Differences in midgut transcriptomes between resistant and susceptible strains of Chilo suppressalis to Cry1C toxin

Geng Chen,Fajun Chen,Lanzhi Han,Yanhui Wang,Yanmin Liu

doi:10.1186/s12864-020-07051-6

Abstract

BackgroundChilo suppressalis is a widespread rice pest that poses a major threat to food security in China. This pest can develop resistance to Cry toxins from Bacillus thuringiensis (Bt), threatening the sustainable use of insect-resistant transgenic Bt rice. However, the molecular basis for the resistance mechanisms of C. suppressalis to Cry1C toxin remains unknown. This study aimed to identify genes associated with the mechanism of Cry1C resistance in C. suppressalis by comparing the midgut transcriptomic responses of resistant and susceptible C. suppressalis strains to Cry1C toxin and to provide information for insect resistance management.ResultsA C. suppressalis midgut transcriptome of 139,206 unigenes was de novo assembled from 373 million Illumina HiSeq and Roche 454 clean reads. Comparative analysis identified 5328 significantly differentially expressed unigenes (DEGs) between C. suppressalis Cry1C-resistant and -susceptible strains. DEGs encoding Bt Cry toxin receptors, aminopeptidase-P like protein, the ABC subfamily and alkaline phosphatase were downregulated, suggesting an association with C. suppressalis Cry1C resistance. Additionally, Cry1C resistance in C. suppressalis may be related to changes in the transcription levels of enzymes involved in hydrolysis, digestive, catalytic and detoxification processes.ConclusionOur study identified genes potentially involved in Cry1C resistance in C. suppressalis by comparative transcriptome analysis. The assembled and annotated transcriptome data provide valuable genomic resources for further study of the molecular mechanisms of C. suppressalis resistance to Cry toxins.

Highlights

Chilo suppressalis is a widespread rice pest that poses a major threat to food security in China
The interaction between the activated toxin and cadherin receptor results in proteolytic cleavage and activated toxin oligomerization. These oligomers bind to glycosylphosphatidylinositol (GPI)-anchoring receptors, aminopeptidase N (APN) and alkaline phosphatase (ALP), among others; the oligomers are inserted into lipid raft membranes and form pores that affect the ionic balance across the cell membrane, causing cell death due to osmotic lysis [12, 13]
In conclusion, this study is the first to report the mechanism of C. suppressalis resistance to Cry toxin based on genetic information from the sequenced transcriptome, revealing a large number of unigenes with greatly enriched sequence information for C. suppressalis

Summary

Introduction

Based on the pore formation model, protoxin is solubilized in the alkaline gut, digested by gut proteinase, and converted to the activated toxin, which binds to the cadherin receptor located in the cell membrane of the insect midgut. Decreased conversion of the protoxin to activated toxin and reduced toxin binding of Cry toxin to receptors are considered the most common mechanisms resulting in insect resistance to Cry toxins due to downregulation or mutation of the midgut proteinase and receptors [15, 16]. Reduced binding ability of Cry toxin to midgut receptors via a decrease in the activity and transcription of ALP or APN as well as mutations of APN, cadherin, and ABCC2 [14, 22, 25,26,27,28] lead to Cry1A resistance in H. armigera, Heliothis virescens, Plutella xylostella and Bombyx. Reduced binding ability of Cry toxin to midgut receptors via a decrease in the activity and transcription of ALP or APN as well as mutations of APN, cadherin, and ABCC2 [14, 22, 25,26,27,28] lead to Cry1A resistance in H. armigera, Heliothis virescens, Plutella xylostella and Bombyx. mori

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