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Lepidopteran Peritrophic Matrix Composition, Function, and Formation

  • Dwayne D. Hegedus
  • Umut Toprak
  • Martin Erlandson
Chapter
Part of the Entomology in Focus book series (ENFO, volume 4)

Abstract

Lepidopteran larvae possess a robust digestive system featuring a multitude of hydrolytic enzymes that are able to accommodate an often highly polyphagous diet. Additional digestive complexity arises from the peritrophic matrix (PM) which encases the food bolus and compartmentalizes digestive processes. This review focuses on genomic and proteomic studies from several species that have identified what is likely to be the entire complement of proteins associated with the lepidopteran PM. In the process, a basal set of structural proteins common to the lepidopteran PM is described, and the roles of these proteins in PM structure and function are discussed. Finally, updated models for PM molecular architecture and formation which incorporate information about recently discovered proteins are provided.

Keywords

Food Bolus Midgut Epithelium Lepidopteran Larva Peritrophic Matrix Anterior Midgut 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

ALP

alkaline phosphatase

AMY

amylase

AST

astacin

CBD

chitin-binding domain

CDA

chitin deacetylase

CHI

endo-chitinase

CHS-2

chitin synthase 2

CLECT

C-type lectin

CBP

chitin-binding protein

Ek

Ephestia kuehniella

GlcNAc

N-acetylglucosamine

GPI

glycosylphosphatidylinositol

β1,3GLU

β-1,3-glucanase

Ha

Helicoverpa armigera

IIL

insect intestinal lipase

IIM

insect intestinal mucin

Lsti

Loxostege sticticalis

mRNA

messenger RNA

Mc

Mamestra configurata

MD

mucin domain

NAG

N-acetylglucosaminidase

On

Ostrinia nubilalis

PAD

peritrophin-A domain

PBD

peritrophin-B domain

PCD

peritrophin-C domain

PM

peritrophic matrix

REPAT

response to pathogen

RNA

ribonucleic acid

Se

Spodoptera exigua

Tn

Trichoplusia ni

References

  1. 1.
    Lyonet, P. (1762). Traité Anatomique de la Chenille. La Haye: Grosse Pinet.Google Scholar
  2. 2.
    Balbiani, E. G. (1890). Études anatomiques et histologiques sur le tube digestif des Crytops. Archives of Zoological Experimental Genome, 8, 1–82.Google Scholar
  3. 3.
    Peters, W. (1992). Peritrophic membranes. In D. Bradshaw, W. Burggren, H.C. Heller, S. Ishii, H. Langer, G. Neuweiler & D. J. Randall (Eds.), Zoophysiology (Vol. 130). Berlin: Springer.Google Scholar
  4. 4.
    Vignon, P. (1901). Recherches sur les épithéliums. Archives of Zoological Experimental Genome Series, 3(9), 371–715.Google Scholar
  5. 5.
    Wigglesworth, V. B. (1930). The formation of the peritrophic membrane in insects, with special reference to the larvae of mosquitoes. Quarterly. Journal of Microscopical Science, 73, 583–616.Google Scholar
  6. 6.
    Waterhouse, D. F. (1957). Digestion in insects. Annual Review of Entomology, 2, 1–18.CrossRefGoogle Scholar
  7. 7.
    Bolognesi, R., Terra, W. R., & Ferreira, C. (2008). Peritrophic membrane role in enhancing digestive efficiency: Theoretical and experimental models. Journal of Insect Physiology, 54, 1413–1422.CrossRefPubMedGoogle Scholar
  8. 8.
    Tellam, R. L. (1996). The peritrophic matrix. In M. J. Lehane & P. F. Billingsley (Eds.), Biology of the insect midgut (pp. 86–114). London: Chapman and Hall.CrossRefGoogle Scholar
  9. 9.
    Lehane, M. J. (1997). Peritrophic matrix structure and function. Annual Review of Entomology, 42, 525–550.CrossRefPubMedGoogle Scholar
  10. 10.
    Terra, W. R. (2001). The origin and functions of the insect peritrophic membrane and peritrophic gel. Archives of Insect Biochemistry and Physiology, 47, 47–61.CrossRefPubMedGoogle Scholar
  11. 11.
    Hegedus, D., Erlandson, M., Gillott, C., & Toprak, U. (2009). New insights into peritrophic matrix synthesis, architecture, and function. Annual Review of Entomology, 54, 285–302.CrossRefPubMedGoogle Scholar
  12. 12.
    Toprak, U., Erlandson, M., & Hegedus, D. D. (2010). Peritrophic matrix proteins. Trends in Entomology, 6, 23–51.Google Scholar
  13. 13.
    Elvin, C. M., Vuocolo, T., Pearson, R. D., East, I. J., Riding, G. A., Eisemann, C. H., & Tellam, R. L. (1996). Characterization of a major peritrophic membrane protein, Peritrophin-44, from the larvae of Lucilia cuprina. The Journal of Biological Chemistry, 271, 8925–8935.CrossRefPubMedGoogle Scholar
  14. 14.
    Wang, P., & Granados, R. R. (2001). Molecular structure of the peritrophic membrane (PM): Identification of potential PM target sites for insect control. Archives of Insect Biochemistry and Physiology, 47, 110–118.CrossRefPubMedGoogle Scholar
  15. 15.
    Toprak, U., Erlandson, M., & Hegedus, D. D. (2015) Identification of the Mamestra configurata (Lepidoptera:Noctuidae) peritrophic matrix proteins and enzymes involved in peritrophic matrix chitin metabolism. Insect Science, Epub ahead of print (doi:  10.1111/1744-7917.12225).
  16. 16.
    Mercer, E. H., & Day, M. F. (1952). The fine structure of the peritrophic membranes of certain insects. The Biological Bulletin, 103, 384–394.CrossRefGoogle Scholar
  17. 17.
    Toprak, U., Baldwin, D., Erlandson, M., Gillott, C., Hou, X., Coutu, C., & Hegedus, D. D. (2008). A chitin deacetylase and putative insect intestinal lipases are integral components of Mamestra configurata peritrophic matrix. Insect Molecular Biology, 17, 573–585.CrossRefPubMedGoogle Scholar
  18. 18.
    Cohen, E. (2010). Chitin biochemistry: Synthesis, hydrolysis and inhibition. Advances in Insect Physiology, 38, 5–74.CrossRefGoogle Scholar
  19. 19.
    Tellam, R. L., Wijffels, G., & Willadsen, P. (1999). Peritrophic matrix proteins. Insect Biochemistry and Molecular Biology, 29, 87–101.CrossRefPubMedGoogle Scholar
  20. 20.
    Lehane, M. J., Aksoy, S., Gibson, W., Kerhornou, A., Berriman, M., Hamilton, J., Soares, M. B., Bonaldo, M. F., Lehane, S., & Hall, N. (2003). Adult midgut expressed sequence tags from the tsetse fly Glossina morsitans morsitans and expression analysis of putative immune response genes. Genome Biology, 4, R63.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Shi, X., Chamankhah, M., Visal-Shah, S., Hemmingsen, S. M., Erlandson, M., Braun, L., Alting-Mees, M., Khachatourians, G. G., O’Grady, M., & Hegedus, D. D. (2004). Modeling the structure of the Type I peritrophic matrix: Characterization of a Mamestra configurata intestinal mucin and a novel peritrophin containing 19 chitin-binding domains. Insect Biochemistry and Molecular Biology, 34, 1101–1115.CrossRefPubMedGoogle Scholar
  22. 22.
    Simpson, R. M., Newcomb, R. D., Gatehouse, H. S., Crowhurst, R. N., Chagné, D., Gatehouse, L. N., Markwick, N. P., Beuning, L. L., Murray, C., Marshall, S. D., Yauk, Y.-K., Nain, B., Wang, Y.-Y., Gleave, A. P., & Christeller, J. T. (2007). Expressed sequence tags from the midgut of Epiphyas postvittana (Walker) (Lepidoptera: Tortricidae). Insect Molecular Biology, 16, 675–690.CrossRefPubMedGoogle Scholar
  23. 23.
    Ramalho-Ortigao, M., Jochim, R. C., Anderson, J. M., Lawyer, P. G., Pham, V.-M., Kamhawi, S., & Valenzuela, J. G. (2007). Exploring the midgut transcriptome of Phlebotomus papatasi: Comparative analysis of expression profiles of sugar-fed, blood-fed and Leishmania major-infected sandflies. BMC Genomics, 8, 300.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Jochim, R. C., Teixeira, C. R., Laughinghouse, A., Mu, J., Oliveira, F., Gomes, R. B., Elnaiem, D.-E., & Valenzuela, J. G. (2008). The midgut transcriptome of Lutzomyia longipalpis: Comparative analysis of cDNA libraries from sugar-fed, blood-fed, post-digested and Leishmania infantum chagasi-infected sand flies. BMC Genomics, 9, 15.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Morris, K., Lorenzen, M. D., Hiromasa, Y., Tomich, J. M., Oppert, C., Elpidina, E. N., Vinokurov, K., Jurat-Fuentes, J. L., Fabrick, J., & Oppert, B. (2009). Tribolium castaneum larval gut transcriptome and proteome: A resource for the study of the coleopteran gut. Journal of Proteome Research, 8, 3889–3898.CrossRefPubMedGoogle Scholar
  26. 26.
    Pauchet, Y., Wilkinson, P., van Munster, M., Augustin, S., Pauron, D., & ffrench-Constant, R. H. (2009). Pyrosequencing of the midgut transcriptome of the poplar leaf beetle Chrysomela tremulae reveals new gene families in Coleoptera. Insect Biochemistry and Molecular Biology, 39, 403–413.CrossRefPubMedGoogle Scholar
  27. 27.
    Venancio, T. M., Cristofoletti, P. T., Ferreira, C., Verjovski-Almeida, S., & Terra, W. R. (2009). The Aedes aegypti larval transcriptome: A comparative perspective with emphasis on trypsins and the domain structure of peritrophins. Insect Molecular Biology, 18, 33–44.CrossRefPubMedGoogle Scholar
  28. 28.
    Pauchet, Y., Wilkinson, P., Vogel, H., Nelson, D. R., Reynolds, S. E., Heckel, D. G., & French-Constant, R. H. (2010). Pyrosequencing the Manduca sexta larval midgut transcriptome: Messages for digestion, detoxification and defence. Insect Molecular Biology, 19, 61–75.CrossRefPubMedGoogle Scholar
  29. 29.
    Ferreira, A. H. P., Cristofoletti, P. T., Lorenzinic, D. M., Guerra, L. O., Paiva, P. B., Briones, M. R. S., Terra, W. R., & Ferreira, C. (2007). Identification of midgut microvillar proteins from Tenebrio molitor and Spodoptera frugiperda by cDNA library screenings with antibodies. Journal of Insect Physiology, 53, 1112–1124.CrossRefPubMedGoogle Scholar
  30. 30.
    Campbell, P. M., Cao, A. T., Hines, E. R., East, P. D., & Gordon, K. H. J. (2008). Proteomic analysis of the peritrophic matrix from the gut of the caterpillar, Helicoverpa armigera. Insect Biochemistry and Molecular Biology, 38, 950–958.CrossRefPubMedGoogle Scholar
  31. 31.
    Pauchet, Y., Muck, A., Svatos, A., Heckel, D. G., & Preiss, S. (2008). Mapping the larval midgut lumen proteome of Helicoverpa armigera, a generalist herbivorous insect. Journal of Proteome Research, 7, 1629–1639.CrossRefPubMedGoogle Scholar
  32. 32.
    Dinglasan, R. R., Devenport, M., Florens, L., Johnson, J. R., McHugh, C. A., Donnelly-Doman, M., Carucci, D. J., Yates, J. R. I. I. I., & Jacobs-Lorena, M. (2009). The Anopheles gambiae adult midgut peritrophic matrix proteome. Insect Biochemistry and Molecular Biology, 39, 125–134.CrossRefPubMedGoogle Scholar
  33. 33.
    Liu, J., Zheng, S., Liu, L., & Feng, Q. (2010). Protein profiles of the midgut of Spodoptera litura larvae at the sixth instar feeding stage by shotgun ESI-MS approach. Journal of Proteome Research, 9, 2117–2147.CrossRefPubMedGoogle Scholar
  34. 34.
    Hu, X., Chen, L., Xiang, X., Yang, R., Yu, S., & Wu, X. (2012). Proteomic analysis of peritrophic membrane (PM) from the midgut of fifth-instar larvae, Bombyx mori. Molecular Biology Reports, 39, 3427–3434.CrossRefPubMedGoogle Scholar
  35. 35.
    Zhong, X., Zhang, L., Zou, Y., Yi, Q., & Zhao, P. (2012). Shotgun analysis on the peritrophic membrane of the silkworm Bombyx mori. BMB Reports, 45, 665–670.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Rose, C., Belmonte, R., Armstrong, S. D., Molyneux, G., Haines, L. R., Lehane, M. J., Wastling, J., & Acosta-Serrano, A. (2014). An investigation into the protein composition of the teneral Glossina morsitans morsitans peritrophic matrix. PLoS Neglected Tropical Diseases, 8, e2691.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Wang, P., & Granados, R. R. (1997). Molecular cloning and sequencing of a novel invertebrate intestinal mucin cDNA. The Journal of Biological Chemistry, 272, 16663–16669.CrossRefPubMedGoogle Scholar
  38. 38.
    Wang, P., & Granados, R. R. (1997). An intestinal mucin is the target substrate for a baculovirus enhancin. Proceedings of the National Academy of Sciences of the United States of America, 94, 6977–6982.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Tetreau, G., Dittmer, N. T, Cao, X., Agrawal, S., Chen, Y., Muthukrishnan, S., Haobo, J., Blissard, G. W., Kanost, M. R., & Wang, P. (2015). Analysis of chitin-binding proteins from Manduca sexta provides new insights into evolution of peritrophin A-type chitin-binding domains in insects. Insect Biochemistry and Molecular Biology. doi:  10.1016/j.ibmb.2014.12.002. [Epub ahead of print]
  40. 40.
    Toprak, U., Baldwin, D., Erlandson, M., Gillott, C., Harris, S., & Hegedus, D. D. (2010). Expression patterns of genes encoding proteins with peritrophin A domains and protein localization in Mamestra configurata. Journal of Insect Physiology, 56, 1711–1720.CrossRefPubMedGoogle Scholar
  41. 41.
    Wijffels, G., Eisemann, C., Riding, G., Pearson, R., Jones, A., Willadsen, P., & Tellam, R. (2001). A novel family of chitin-binding proteins from insect type 2 peritrophic matrix: cDNA sequences, chitin binding activity, and cellular localization. The Journal of Biological Chemistry, 276, 15527–15536.CrossRefPubMedGoogle Scholar
  42. 42.
    Weiss, B. L., Savage, A. F., Griffith, B. C., Wu, Y., & Aksoy, S. (2014). The peritrophic matrix mediates differential infection outcomes in the tsetse fly gut following challenge with commensal, pathogenic, and parasitic microbes. The Journal of Immunology, 193, 773–782.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Toprak, U., Harris, S., Baldwin, D., Theilmann, D., Gillott, C., Hegedus, D. D., & Erlandson, M. (2012). Role of enhancin in Mamestra configurata nucleopolyhedrovirus virulence: Selective degradation of host peritrophic matrix proteins. The Journal of General Virology, 93, 744–753.CrossRefPubMedGoogle Scholar
  44. 44.
    Toprak, U., Baldwin, D., Erlandson, M., Gillott, C., & Hegedus, D. D. (2010). Insect intestinal mucins and serine proteases associated with the peritrophic matrix from feeding, starved and molting Mamestra configurata larvae. Insect Molecular Biology, 19, 163–175.CrossRefPubMedGoogle Scholar
  45. 45.
    Sarauer, B. L., Gillott, C., & Hegedus, D. D. (2003). Characterization of an intestinal mucin from the peritrophic matrix of the diamondback moth, Plutella xylostella. Insect Molecular Biology, 12, 333–343.CrossRefPubMedGoogle Scholar
  46. 46.
    Zhang, X., & Guo, W. (2011). Isolation and identification of insect intestinal mucin Haiim86 – The new target for Helicoverpa armigera biocontrol. International Journal of Biology, 7, 286–296.CrossRefGoogle Scholar
  47. 47.
    Perez-Vilar, J., & Hill, R. L. (1999). The structure and assembly of secreted mucins. The Journal of Biological Chemistry, 274, 31751–31754.CrossRefPubMedGoogle Scholar
  48. 48.
    Harper, M. S., & Granados, R. R. (1999). Peritrophic membrane structure and formation of larval Trichoplusia ni with an investigation on the secretion patterns of a PM mucin. Tissue and Cell, 31, 202–211.CrossRefPubMedGoogle Scholar
  49. 49.
    Devine, P. L., & McKenzie, F. C. (1992). Mucins: Structure, function, and associations with malignancy. BioEssays, 14, 619–625.CrossRefPubMedGoogle Scholar
  50. 50.
    Van den Steen, P., Rudd, P. M., Dwek, R. A., & Opdenakker, G. (1998). Concepts and principles of O-linked glycosylation. Critical Reviews in Biochemistry and Molecular Biology, 33, 151–208.CrossRefPubMedGoogle Scholar
  51. 51.
    Van Klinken, B. J.-W., Dekker, J., Buller, H. A., & Einerhand, A. W. C. (1995). Mucin gene structure and expression: Protection vs. adhesion. The American Journal of Physiology, 269G, 613–627.Google Scholar
  52. 52.
    Agrawal, S., Kelkenberg, M., Begum, K., Steinfeld, L., Williams, C. E., Kramer, K. J., Beeman, R. W., Park, Y., Muthukrishnan, S., & Merzendorfer, H. (2014). Two essential peritrophic matrix proteins mediate matrix barrier functions in the insect midgut. Insect Biochemistry and Molecular Biology, 49, 24–34.CrossRefPubMedGoogle Scholar
  53. 53.
    Kuraishi, T., Binggeli, O., Opota, O., Buchon, N., & Lemaitre, B. (2011). Genetic evidence for a protective role of the peritrophic matrix against bacterial infection in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America, 20, 15966–15971.CrossRefGoogle Scholar
  54. 54.
    Wang, P., & Granados, R. R. (2000). Calcofluor disrupts the midgut defense systems in insects. Insect Biochemistry and Molecular Biology, 30, 135–143.CrossRefPubMedGoogle Scholar
  55. 55.
    Levy, S. M., Falleiros, A. M., Moscardi, F., & Gregorio, E. A. (2011). The role of peritrophic membrane in the resistance of Anticarsia gemmatalis larvae (Lepidoptera: Noctuidae) during the infection by its nucleopolyhedrovirus (AgMNPV). Arthropod Structures, 40, 429–434.CrossRefGoogle Scholar
  56. 56.
    Li, Q., Li, L., Moore, K., Donly, C., Theilmann, D. A., & Erlandson, M. (2003). Characterization of Mamestra configurata nucleopolyhedrovirus enhancin and its functional analysis via expression in an Autographa californica M nucleopolyhedrovirus recombinant. The Journal of General Virology, 84123–132.Google Scholar
  57. 57.
    Hoover, K., Humphries, M. A., Gendron, A. R., & Slavicek, J. M. (2010). Impact of viral enhancin genes on potency of Lymantria dispar multiple nucleopolyhedrovirus in L. dispar following disruption of the peritrophic matrix. Journal of Invertbrate Pathology, 104, 150–152.CrossRefGoogle Scholar
  58. 58.
    Fang, S., Wang, L., Guo, W., Zhang, X., Peng, D., Luo, C., Yu, Z., & Sun, M. (2009). Bacillus thuringiensis Bel protein enhances the toxicity of Cry1Ac protein to Helicoverpa armigera larvae by degrading insect intestinal mucin. Applied and Environmental Microbiology, 75, 5237–5243.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Sudha, P. M., & Muthu, S. P. (1988). Damage to the midgut epithelium caused by food in the absence of peritrophic membrane. Current Science, 57, 624–625.Google Scholar
  60. 60.
    Hegedus, D. D., Baldwin, D., O’Grady, M., Braun, L., Gleddie, S., Sharpe, A., Lydiate, D., & Erlandson, M. (2003). Midgut proteases from Mamestra configurata (Lepidoptera: Noctuidae) larvae: Characterization, cDNA cloning and expressed sequence tag analysis. Archives of Insect Biochemistry and Physiology, 53, 30–47.CrossRefPubMedGoogle Scholar
  61. 61.
    Erlandson, M. A., Hegedus, D. D., Baldwin, D., & Toprak, U. (2010). Characterization of the Mamestra configurata (Lepidoptera: Noctuidae) larval midgut protease complement and adaptation to feeding on artificial diet, Brassica species and protease inhibitor. Archives of Insect Biochemistry, 75, 70–91.CrossRefGoogle Scholar
  62. 62.
    Wang, P., Li, G., & Granados, R. R. (2004). Identification of two new peritrophic membrane proteins from larval Trichoplusia ni: Structural characteristics and their functions in the protease rich insect gut. Insect Biochemistry and Molecular Biology, 34, 215–227.CrossRefPubMedGoogle Scholar
  63. 63.
    Devenport, M., Alvarenga, P. H., Shao, L., Fujioka, H., Bianconi, M. L., Oliveira, P. L., & Jacobs-Lorena, M. (2006). Identification of the Aedes aegypti peritrophic matrix protein AeIMUCI as a heme-binding protein. Biochemistry, 45, 9540–9549.CrossRefPubMedGoogle Scholar
  64. 64.
    Chen, W.-J., Huang, L.-X., Hu, D., Liu, L.-Y., Gu, J., Huang, L.-H., & Feng, Q.-L. (2014). Cloning, expression and chitin-binding activity of two peritrophin-like protein genes in the common cutworm, Spodoptera litura. Insect Science, 21, 449–448.CrossRefPubMedGoogle Scholar
  65. 65.
    Ferreira, C., & Terra, W. R. (1989). Spatial organization of digestion, secretory mechanisms and digestive enzyme properties in Pheropsophus aequinoctialis (Coleoptera: Carabidae). Insect Biochemistry, 19, 383–391.CrossRefGoogle Scholar
  66. 66.
    Jordão, B. P., Capella, A. N., Terra, W. R., Ribeiro, A. F., & Ferreira, C. (1999). Nature of the anchors of membrane-bound aminopeptidase, amylase, and trypsin and secretory mechanisms in Spodoptera frugiperda (Lepidoptera) midgut cells. Journal of Insect Physiology, 45, 29–37.CrossRefPubMedGoogle Scholar
  67. 67.
    Jordão, B. P., & Terra, W. R. (1991). Regional distribution and substrate specificity of digestive enzymes involved in terminal digestion in Musca domestica hind-midguts. Archives of Insect Biochemistry and Physiology, 17, 157–168.CrossRefPubMedGoogle Scholar
  68. 68.
    Santos, C. D., & Terra, W. R. (1986). Distribution and characterization of oligomeric digestive enzymes from Erinnyis Ello larvae and inferences concerning secretory mechanisms and the permeability of the peritrophic membrane. Insect Biochemistry, 16, 691–700.CrossRefGoogle Scholar
  69. 69.
    Takesue, Y., Yokota, K., Miyajima, S., Taguchi, R., & Ikezawa, H. (1989). Membrane anchors of alkaline phosphatase and trehalase associated with the plasma membrane of larval midgut epithelial cells of the silkworm, Bombyx mori. Journal of Biochemistry, 105, 998–1001.CrossRefPubMedGoogle Scholar
  70. 70.
    Guo, W., Li, G., Pang, Y., & Wang, P. (2005). A novel chitin-binding protein identified from the peritrophic membrane of the cabbage looper, Trichoplusia ni. Insect Biochemistry and Molecular Biology, 35, 1224–1234.CrossRefPubMedGoogle Scholar
  71. 71.
    Yang, H.-J., Zhou, F., Malik, F. A., Bhaskar, R., Li, X.-H., Hu, J.-B., Sun, C.-B., & Miao, Y.-G. (2010). Identification and characterization of two chitin-binding proteins from the peritrophic membrane of the silkworm, Bombyx mori. Archives of Insect Biochemistry and Physiology, 75, 221–230.CrossRefPubMedGoogle Scholar
  72. 72.
    Zhong, X.-W., Wang, X.-H., Tan, A., Xia, Q.-Y., Xiang, Z.-H., & Zhao, P. (2014). Identification and molecular characterization of a chitin deacetylase from Bombyx mori peritrophic membrane. International Journal of Molecular Sciences, 15, 1946–1961.CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Jakubowska, A. K., Caccia, S., Gordon, K. H., Ferré, J., & Herrero, S. (2010). Downregulation of a chitin deacetylase-like protein in response to baculovirus infection and its application for improving baculovirus infectivity. Journal of Virology, 84, 2546–2555.CrossRefGoogle Scholar
  74. 74.
    Cho, Y. W., Jang, J., Park, C. R., & Ko, S. W. (2000). Preparation and solubility in acid and water of partially deacetylated chitins. Biomacromolecules, 1, 609–614.CrossRefPubMedGoogle Scholar
  75. 75.
    Wenling, C., Duohui, J., Jiamou, L., Yandao, G., Nanming, Z., & Xiufang, Z. (2005). Effects of the degree of deacetylation on the physicochemical properties and Schwann cell affinity of chitosan films. Journal of Biomaterials Applications, 20, 157–177.CrossRefPubMedGoogle Scholar
  76. 76.
    Tellam, R. L., & Eisemann, C. (2000). Chitin is only a minor component of the peritrophic matrix from larvae of Lucilia cuprina. Insect Biochemistry and Molecular Biology, 30, 1189–1201.CrossRefPubMedGoogle Scholar
  77. 77.
    Zheng, Y. P., Retnakaran, A., Krell, P. J., Arif, B. M., Primavera, M., & Feng, Q. L. (2003). Temporal, spatial and induced expression of chitinase in the spruce budworm, Choristoneura fumiferana. Journal of Insect Physiology, 49, 241–247.CrossRefPubMedGoogle Scholar
  78. 78.
    Toprak, U., Hegedus, D. D., Baldwin, D., Coutu, C., & Erlandson, M. (2014). Spatial and temporal synthesis of Mamestra configurata peritrophic matrix through a larval stadium. Insect Molecular Biology and Biochemistry, 54, 89–97.CrossRefGoogle Scholar
  79. 79.
    Ahmad, T., Rajagopal, R., & Bhatnagar, K. (2003). Molecular characterization of chitinase from polyphagous pest Helicoverpa armigera. Biochemical and Biophysical Research Communications, 310, 188–195.CrossRefPubMedGoogle Scholar
  80. 80.
    Girard, C., & Jouanin, L. (1999). Molecular cloning of a gut-specific chitinase cDNA from the beetle Phaedon cochleariae. Insect Biochemistry and Molecular Biology, 29, 549–556.CrossRefPubMedGoogle Scholar
  81. 81.
    Zhu, Q., Arakane, Y., Beeman, R. W., Kramer, K. J., & Muthukrishnan, S. (2008). Functional specialization among insect chitinase family genes revealed by RNA interference. Proceedings of the National Academy of Sciences of the United States of America, 105, 6650–6655.CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Shen, Z., & Jacobs-Lorena, M. (1997). Characterization of a novel gut specific chitinase gene from the human malaria vector, Anopheles gambiae. The Journal of Biological Chemistry, 272, 28895–28900.CrossRefPubMedGoogle Scholar
  83. 83.
    Filho, B. P. D., Lemos, F. J. A., Secundino, N. F. C., Pascoa, V., Pereira, S. T., & Pimenta, P. F. P. (2002). Presence of chitinase and beta-N-acetylglucosaminidase in the Aedes aegypti: A chitinolytic system involving peritrophic matrix formation and degradation. Insect Biochemistry and Molecular Biology, 32, 1723–1729.CrossRefPubMedGoogle Scholar
  84. 84.
    Ramalho-Ortigao, J. M., & Traub-Cseko, Y. M. (2003). Molecular characterization of Llchit1, a midgut chitinase cDNA from the leishmaniasis vector Lutzomyia longipalpis. Insect Biochemistry and Molecular Biology, 33, 279–287.CrossRefPubMedGoogle Scholar
  85. 85.
    Khajuria, C., Buschman, L. L., Chen, M. S., Muthukrishnan, S., & Zhu, K. Y. (2010). A gut-specific chitinase gene essential for regulation of chitin content of peritrophic matrix and growth of Ostrinia nubilalis larvae. Insect Biochemistry and Molecular Biology, 40, 621–629.CrossRefPubMedGoogle Scholar
  86. 86.
    Christeller, J. T., Laing, W. A., Markwick, N. P., & Burgess, E. P. J. (1992). Midgut protease activities in 12 phytophagous Lepidopteran larvae: Dietary and protease inhibitor interactions. Insect Biochemistry and Molecular Biology, 22, 735–746.CrossRefGoogle Scholar
  87. 87.
    Eguchi, M., Iwamoto, A., & Yamauchi, K. (1982). Interrelation of proteases from the midgut lumen, epithelia and peritrophic membrane of the silkworm, Bombyx mori L. Comparative Biochemistry and Physiology A, 72, 359–363.CrossRefGoogle Scholar
  88. 88.
    Terra, W. R., & Ferreira, C. (1994). Insect digestive enzymes: Properties, compartmentalization and function. Comparative Biochemistry and Physiology. B, 109, 1–62.CrossRefGoogle Scholar
  89. 89.
    Ferreira, C., Capella, A. N., Sitnik, R., & Terra, W. R. (1994). Digestive enzymes in midgut cells, endo- and ectoperitrophic contents, and peritrophic membranes of Spodoptera frugiperda (lepidoptera) larvae. Archives of Insect Biochemistry and Physiology, 26, 299–313.CrossRefGoogle Scholar
  90. 90.
    Bolognesi, R., Ribeiro, A. F., Terra, W. R., & Ferreira, C. (2001). The peritrophic membrane of Spodoptera frugiperda: Secretion of peritrophins and role in immobilization and recycling digestive enzymes. Archives of Insect Biochemistry and Physiology, 47, 62–75.CrossRefPubMedGoogle Scholar
  91. 91.
    Möhrlen, F., Maniura, M., Plickert, G., Frohme, M., & Frank, U. (2006). Evolution of astacin-like metalloproteases in animals and their function in development. Evolution and Development, 8, 223–231.CrossRefPubMedGoogle Scholar
  92. 92.
    Yan, J., Cheng, Q., Li, C. B., & Aksoy, S. (2002). Molecular characterization of three gut genes from Glossina morsitans morsitans: Cathepsin B, zinc-metalloprotease and zinc-carboxypeptidase. Insect Molecular Biology, 11, 57–65.CrossRefPubMedGoogle Scholar
  93. 93.
    Wagner, W., Krieger, L., & Schnetter, W. (2000). Why is the scarab specific Bacillus thuringiensis ssp japonensis strain Buibui inefficient against Melolontha spp. In S. Keller (Ed.), Integrated control of soil pest subgroup “Melolontha”. Conference Proceedings IOBC/WPRS 23, 55–60.Google Scholar
  94. 94.
    Billingsley, P. F., & Downe, A. E. R. (1985). Cellular localisation of aminopeptidase in the midgut of Rhodnius prolixus Stål (Hemiptera: Reduviidae) during blood digestion. Cell and Tissue Research, 241, 421–428.CrossRefGoogle Scholar
  95. 95.
    Crava, C. M., Bel, Y., Lee, S. F., Manachini, B., Heckel, D. G., & Escriche, B. (2010). Study of the aminopeptidase N gene family in the lepidopterans Ostrinia nubilalis (Hübner) and Bombyx mori (L.): Sequences, mapping and expression. Insect Biochemistry and Molecular Biology, 40, 506–515.CrossRefPubMedGoogle Scholar
  96. 96.
    Garczynski, S. F., & Adang, M. J. (1995). Bacillus thuringiensis CryIA(c) δ-endotoxin binding aminopeptidase in the Manduca sexta midgut has a glycosyl-phosphatidylinositol anchor. Insect Biochemistry and Molecular Biology, 25, 409–415.CrossRefGoogle Scholar
  97. 97.
    Takesue, S., Yokota, K., Miyajima, S., Taguchi, R., Ikezawa, H., & Takesue, Y. (1992). Partial release of aminopeptidase N from larval midgut cell membranes of the silkworm, Bombyx mori, by phosphatidylinositol-specific phospholipase C. Comparative Biochemistry and Physiology - Part B, 102, 7–11.CrossRefGoogle Scholar
  98. 98.
    Rees, J. S., Jarrett, P., & Ellar, D. J. (2009). Peritrophic membrane contribution to Bt Cry delta-endotoxin susceptibility in Lepidoptera and the effect of calcofluor. Journal of Invertebrate Pathology, 100, 139–146.CrossRefPubMedGoogle Scholar
  99. 99.
    Arreguin-Espinosa, R., Arreguin, B., & Gonzales, C. (2000). Purification and properties of a lipase from Cephaloleia presignis (Coleoptera, Chrysomelidae). Biotechnology and Applied Biochemistry, 31, 239–244.CrossRefPubMedGoogle Scholar
  100. 100.
    Rebers, J. E., & Riddiford, L. M. (1988). Structure and expression of a Manduca sexta larval cuticle gene homologous to Drosophila cuticle genes. Journal of Molecular Biology, 203, 411–23.CrossRefPubMedGoogle Scholar
  101. 101.
    Bragatto, I., Genta, F. A., Ribeiro, A. F., Terra, W. R., & Ferreira, C. (2010). Characterization of a β-1, 3-glucanase active in the alkaline midgut of Spodoptera frugiperda larvae and its relation to β-glucan-binding proteins. Insect Biochemistry and Molecular Biology, 40, 861–872.CrossRefPubMedGoogle Scholar
  102. 102.
    Genta, F. A., Blanes, L., Cristofoletti, P. T., do Lago, C. L., Terra, W. R., & Ferreira, C. (2006). Purification, characterization and molecular cloning of the major chitinase from Tenebrio molitor larval midgut. Insect Biochemistry and Molecular Biology, 36, 789–800.CrossRefPubMedGoogle Scholar
  103. 103.
    Pytelkova, J., Hubert, J., Lepsik, M., Sobotnik, J., Sindelka, R., Krizková, I., Horn, M., & Mares, M. (2009). Digestive alpha-amylases of the flour moth Ephestia kuehniella – adaptation to alkaline environment and plant inhibitors. The FEBS Journal, 276, 3531–3546.CrossRefPubMedGoogle Scholar
  104. 104.
    Yoshitake, N., Eguchi, M., & Akiyama, A. (1966). Genetic control on the alkaline phosphatase of the midgut in the silkworm. Journal of Sericultural Science of Japan, 35, 1–6.Google Scholar
  105. 105.
    Okada, N., Azuma, M., & Eguchi, M. (1989). Alkaline phosphatase isozymes in the midgut of silkworm: Purification of high pH-stable microvillus and labile cytosolic enzymes. Journal of Comparative Physiology B, 159, 123–130.CrossRefGoogle Scholar
  106. 106.
    Perera, O. P., Willis, J. D., Adang, M. J., & Jurat-Fuentes, J. L. (2009). Cloning and characterization of the Cry1Ac-binding alkaline phosphatase (HvALP) from Heliothis virescens. Insect Biochemistry and Molecular Biology, 39, 294–302.CrossRefPubMedGoogle Scholar
  107. 107.
    Ning, C., Wu, K., Liu, C., Gao, Y., Jurat-Fuentes, J. L., & Gao, X. (2010). Characterization of a Cry1Ac toxin-binding alkaline phosphatase in the midgut from Helicoverpa armigera (Hübner) larvae. Journal of Insect Physiology, 56, 666–672.CrossRefPubMedGoogle Scholar
  108. 108.
    Kayser, H. (2005). Lipocalins and structurally related ligand-binding proteins. In L.I. Gilbert, K. Iatrou & S. Gill (Eds.), Comprehensive molecular insect science (Vol. 4). Oxford: Elsevier.Google Scholar
  109. 109.
    Pandian, G. N., Ishikawa, T., Togashi, M., Shitomi, Y., Haginoya, K., Yamamoto, S., Nishiumi, T., & Hori, H. (2008). Bombyx mori midgut membrane protein P252, which binds to Bacillus thuringiensis Cry1A, is a chlorophyllide-binding protein, and the resulting complex has antimicrobial activity. Applied and Environmental Microbiology, 74, 1324–1331.CrossRefPubMedPubMedCentralGoogle Scholar
  110. 110.
    Mauchamp, B., Royer, C., Garel, A., Jalabert, A., Da Rocha, M., Grenier, A. M., Labas, V., Mita, K., Kadono, K., & Chavancy, G. (2006). Polycalin (chlorophyllid A binding protein): A novel, very large fluorescent lipocalin from the midgut of the domestic silkworm Bombyx mori L. Insect Biochemistry and Molecular Biology, 36, 623–633.CrossRefPubMedGoogle Scholar
  111. 111.
    Angelucci, C., Barrett-Wilt, G. A., Hunt, D. F., Akhurst, R. J., East, P. D., Gordon, K. H. J., & Campbell, P. M. (2008). Diversity of aminopeptidases, derived from four lepidopteran gene duplications, and polycalins expressed in the midgut of Helicoverpa armigera: Identification of proteins binding the δ-endotoxin, Cry1Ac of Bacillus thuringiensis. Insect Biochemistry and Molecular Biology, 38, 685–696.CrossRefPubMedPubMedCentralGoogle Scholar
  112. 112.
    Barbehenn, R. V. (2001). Roles of peritrophic membranes in protecting herbivorous insects from ingested plant allelochemicals. Archives of Insect Biochemistry and Physiology, 47, 86–99.CrossRefPubMedGoogle Scholar
  113. 113.
    Jiang, H., Wang, Y., Huang, Y., Mulnix, A., Kadel, J., Cole, K., & Kanost, M. (1996). Organization of Serpin Gene-1 from Manduca sexta: Evolution of a family of alternate exons encoding the reactive site loop. The Journal of Biological Chemistry, 271, 28017–28023.CrossRefPubMedGoogle Scholar
  114. 114.
    Molnar, K., Holderith Borhegyi, N., Csikos, G., & Sass, M. (2001). Distribution of serpins in the tissues of the tobacco hornworm (Manduca sexta) larvae: Existence of new serpins possibly encoded by a gene distinct from the serpin-1 gene. Journal of Insect Physiology, 47, 675–687.CrossRefPubMedGoogle Scholar
  115. 115.
    Hegedus, D. D., Erlandson, M., Baldwin, D., Hou, X., & Chamankhah, M. (2008). Differential expansion and evolution of the exon family encoding the Serpin-1 reactive centre loop has resulted in divergent serpin repertoires among the Lepidoptera. Gene, 418, 15–21.CrossRefPubMedGoogle Scholar
  116. 116.
    Chamankhah, M., Braun, L., Visal-Shah, S., O’Grady, M., Baldwin, D., Shi, X., Hemmingsen, S. M., Alting-Mees, M., & Hegedus, D. D. (2003). Mamestra configurata Serpin-1 homologues: Implications for a regulatory role for serpins in molting. Insect Biochemistry and Molecular Biology, 33, 355–369.CrossRefPubMedGoogle Scholar
  117. 117.
    Peters, W., Kolb, H., & Kolb-Bachofen, V. (1983). Evidence for a sugar receptor (lectin) in the peritrophic membrane of the blowfly larva, Calliphora erythrocephala Mg. (Diptera). Journal of Insect Physiology, 29, 275–280.CrossRefGoogle Scholar
  118. 118.
    Chai, L. Q., Tian, Y. Y., Yang, D. T., Wang, J. X., & Zhao, X. F. (2008). Molecular cloning and characterization of a C-type lectin from the cotton bollworm, Helicoverpa armigera. Developmental and Comparative Immunology, 32, 71–83.CrossRefPubMedGoogle Scholar
  119. 119.
    Takase, H., Watanabe, A., Yoshizawa, Y., Kitami, M., & Ryoichi, S. (2009). Identification and comparative analysis of three novel C-type lectins from the silkworm with functional implications in pathogen recognition. Developmental and Comparative Immunology, 33, 789–800.CrossRefPubMedGoogle Scholar
  120. 120.
    Yu, X. Q., & Kanost, M. R. (2000). Immulectin-2, a lipopolysaccharide-specific lectin from an insect, Manduca sexta, is induced in response to gram-negative bacteria. The Journal of Biological Chemistry, 275, 37373–37381.CrossRefPubMedGoogle Scholar
  121. 121.
    Lehane, M. J1., & Msangi, A. R. (1991). Lectin and peritrophic membrane development in the gut of Glossina m. morsitans and a discussion of their role in protecting the fly against trypanosome infection. Medical and Veterinary Entomology, 5, 495–501.CrossRefPubMedGoogle Scholar
  122. 122.
    Herrero, S., Ansems, M., Van Oers, M. M., Vlak, J. V., Bakker, P. L., & de Maagd, R. A. (2007). REPAT, a new family of proteins induced by bacterial toxins and baculovirus infection in Spodoptera exigua. Insect Biochemistry and Molecular Biology, 37, 1109–1118.CrossRefPubMedGoogle Scholar
  123. 123.
    Dong, D.-J., He, H.-J., Chai, L.-Q., Wang, J.-X., & Zhao, X.-F. (2007). Identification of differentially expressed genes during larval molting and metamorphosis of Helicoverpa armigera. BMC Developmental Biology, 7, 73.CrossRefPubMedPubMedCentralGoogle Scholar
  124. 124.
    Wang, J.-L., Jiang, X.-J., Wang, Q., Hou, L.-J., Xu, D.-W., Wang, J.-X., & Zhao, X.-F. (2007). Identification and expression profile of a putative basement membrane protein gene in the midgut of Helicoverpa armigera. BMC Developmental Biology, 7, 76.CrossRefPubMedPubMedCentralGoogle Scholar
  125. 125.
    Yin, J., Wei, Z.-J., Li, K.-B., Cao, Y.-Z., & Guo, W. (2010). Identification and molecular characterization of a new member of the peritrophic membrane proteins from the meadow moth, Loxostege sticticalis. International Journal of Biological Sciences, 6, 491–498.CrossRefPubMedPubMedCentralGoogle Scholar
  126. 126.
    Richards, A. G., & Richards, P. A. (1977). The peritrophic membrane of insects. Annual Review of Entomology, 22, 219–240.CrossRefPubMedGoogle Scholar
  127. 127.
    Binnington, K. C. (1988). Ultrastructure of the peritrophic membrane-secreting cells in the cardia of the blowfly, Lucilia cuprina. Tissue and Cell, 20, 269–281.CrossRefPubMedGoogle Scholar
  128. 128.
    Waterhouse, D. F. (1953). The occurrence and significance of the peritrophic membrane with special reference to adult Lepidoptera and Diptera. Australian Journal of Zoology, 1, 299–318.CrossRefGoogle Scholar
  129. 129.
    Harper, M. S., & Hopkins, T. L. (1997). Peritrophic membrane structure and secretion in European corn borer larvae (Ostrinia nubilalis). Tissue and Cell, 29, 463–475.CrossRefPubMedGoogle Scholar
  130. 130.
    Adang, M. J., & Spence, K. D. (1981). Surface morphology of peritrophic membrane formation in the cabbage looper, Trichoplusia ni. Cell and Tissue Research, 218, 141–147.CrossRefPubMedGoogle Scholar
  131. 131.
    Ryerse, J. S., Purcell, J. P., Sammons, R. D., & Lavrik, P. B. (1992). Peritrophic membrane structure and formation in the larva of a moth, Heliothis. Tissue and Cell, 24, 751–771.CrossRefPubMedGoogle Scholar
  132. 132.
    Silva, W., Cardoso, C., Ribeiro, A. F., Terra, W. R., & Ferreira, C. (2013). Midgut proteins released by microapocrine secretion in Spodoptera frugiperda. Journal of Insect Physiology, 59, 70–80.CrossRefPubMedGoogle Scholar
  133. 133.
    Hopkins, T. L., & Harper, M. S. (2001). Lepidopteran peritrophic membranes and effects of dietary wheat germ agglutinin on their formation and structure. Archives of Insect Biochemistry and Physiology, 47, 100–109.CrossRefPubMedGoogle Scholar
  134. 134.
    Kabir, A. (1987). Peritrophic membrane of the jute hairy caterpillar Diacrisia obliqua Walker. Bangladesh Journal of Zoology, 1, 9–16.Google Scholar
  135. 135.
    Zimoch, L., & Merzendorfer, H. (2002). Immunolocalization of chitin synthase in the tobacco hornworm. Cell and Tissue Research, 308, 287–297.CrossRefPubMedGoogle Scholar
  136. 136.
    Arakane, Y., Hogenkamp, D. G., Zhu, Y. C., Kramer, K. J., Specht, C. A., Beeman, R. W., Kanost, M. R., & Muthukrishnan, S. (2004). Characterization of two chitin synthase genes of the red flour beetle, Tribolium castaneum, and alternate exon usage in one of the genes during development. Insect Biochemistry and Molecular Biology, 34, 291–304.CrossRefPubMedGoogle Scholar
  137. 137.
    Hogenkamp, D. G., Arakane, Y., Zimoch, L., Merzendorfer, H., Kramer, K. J., Beeman, R. W., Kanost, M. R., Specht, C. A., & Muthukrishnan, S. (2005). Chitin synthase genes in Manduca sexta: Characterization of a gut-specific transcript and differential tissue expression of alternately spliced mRNAs during development. Insect Biochemistry and Molecular Biology, 35, 529–540.CrossRefPubMedGoogle Scholar
  138. 138.
    Terenius, O., Papanicolaou, A., Garbutt, J. S., Eleftherianos, I., Huvenne, H., Sriramana, K., Albrechtsen, M., An, C., Aymeric, J.-L., Barthel, A., Bebas, P., Bitra, K., Bravo, A., Chevalier, F., Collinge, D. P., Crava, C. M., de Maagd, R. A., Duvic, B., Erlandson, M., Faye, I., Felföldi, G., Fujiwara, H., Futahashi, R., Gandhe, A. S., Gatehouse, H. S., Gatehouse, L. N., Giebultowicz, J., Gómez, I., Grimmelikhuijzen, C. J., Groot, A. T., Hauser, F., Heckel, D. G., Hegedus, D. D., Hrycaj, S., Huang, L., Hull, J. J., Iatrou, K., Iga, M., Kanost, M. R., Kotwica, J., Li, C., Li, J., Liu, J., Lundmark, M., Matsumoto, S., Meyering-Vos, M., Millichap, P. J., Monteiro, A., Mrinal, N., Niimi, T., Nowara, D., Ohnishi, A., Oostra, V., Ozaki, K., Papakonstantinou, M., Popadic, A., Rajam, M. V., Saenko, S., Simpson, R. M., Soberón, M., Strand, M. R., Tomita, S., Toprak, U., Wang, P., Wee, C. W., Whyard, S., Zhang, W., Nagaraju, J., ffrench-Constant, R. H., Herrero, S., Gordon, K., Swevers, L., & Smagghe, G. (2011). RNA interference in lepidoptera: An overview of successful and unsuccessful studies and implications for experimental design. Journal of Insect Physiology, 57, 231–245.CrossRefPubMedGoogle Scholar
  139. 139.
    Whyard, S., Singh, A. D., & Wong, S. (2009). Ingested double-stranded RNAs can act as species-specific insecticides. Insect Biochemistry and Molecular Biology, 39, 824–832.CrossRefPubMedGoogle Scholar
  140. 140.
    Turner, C. T., Davy, M. W., MacDiarmid, R. M., Plummer, K. M., Birch, N. P., & Newcomb, R. D. (2006). RNA interference in the light brown apple moth, Epiphyas postvittana (Walker) induced by double-stranded RNA feeding. Insect Molecular Biology, 15, 383–391.CrossRefPubMedGoogle Scholar
  141. 141.
    Yang, Y., Zhu, Y. C., Ottea, J., Husseneder, C., Leonard, B. R., Abel, C., & Huang, F. (2010). Molecular characterization and RNA interference of three midgut aminopeptidase N isozymes from Bacillus thuringiensis-susceptible and -resistant strains of sugarcane borer, Diatraea saccharalis. Insect Biochemistry and Molecular Biology, 40, 592–603.CrossRefPubMedGoogle Scholar
  142. 142.
    Jayachandran, B., Hussain, M., & Asgari, S. (2013). An insect trypsin-like serine protease as a target of microRNA: Utilization of microRNA mimics and inhibitors by oral feeding. Insect Biochemistry and Molecular Biology, 43, 398–406.CrossRefPubMedGoogle Scholar
  143. 143.
    Toprak, U., Baldwin, D., Erlandson, M., Gillott, C., Harris, S., & Hegedus, D. D. (2013). In vitro and in vivo application of RNA interference for targeting genes involved in peritrophic matrix synthesis in a lepidopteran system. Insect Science, 20, 92–100.CrossRefPubMedGoogle Scholar
  144. 144.
    Jin, S., Singh, N. D., Li, L., Zhang, X., & Daniell, H. (2015). Engineered chloroplast dsRNA silences cytochrome p450 monooxygenase, V-ATPase and chitin synthase genes in the insect gut and disrupts Helicoverpa armigera larval development and pupation. Plant Biotechnology Journal, 13, 435–446.CrossRefPubMedPubMedCentralGoogle Scholar
  145. 145.
    Park, Y., & Kim, Y. (2013). RNA interference of cadherin gene expression in Spodoptera exigua reveals its significance as a specific Bt target. Journal of Invertebrate Pathology, 114, 285–291.CrossRefPubMedGoogle Scholar
  146. 146.
    Mao, Y. B., Cai, W. J., Wang, J. W., Hong, G. J., Tao, X. Y., Wang, L. J., Huang, Y. P., & Chen, X. Y. (2007). Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nature Biotechnology, 25, 1307–1313.CrossRefPubMedGoogle Scholar
  147. 147.
    Tian, H., Peng, H., Yao, Q., Chen, H., Xie, Q., Tang, B., & Zhang, W. (2009). Developmental control of a lepidopteran pest Spodoptera exigua by ingestion of bacteria expressing dsRNA of a non-midgut gene. PLoS One, 4, e6225.CrossRefPubMedPubMedCentralGoogle Scholar
  148. 148.
    Palli, S. R. (2012). RNAi methods for management of insects and their pathogens. CAB Review, 7, 1–10.CrossRefGoogle Scholar
  149. 149.
    Toprak, U., Coutu, C., Baldwin, D., Erlandson, M., & Hegedus, D. D. (2014). Development of an improved RNA interference vector system for Agrobacterium-mediated plant transformation. Turkish Journal of Biology, 38, 40–47.CrossRefGoogle Scholar
  150. 150.
    Zhang, J., Khan, S. A., Hasse, C., Ruf, S., Heckel, D. G., & Bock, R. (2015). Pest control. Full crop protection from an insect pest by expression of long double-stranded RNAs in plastids. Science, 347, 991–994.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Dwayne D. Hegedus
    • 1
    • 2
  • Umut Toprak
    • 3
  • Martin Erlandson
    • 2
    • 4
  1. 1.Department of Food and Bioproduct SciencesUniversity of SaskatchewanSaskatoonCanada
  2. 2.Agriculture and Agri-Food CanadaSaskatoonCanada
  3. 3.Department of Plant Protection, College of AgricultureUniversity of AnkaraAnkaraTurkey
  4. 4.Department of BiologyUniversity of SaskatchewanSaskatoonCanada

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