Comparative Proteomics of Peritrophic Matrix Provides an Insight into Its Role in Cry1Ac Resistance of Cotton Bollworm

Overview

Journal Toxins (Basel)

Publisher MDPI

Specialty Toxicology

Date 2019 Feb 6

PMID 30717423

Citations 5

Authors

Minghui Jin

Chongyu Liao

Swapan Chakrabarty

Kongming Wu

Yutao Xiao

Affiliations

Soon will be listed here.

Abstract

Crystalline (Cry) proteins from (Bt) are widely used in sprays and transgenic crops to control insect pests, but the evolution of insect resistance threatens their long-term use. Different resistance mechanisms have been identified, but some have not been completely elucidated. Here, the transcriptome of the midgut and proteome of the peritrophic matrix (PM) were comparatively analyzed to identify potential mechanism of resistance to Cry1Ac in laboratory-selected strain XJ10 of . This strain had a 146-fold resistance to Cry1Ac protoxin and 45-fold resistance to Cry1Ac activated toxin compared with XJ strain. The mRNA and protein levels for several trypsin genes were downregulated in XJ10 compared to the susceptible strain XJ. Furthermore, 215 proteins of the PM were identified, and nearly all had corresponding mRNAs in the midgut. These results provide new insights that the PM may participate in Bt resistance.

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References

Mendelsohn M, Kough J, Vaituzis Z, Matthews K . Are Bt crops safe?. Nat Biotechnol. 2003; 21(9):1003-9. DOI: 10.1038/nbt0903-1003. View

Pardo-Lopez L, Soberon M, Bravo A . Bacillus thuringiensis insecticidal three-domain Cry toxins: mode of action, insect resistance and consequences for crop protection. FEMS Microbiol Rev. 2012; 37(1):3-22. DOI: 10.1111/j.1574-6976.2012.00341.x. View

Tabashnik B, Zhang M, Fabrick J, Wu Y, Gao M, Huang F . Dual mode of action of Bt proteins: protoxin efficacy against resistant insects. Sci Rep. 2015; 5:15107. PMC: 4601037. DOI: 10.1038/srep15107. View

Liu C, Xiao Y, Li X, Oppert B, Tabashnik B, Wu K . Cis-mediated down-regulation of a trypsin gene associated with Bt resistance in cotton bollworm. Sci Rep. 2014; 4:7219. PMC: 4245529. DOI: 10.1038/srep07219. View

Zhang S, Cheng H, Gao Y, Wang G, Liang G, Wu K . Mutation of an aminopeptidase N gene is associated with Helicoverpa armigera resistance to Bacillus thuringiensis Cry1Ac toxin. Insect Biochem Mol Biol. 2009; 39(7):421-9. DOI: 10.1016/j.ibmb.2009.04.003. View

Campbell P, Cao A, Hines E, East P, Gordon K . Proteomic analysis of the peritrophic matrix from the gut of the caterpillar, Helicoverpa armigera. Insect Biochem Mol Biol. 2008; 38(10):950-8. DOI: 10.1016/j.ibmb.2008.07.009. View

Gill S, Cowles E, Pietrantonio P . The mode of action of Bacillus thuringiensis endotoxins. Annu Rev Entomol. 1992; 37:615-36. DOI: 10.1146/annurev.en.37.010192.003151. View

Toprak U, Hegedus D, Baldwin D, Coutu C, Erlandson M . Spatial and temporal synthesis of Mamestra configurata peritrophic matrix through a larval stadium. Insect Biochem Mol Biol. 2014; 54:89-97. DOI: 10.1016/j.ibmb.2014.09.002. View

Wu K, Lu Y, Feng H, Jiang Y, Zhao J . Suppression of cotton bollworm in multiple crops in China in areas with Bt toxin-containing cotton. Science. 2008; 321(5896):1676-8. DOI: 10.1126/science.1160550. View

10.

Jurat-Fuentes J, Gould F, Adang M . Altered Glycosylation of 63- and 68-kilodalton microvillar proteins in Heliothis virescens correlates with reduced Cry1 toxin binding, decreased pore formation, and increased resistance to Bacillus thuringiensis Cry1 toxins. Appl Environ Microbiol. 2002; 68(11):5711-7. PMC: 129908. DOI: 10.1128/AEM.68.11.5711-5717.2002. View

11.

Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg S . TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013; 14(4):R36. PMC: 4053844. DOI: 10.1186/gb-2013-14-4-r36. View

12.

Wang Y, Xiu J, Cheng J, Luo M, Zhao P, Shang X . Proteomic Analysis of the Peritrophic Matrix from the Midgut of Third Instar Larvae, Musca domestica. Biomed Environ Sci. 2016; 29(1):56-65. DOI: 10.3967/bes2015.006. View

13.

Akhurst R, James W, Bird L, Beard C . Resistance to the Cry1Ac delta-endotoxin of Bacillus thuringiensis in the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae). J Econ Entomol. 2003; 96(4):1290-9. DOI: 10.1603/0022-0493-96.4.1290. View

14.

Xiao Y, Zhang T, Liu C, Heckel D, Li X, Tabashnik B . Mis-splicing of the ABCC2 gene linked with Bt toxin resistance in Helicoverpa armigera. Sci Rep. 2014; 4:6184. PMC: 4143771. DOI: 10.1038/srep06184. View

15.

Wang P, Granados R . Molecular structure of the peritrophic membrane (PM): identification of potential PM target sites for insect control. Arch Insect Biochem Physiol. 2001; 47(2):110-8. DOI: 10.1002/arch.1041. View

16.

Wu K, Guo Y . The evolution of cotton pest management practices in China. Annu Rev Entomol. 2004; 50:31-52. DOI: 10.1146/annurev.ento.50.071803.130349. View

17.

Wang P, Granados R . Calcofluor disrupts the midgut defense system in insects. Insect Biochem Mol Biol. 2000; 30(2):135-43. DOI: 10.1016/s0965-1748(99)00108-3. View

18.

Li H, Oppert B, Higgins R, Huang F, Zhu K, Buschman L . Comparative analysis of proteinase activities of Bacillus thuringiensis-resistant and -susceptible Ostrinia nubilalis (Lepidoptera: Crambidae). Insect Biochem Mol Biol. 2004; 34(8):753-62. DOI: 10.1016/j.ibmb.2004.03.010. View

19.

Wei J, Liang G, Wang B, Zhong F, Chen L, Khaing M . Activation of Bt Protoxin Cry1Ac in Resistant and Susceptible Cotton Bollworm. PLoS One. 2016; 11(6):e0156560. PMC: 4892611. DOI: 10.1371/journal.pone.0156560. View

20.

Tabashnik B, Brevault T, Carriere Y . Insect resistance to Bt crops: lessons from the first billion acres. Nat Biotechnol. 2013; 31(6):510-21. DOI: 10.1038/nbt.2597. View