Zhu-Salzman K. 5.  2009. CmCatD, a cathepsin D-like protease has a potential role in insect defense against a phytocystatin. J. Insect Physiol. 55:678–85 [Google Scholar]
  6. Altpeter F, Diaz I, McAuslane H, Gaddour K, Carbonero P, Vasil IK. 6.  1999. Increased insect resistance in transgenic wheat stably expressing trypsin inhibitor CMe. Mol. Breed. 5:53–63 [Google Scholar]
  7. Barrett AJ, Kembhavi AA, Brown MA, Kirschke H, Knight CG. 7.  et al. 1982. l-Trans-epoxysuccinyl-leucylamido(4-guanidino)butane (E-64) and its analogues as inhibitors of cysteine proteinases including cathepsins B, H and L. Biochem. J. 201:189–98 [Google Scholar]
  8. Barrett AJ, Rawlings ND, Woessner JF. 8.  1998. Handbook of Proteolytic Enzymes San Diego, CA: Academic
  9. Baum JA, Bogaert T, Clinton W, Heck GR, Feldmann P. 9.  et al. 2007. Control of coleopteran insect pests through RNA interference. Nat. Biotechnol. 25:1322–26 [Google Scholar]
  10. Bayes A, Comellas-Bigler M, de la Vega MR, Maskos K, Bode W. 10.  et al. 2005. Structural basis of the resistance of an insect carboxypeptidase to plant protease inhibitors. Proc. Natl. Acad. Sci. USA 102:16602–7 [Google Scholar]
  11. Bayes A, de la Vega MR, Vendrell J, Aviles FX, Jongsma MA, Beekwilder J. 11.  2006. Response of the digestive system of Helicoverpa zea to ingestion of potato carboxypeptidase inhibitor and characterization of an uninhibited carboxypeptidase B. Insect Biochem. Mol. 36:654–64 [Google Scholar]
  12. Bhatia V, Bhattacharya R, Uniyal PL, Singh R, Niranjan RS. 12.  2012. Host generated siRNAs attenuate expression of serine protease gene in Myzus persicae. PLOS ONE 7:e46343 [Google Scholar]
  13. Billingsley PF, Lehane MJ. 13.  1996. Structure and ultrastructure of the insect midgut. See Ref. 64 3–30
  14. Bolter CJ, Jongsma MA. 14.  1995. Colorado potato beetles (Leptinotarsa decemlineata) adapt to proteinase-inhibitors induced in potato leaves by methyl jasmonate. J. Insect Physiol. 41:1071–78 [Google Scholar]
  15. Bown DP, Wilkinson HS, Gatehouse JA. 15.  1997. Differentially regulated inhibitor-sensitive and insensitive protease genes from the phytophagous insect pest, Helicoverpa armigera, are members of complex multigene families. Insect Biochem. Mol. 27:625–38 [Google Scholar]
  16. Bown DP, Wilkinson HS, Gatehouse JA. 16.  2004. Regulation of expression of genes encoding digestive proteases in the gut of a polyphagous lepidopteran larva in response to dietary protease inhibitors. Physiol. Entomol. 29:278–90 [Google Scholar]
  17. Breugelmans B, Simonet G, van Hoef V, van Soest S, Broeck JV. 17.  2009. Pacifastin-related peptides: structural and functional characteristics of a family of serine peptidase inhibitors. Peptides 30:622–32 [Google Scholar]
  18. Brioschi D, Nadalini LD, Bengtson MH, Sogayar MC, Moura DS, Silva-Filho MC. 18.  2007. General up regulation of Spodoptera frugiperda trypsins and chymotrypsins allows its adaptation to soybean proteinase inhibitor. Insect Biochem. Mol. 37:1283–90 [Google Scholar]
  19. Brito LO, Lopes AR, Parra JRP, Terra WR, Silva MC. 19.  2001. Adaptation of tobacco budworm Heliothis virescens to proteinase inhibitors may be mediated by the synthesis of new proteinases. Comp. Biochem. Phys. B 128:365–75 [Google Scholar]
  20. Broadway RM. 20.  1997. Dietary regulation of serine proteinases that are resistant to serine proteinase inhibitors. J. Insect Physiol. 43:855–74 [Google Scholar]
  21. Broadway RM, Duffey SS. 21.  1986. Plant proteinase-inhibitors—mechanism of action and effect on the growth and digestive physiology of larval Heliothis zea and Spodoptera exiqua. J. Insect Physiol. 32:827–33 [Google Scholar]
  22. Brunelle F, Cloutier C, Michaud D. 22.  2004. Colorado potato beetles compensate for tomato cathepsin D inhibitor expressed in transgenic potato. Arch. Insect Biochem. Physiol. 55:103–13 [Google Scholar]
  23. Brunelle F, Nguyen-Quoc B, Cloutier C, Michaud D. 23.  1999. Protein hydrolysis by Colorado potato beetle, Leptinotarsa decemlineata, digestive proteases: the catalytic role of cathepsin D. Arch. Insect Biochem. Physiol. 42:88–98 [Google Scholar]
  24. Chapman RF. 24.  1998. Alimentary canal, digestion and absorption. The Insects: Structure and Function38–68 Cambridge: Cambridge Univ. Press, 4th ed.. [Google Scholar]
  25. Chen MS. 25.  2008. Inducible direct plant defense against insect herbivores: a review. Insect Sci. 15:101–14 [Google Scholar]
  26. Chi YH, Salzman RA, Balfe S, Ahn JE, Sun W. 26.  et al. 2009. Cowpea bruchid midgut transcriptome response to a soybean cystatin—costs and benefits of counter-defence. Insect Mol. Biol. 18:97–110 [Google Scholar]
  27. Christeller JT, Laing WA, Markwick NP, Burgess EPJ. 27.  1992. Midgut protease activities in 12 phytophagous Lepidopteran larvae—dietary and protease inhibitor interactions. Insect Biochem. Mol. Biol. 22:735–46 [Google Scholar]
  28. Cloutier C, Jean C, Fournier M, Yelle S, Michaud D. 28.  2000. Adult Colorado potato beetles, Leptinotarsa decemlineata compensate for nutritional stress on oryzacystatin I-transgenic potato plants by hypertrophic behavior and over-production of insensitive proteases. Arch. Insect Biochem. Physiol. 44:69–81 [Google Scholar]
  29. Cristofoletti PT, Ribeiro AF, Deraison C, Rahbe Y, Terra WR. 29.  2003. Midgut adaptation and digestive enzyme distribution in a phloem feeding insect, the pea aphid Acyrthosiphon pisum. J. Insect Physiol. 49:11–24 [Google Scholar]
  30. Cristofoletti PT, Ribeiro AF, Terra WR. 30.  2005. The cathepsin L-like proteinases from the midgut of Tenebrio molitor larvae: sequence, properties, immunocytochemical localization and function. Insect Biochem. Mol. Biol. 35:883–901 [Google Scholar]
  31. Dawkar VV, Chikate YR, Gupta VS, Slade SE, Giri AP. 31.  2011. Assimilatory potential of Helicoverpa armigera reared on host (chickpea) and nonhost (Cassia tora) diets. J. Proteome Res. 10:5128–38 [Google Scholar]
  32. De Leo F, Bonade-Bottino MA, Ceci LR, Gallerani R, Jouanin L. 32.  1998. Opposite effects on Spodoptera littoralis larvae of high expression level of a trypsin proteinase inhibitor in transgenic plants. Plant Physiol. 118:997–1004 [Google Scholar]
  33. Deraison C, Darboux I, Duportets L, Gorojankina T, Rahbe Y, Jouanin L. 33.  2004. Cloning and characterization of a gut-specific cathepsin L from the aphid Aphis gossypii. Insect Mol. Biol. 13:165–77 [Google Scholar]
  34. Duan X, Li X, Xue Q, Abo-el-Saad M, Xu D, Wu R. 34.  1996. Transgenic rice plants harboring an introduced potato proteinase inhibitor II gene are insect resistant. Nat. Biotechnol. 14:494–98 [Google Scholar]
  35. Foissac X, Edwards MG, Du JP, Gatehouse AMR, Gatehouse JA. 35.  2002. Putative protein digestion in a sap-sucking homopteran plant pest (rice brown plant hopper; Nilaparvata lugens: Delphacidae)—identification of trypsin-like and cathepsin B-like proteases. Insect Biochem. Mol. 32:967–78 [Google Scholar]
  36. Fonseca FPP, Soares-Costa A, Ribeiro AF, Rosa JC, Terra WR, Henrique-Silva F. 36.  2012. Recombinant expression, localization and in vitro inhibition of midgut cysteine peptidase (Sl-CathL) from sugarcane weevil, Sphenophorus levis. Insect Biochem. Mol. Biol. 42:58–69 [Google Scholar]
  37. Gatehouse AMR, Davison GM, Newell CA, Merryweather A, Hamilton WDO. 37.  et al. 1997. Transgenic potato plants with enhanced resistance to the tomato moth, Lacanobia oleracea: growth room trials. Mol. Breed. 3:49–63 [Google Scholar]
  38. Gatehouse JA. 38.  2011. Prospects for using proteinase inhibitors to protect transgenic plants against attack by herbivorous insects. Curr. Protein Pept. Sci. 12:409–16 [Google Scholar]
  39. Girard C, Le Metayer M, Bonade-Bottino M, Pham-Delegue MH, Jouanin L. 39.  1998. High level of resistance to proteinase inhibitors may be conferred by proteolytic cleavage in beetle larvae. Insect Biochem. Mol. 28:229–37 [Google Scholar]
  40. Girard C, Le Metayer M, Zaccomer B, Bartlet E, Williams I. 40.  et al. 1998. Growth stimulation of beetle larvae reared on a transgenic oilseed rape expressing a cysteine proteinase inhibitor. J. Insect Physiol. 44:263–70 [Google Scholar]
  41. Giri AP, Harsulkar AM, Deshpande VV, Sainani MN, Gupta VS, Ranjekar PK. 41.  1998. Chickpea defensive proteinase inhibitors can be inactivated by podborer gut proteinases. Plant Physiol. 116:393–401 [Google Scholar]
  42. Green TR, Ryan CA. 42.  1972. Wound-induced proteinase inhibitor in plant leaves—possible defense mechanism against insects. Science 175:776–77 [Google Scholar]
  43. Gruden K, Kuipers AGJ, Guncar G, Slapar N, Strukelj B, Jongsma MA. 43.  2004. Molecular basis of Colorado potato beetle adaptation to potato plant defence at the level of digestive cysteine proteinases. Insect Biochem. Mol. Biol. 34:365–75 [Google Scholar]
  44. Gruden K, Popovic T, Cimerman N, Krizaj I, Strukelj B. 44.  2003. Diverse enzymatic specificities of digestive proteases, ‘intestains’, enable Colorado potato beetle larvae to counteract the potato defence mechanism. Biol. Chem. 384:305–10 [Google Scholar]
  45. Gunduz EA, Douglas AE. 45.  2009. Symbiotic bacteria enable insect to use a nutritionally inadequate diet. Proc. R. Soc. B 276:987–91 [Google Scholar]
  46. Guo F, Lei J, Sun Y, Chi YH, Ge F. 46.  et al. 2012. Antagonistic regulation, yet synergistic defense: effect of bergapten and protease inhibitor on development of cowpea bruchid Callosobruchus maculatus. PLOS ONE 7:e41877 [Google Scholar]
  47. Harsulkar AM, Giri AP, Patankar AG, Gupta VS, Sainani MN. 47.  et al. 1999. Successive use of non-host plant proteinase inhibitors required for effective inhibition of Helicoverpa armigera gut proteinases and larval growth. Plant Physiol. 121:497–506 [Google Scholar]
  48. Hegedus D, Baldwin D, O'Grady M, Braun L, Gleddie S. 48.  et al. 2003. Midgut proteases from Mamestra configurata (Lepidoptera: Noctuidae) larvae: characterization, cDNA cloning, and expressed sequence tag analysis. Arch. Insect Biochem. Physiol. 53:30–47 [Google Scholar]
  49. Hilder VA, Gatehouse AMR, Sheerman SE, Barker RF, Boulter D. 49.  1987. A novel mechanism of insect resistance engineered into tobacco. Nature 330:160–63 [Google Scholar]
  50. Houseman JG, Philogene BJR, Downe AER. 50.  1989. Partial characterization of proteinase activity in the larval midgut of the European corn-borer, Ostrinia nubilalis Hübner (Lepidoptera, Pyralidae). Can. J. Zool. 67:864–68 [Google Scholar]
  51. Illy C, Quraishi O, Wang J, Purisima E, Vernet T, Mort JS. 51.  1997. Role of the occluding loop in cathepsin B activity. J. Biol. Chem. 272:1197–202 [Google Scholar]
  52. 52. Int. Aphid Genomics Consort 2010. Genome sequence of the pea aphid Acyrthosiphon pisum. PLOS Biol. 8:e1000313 [Google Scholar]
  53. Johnston KA, Lee MJ, Brough G, Hilder VA, Gatehouse AMR, Gatehouse JA. 53.  1995. Protease activities in the larval midgut of Heliothis virescens—evidence for trypsin and chymotrypsin-like enzymes. Insect Biochem. Mol. Biol. 25:375–83 [Google Scholar]
  54. Johnston KA, Lee MJ, Gatehouse JA, Anstee JH. 54.  1991. The partial purification and characterisation of serine protease activity in midgut of larval Helicoverpa armigera. Insect Biochem. 21:389–97 [Google Scholar]
  55. Jongsma MA, Bakker PL, Peters J, Bosch D, Stiekema WJ. 55.  1995. Adaptation of Spodoptera exigua larvae to plant proteinase inhibitors by induction of gut proteinase activity insensitive to inhibition. Proc. Natl. Acad. Sci. USA 92:8041–45 [Google Scholar]
  56. Jongsma MA, Beekwilder J. 56.  2011. Co-Evolution of insect proteases and plant protease inhibitors. Curr. Protein Pept. Sci. 12:437–47 [Google Scholar]
  57. Keeling CI, Yuen MMS, Liao NY, Docking TR, Chan SK. 57.  et al. 2013. Draft genome of the mountain pine beetle, Dendroctonus ponderosae Hopkins, a major forest pest. Genome Biol. 14:R27 [Google Scholar]
  58. Kessler A, Baldwin IT. 58.  2002. Plant responses to insect herbivory: the emerging molecular analysis. Annu. Rev. Plant Biol. 53:299–328 [Google Scholar]
  59. Koiwa H, Bressan RA, Hasegawa PM. 59.  1997. Regulation of protease inhibitors and plant defense. Trends Plant Sci. 2:379–84 [Google Scholar]
  60. Koiwa H, Shade RE, Zhu-Salzman K, D'Urzo MP, Murdock LL. 60.  et al. 2000. A plant defensive cystatin (soyacystatin) targets cathepsin L-like digestive cysteine proteinases (DvCALs) in the larval midgut of western corn rootworm (Diabrotica virgifera virgifera). FEBS Lett. 471:67–70 [Google Scholar]
  61. Kolliopoulou A, Swevers L. 61.  2013. Functional analysis of the RNAi response in ovary-derived silkmoth Bm5 cells. Insect Biochem. Mol.Biol. 43:654–63 [Google Scholar]
  62. Koo YD, Ahn JE, Salzman RA, Moon J, Chi YH. 62.  et al. 2008. Functional expression of an insect cathepsin B-like counter-defence protein. Insect Mol. Biol. 17:235–45 [Google Scholar]
  63. Lawrence PK, Koundal KR. 63.  2002. Plant protease inhibitors in control of phytophagous insects. Electron. J. Biotechno. 5:93–109 [Google Scholar]
  64. Lehane MJ, Billingsley PF. 64.  Biology of the Insect Midgut London: Champan & Hall
  65. Leple JC, Bonadebottino M, Augustin S, Pilate G, Letan VD. 65.  et al. 1995. Toxicity to Chrysomela tremulae (Coleoptera: Chrysomelidae) of transgenic poplars expressing a cysteine proteinase inhibitor. Mol. Breed. 1:319–28 [Google Scholar]
  66. Liddle RA. 66.  1995. Regulation of cholecystokinin secretion by intraluminal releasing factors. Am. J. Physiol. Gastrointest. Liver Physiol. 269:G319–27 [Google Scholar]
  67. Liu YL, Salzman RA, Pankiw T, Zhu-Salzman K. 67.  2004. Transcriptional regulation in southern corn rootworm larvae challenged by soyacystatin N. Insect Biochem. Mol. Biol. 34:1069–77 [Google Scholar]
  68. Lopes AR, Juliano MA, Juliano L, Terra WR. 68.  2004. Coevolution of insect trypsins and inhibitors. Arch. Insect Biochem. Physiol. 55:140–52 [Google Scholar]
  69. Lopes AR, Juliano MA, Marana SR, Juliano L, Terra WR. 69.  2006. Substrate specificity of insect trypsins and the role of their subsites in catalysis. Insect Biochem. Mol. Biol. 36:130–40 [Google Scholar]
  70. Mao YB, Cai WJ, Wang JW, Hong GJ, Tao XY. 70.  et al. 2007. Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat. Biotechnol. 25:1307–13 [Google Scholar]
  71. Mazumdar-Leighton S, Broadway RM. 71.  2001. Identification of six chymotrypsin cDNAs from larval midguts of Helicoverpa zea and Agrotis ipsilon feeding on the soybean (Kunitz) trypsin inhibitor. Insect Biochem. Mol. Biol. 31:633–44 [Google Scholar]
  72. Mazumdar-Leighton S, Broadway RM. 72.  2001. Transcriptional induction of diverse midgut trypsins in larval Agrotis ipsilon and Helicoverpa zea feeding on the soybean trypsin inhibitor. Insect Biochem. Mol. Biol. 31:645–57 [Google Scholar]
  73. Michaud D, Cantin L, Vrain TC. 73.  1995. Carboxy-terminal truncation of oryzacysatin II by oryzacytatin-insensitive insect digestive proteinases. Arch. Biochem. Biophys. 322:469–74 [Google Scholar]
  74. Mlodzik M, Hiromi Y, Weber U, Goodman CS, Rubin GM. 74.  1990. The Drosophila seven-up gene, a member of the steroid-receptor gene superfamily, controls photoreceptor cell fates. Cell 60:211–24 [Google Scholar]
  75. Moon J, Salzman RA, Ahn JE, Koiwa H, Zhu-Salzman K. 75.  2004. Transcriptional regulation in cowpea bruchid guts during adaptation to a plant defence protease inhibitor. Insect Mol. Biol. 13:283–91 [Google Scholar]
  76. Morris K, Lorenzen MD, Hiromasa Y, Tomich JM, Oppert C. 76.  et al. 2009. Tribolium castaneum larval gut transcriptome and proteome: a resource for the study of the coleopteran gut. J. Proteome Res. 8:3889–98 [Google Scholar]
  77. Mosolov VV, Valueva TA. 77.  2008. Proteinase inhibitors in plant biotechnology: a review. Appl. Biochem. Microbiol. 44:233–40 [Google Scholar]
  78. Muhlia-Almazán A, Sánchez-Paz A, García-Carreño FL. 78.  2008. Invertebrate trypsins: a review. J. Comp. Physiol. B 178:655–72 [Google Scholar]
  79. Murdock LL, Brookhart G, Dunn PE, Foard DE, Kelley S. 79.  et al. 1987. Cysteine digestive proteinases in Coleoptera. Comp. Biochem. Phys. B 87:783–87 [Google Scholar]
  80. Musil D, Zucic D, Turk D, Engh RA, Mayr I. 80.  et al. 1991. The refined 2.15 Å X-ray crystal structure of human liver cathepsin B: the structural basis for its specificity. EMBO J. 10:2321–30 [Google Scholar]
  81. Nauen R, Sorge D, Sterner A, Borovsky D. 81.  2001. TMOF-like factor controls the biosynthesis of serine proteases in the larval gut of Heliothis virescens. Arch. Insect Biochem. Physiol. 47:169–80 [Google Scholar]
  82. Oppert B, Elpidina EN, Toutges M, Mazumdar-Leighton S. 82.  2010. Microarray analysis reveals strategies of Tribolium castaneum larvae to compensate for cysteine and serine protease inhibitors. Comp. Biochem. Phys. D 5:280–87 [Google Scholar]
  83. Oppert B, Morgan TD, Hartzer K, Kramer KJ. 83.  2005. Compensatory proteolytic responses to dietary proteinase inhibitors in the red flour beetle, Tribolium castaneum (Coleoptera: Tenebrionidae). Comp. Biochem. Phys. C 140:53–58 [Google Scholar]
  84. Orr GL, Strickland JA, Walsh TA. 84.  1994. Inhibition of Diabrotica larval growth by a multicystatin from potato tubers. J. Insect Physiol. 40:893–900 [Google Scholar]
  85. Outchkourov NS, de Kogel WJ, Wiegers GL, Abrahamson M, Jongsma MA. 85.  2004. Engineered multidomain cysteine protease inhibitors yield resistance against western flower thrips (Franklinielia occidentalis) in greenhouse trials. Plant Biotechnol. J. 2:449–58 [Google Scholar]
  86. Pauchet Y, Wilkinson P, van Munster M, Augustin S, Pauron D, Ffrench-Constant RH. 86.  2009. Pyrosequencing of the midgut transcriptome of the poplar leaf beetle Chrysomela tremulae reveals new gene families in Coleoptera. Insect Biochem. Mol. 39:403–13 [Google Scholar]
  87. Pauchet Y, Wilkinson P, Vogel H, Nelson DR, Reynolds SE. 87.  et al. 2010. Pyrosequencing the Manduca sexta larval midgut transcriptome: messages for digestion, detoxification and defence. Insect Mol. Biol. 19:61–75 [Google Scholar]
  88. Petek M, Turnsek N, Gasparic MB, Novak MP, Gruden K. 88.  et al. 2012. A complex of genes involved in adaptation of Leptinotarsa decemlineata larvae to induced potato defense. Arch. Insect Biochem. Physiol. 79:153–81 [Google Scholar]
  89. Pyati P, Bandani AR, Fitches E, Gatehouse JA. 89.  2011. Protein digestion in cereal aphids (Sitobion avenae) as a target for plant defence by endogenous proteinase inhibitors. J. Insect Physiol. 57:881–91 [Google Scholar]
  90. Rawlings ND, Tolle DP, Barrett AJ. 90.  2004. Evolutionary families of peptidase inhibitors. Biochem. J. 378:705–16 [Google Scholar]
  91. Ribeiro APO, Pereira EJG, Galvan TL, Picanco MC, Picoli EAT. 91.  et al. 2006. Effect of eggplant transformed with oryzacystatin gene on Myzus persicae and Macrosiphum euphorbiae. J. Appl. Entomol. 130:84–90 [Google Scholar]
  92. Richards S, Gibbs RA, Weinstock GM, Brown SJ, Denell R. 92.  et al. 2008. The genome of the model beetle and pest Tribolium castaneum. Nature 452:949–55 [Google Scholar]
  93. Rispe C, Kutsukake M, Doublet V, Hudaverdian S, Legeai F. 93.  et al. 2008. Large gene family expansion and variable selective pressures for cathepsin B in aphids. Mol. Biol. Evol. 25:5–17 [Google Scholar]
  94. Ryan CA. 94.  1990. Protease inhibitors in plants: genes for improving defenses against insects and pathogens. Annu. Rev. Phytopathol. 28:425–49 [Google Scholar]
  95. Schechter I, Berger A. 95.  1967. On the size of the active site in proteases. I. Papain. Biochem. Biophys. Res. Commun. 27:157–62 [Google Scholar]
  96. Schmelz EA, Carroll MJ, LeClere S, Phipps SM, Meredith J. 96.  et al. 2006. Fragments of ATP synthase mediate plant perception of insect attack. Proc. Natl. Acad. Sci. USA 103:8894–99 [Google Scholar]
  97. Shinde AA, Shaikh FK, Padul MV, Kachole MS. 97.  2012. Bacillus subtillis RTSBA6 6.00, a new strain isolated from gut of Helicoverpa armigera (Lepidoptera: Noctuidae) produces chymotrypsin-like proteases. Saudi J. Biol. Sci. 19:317–23 [Google Scholar]
  98. Siegfried BD, Waterfield N, Ffrench-Constant RH. 98.  2005. Expressed sequence tags from Diabrotica virgifera virgifera midgut identify a coleopteran cadherin and a diversity of cathepsins. Insect Mol. Biol. 14:137–43 [Google Scholar]
  99. Soares-Costa A, Dias AB, Dellamano M, de Paula FF, Carmona AK. 99.  et al. 2011. Digestive physiology and characterization of digestive cathepsin L-like proteinase from the sugarcane weevil Sphenophorus levis. J. Insect Physiol. 57:462–68 [Google Scholar]
  100. Spit J, Breugelmans B, van Hoef V, Simonet G, Zels S, Broeck JV. 100.  2012. Growth-inhibition effects of pacifastin-like peptides on a pest insect: the desert locust, Schistocerca gregaria. Peptides 34:251–57 [Google Scholar]
  101. Srinivasan A, Giri AP, Gupta VS. 101.  2006. Structural and functional diversities in lepidopteran serine proteases. Cell. Mol. Biol. Lett. 11:132–54 [Google Scholar]
  102. Srinivasan A, Giri AP, Harsulkar AM, Gatehouse JA, Gupta VS. 102.  2005. A Kunitz trypsin inhibitor from chickpea (Cicer arietinum L.) that exerts anti-metabolic effect on podborer (Helicoverpa armigera) larvae. Plant Mol. Biol. 57:359–74 [Google Scholar]
  103. Steppuhn A, Baldwin IT. 103.  2007. Resistance management in a native plant: Nicotine prevents herbivores from compensating for plant protease inhibitors. Ecol. Lett. 10:499–511 [Google Scholar]
  104. Swevers L, Huvenne H, Menschaert G, Kontogiannatos D, Kourti A. 104.  et al. 2013. Colorado potato beetle (Coleoptera) gut transcriptome analysis: expression of RNA interference-related genes. Insect Mol. Biol. 22:668–84 [Google Scholar]
  105. Tan A, Palli SR. 105.  2008. Identification and characterization of nuclear receptors from the red flour beetle, Tribolium castaneum. Insect Biochem. Mol. Biol. 38:430–39 [Google Scholar]
  106. Telang MA, Giri AP, Sainani MN, Gupta VS. 106.  2005. Characterization of two midgut proteinases of Helicoverpa armigera and their interaction with proteinase inhibitors. J. Insect Physiol. 51:513–22 [Google Scholar]
  107. Terenius O, Papanicolaou A, Garbutt JS, Eleftherianos I, Huvenne H. 107.  et al. 2011. RNA interference in Lepidoptera: an overview of successful and unsuccessful studies and implications for experimental design. J. Insect Physiol. 57:231–45 [Google Scholar]
  108. Terra WR, Ferreira C. 108.  1994. Insect digestive enzymes—properties, compartmentalization and function. Comp. Biochem. Phys. B 109:1–62 [Google Scholar]
  109. Terra WR, Ferreira C, Baker JE. 109.  1996. Compartmentalization of digestion. See Ref. 64, pp. 206–35
  110. Ussuf KK, Laxmi NH, Mitra R. 110.  2001. Proteinase inhibitors: plant-derived genes of insecticidal protein for developing insect-resistant transgenic plants. Curr. Sci. India 80:847–53 [Google Scholar]
  111. Visotto LE, Oliveira MG, Ribon AO, Mares-Guia TR, Guedes RN. 111.  2009. Characterization and identification of proteolytic bacteria from the gut of the velvetbean caterpillar (Lepidoptera: Noctuidae). Environ. Entomol. 38:1078–85 [Google Scholar]
  112. Volpicella M, Ceci LR, Cordewener J, America T, Gallerani R. 112.  et al. 2003. Properties of purified gut trypsin from Helicoverpa zea, adapted to proteinase inhibitors. Eur. J. Biochem. 270:10–19 [Google Scholar]
  113. Walsh TA, Strickland JA. 113.  1993. Proteolysis of the 85-kilodalton crystalline cysteine proteinase inhibitor from potato releases functional cystatin domains. Plant Physiol. 103:1227–34 [Google Scholar]
  114. Winterer J, Bergelson J. 114.  2001. Diamondback moth compensatory consumption of protease inhibitor-transformed plants. Mol. Ecol. 10:1069–74 [Google Scholar]
  115. Wolfson JL, Murdock LL. 115.  1987. Suppression of larval Colorado potato beetle growth and development by digestive proteinase inhibitors. Entomol. Exp. Appl. 44:235–40 [Google Scholar]
  116. Yang L, Fang Z, Dicke M, van Loon JJ, Jongsma MA. 116.  2009. The diamondback moth, Plutella xylostella, specifically inactivates Mustard Trypsin Inhibitor 2 (MTI2) to overcome host plant defence. Insect Biochem. Mol. Biol. 39:55–61 [Google Scholar]
  117. You MS, Yue Z, He WY, Yang XH, Yang G. 117.  et al. 2013. A heterozygous moth genome provides insights into herbivory and detoxification. Nat. Genet. 45:220–25 [Google Scholar]
  118. Zavala JA, Giri AP, Jongsma MA, Baldwin IT. 118.  2008. Digestive duet: midgut digestive proteinases of Manduca sexta ingesting Nicotiana attenuata with manipulated trypsin proteinase inhibitor expression. PLOS ONE 3:e2008 [Google Scholar]
  119. Zhang S, Shukle R, Mittapalli O, Zhu YC, Reese JC. 119.  et al. 2010. The gut transcriptome of a gall midge, Mayetiola destructor. J. Insect Physiol. 56:1198–206 [Google Scholar]
  120. Zhu F, Xu JJ, Palli R, Ferguson J, Palli SR. 120.  2011. Ingested RNA interference for managing the populations of the Colorado potato beetle, Leptinotarsa decemlineata. Pest Manag. Sci. 67:175–82 [Google Scholar]
  121. Zhu-Salzman K, Koiwa H, Salzman RA, Shade RE, Ahn JE. 121.  2003. Cowpea bruchid Callosobruchus maculatus uses a three-component strategy to overcome a plant defensive cysteine protease inhibitor. Insect Mol. Biol. 12:135–45 [Google Scholar]
  122. Zhu-Salzman K, Luthe DS, Felton GW. 122.  2008. Arthropod-inducible proteins: broad spectrum defenses against multiple herbivores. Plant Physiol. 146:852–58 [Google Scholar]
  123. Zhu-Salzman K, Zeng RS. 123.  2008. Molecular mechanisms of insect adaptation to plant defense: lessons learned from a Bruchid beetle. Insect Sci. 15:477–81 [Google Scholar]
/content/journals/10.1146/annurev-ento-010814-020816
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Insect Response to Plant Defensive Protease Inhibitors
Annual Review of Entomology 60, 233 (2015); https://doi.org/10.1146/annurev-ento-010814-020816
/content/journals/10.1146/annurev-ento-010814-020816
/content/journals/10.1146/annurev-ento-010814-020816
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