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Glucosinolate induces transcriptomic and metabolic reprogramming in Helicoverpa armigera

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Abstract

Glucosinolates protect plants from herbivory. Lepidopteran insects have developed resistance to glucosinolates which is well studied. However, the molecular effects of glucosinolate intake on insects are unexplored. To elucidate this, we performed transcriptomics and metabolomics of sinigrin-fed Helicoverpa armigera. Transcriptomics exhibits significant dysregulation of 2375 transcripts, of which 1575 are upregulated and 800 downregulated. Gene Ontology analysis of differentially expressed genes reveals that key hydrolases, oxidoreductases, and transferases are majorly affected. The negative impact of sinigrin is significant and localized in the endomembrane system and mitochondria. It also disturbs various biological processes such as regulation of protein metabolism and cytoskeletal organization. Furthermore, H. armigera putative myrosinase-like enzymes may catalyze the breakdown of sinigrin to allyl isothiocyanate (AITC). AITC targets the electron transport chain causing oxidative stress. KEGG pathway enrichment shows significant upregulation of oxidative phosphorylation, glutathione metabolism and amino acid metabolism. Activation of these pathways induces glutathione synthesis for sinigrin detoxification. Differential gene expression indicates upregulation of glutathione S-transferase and succinate dehydrogenase suggesting mitochondrial impact. Transcriptomics data correlated with metabolomics show changes in serine, methionine, ornithine, and other metabolite levels. It corroborates well with the transcript alterations supporting the increased glutathione production. Thus, our data suggest that sinigrin generates oxidative stress in H. armigera and insects alter their metabolic wiring to overcome sinigrin-mediated deleterious effects.

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Acknowledgement

The project work is supported by the research grant from the Department of Science and Technology—Science and Engineering Research Board (DST-SERB), Government of India under ECR/2015/000502 grant. The authors acknowledge the Council of Scientific and Industrial Research (CSIR), New Delhi, India and CSIR-National Chemical Laboratory, Pune, India for providing infrastructure and financial support.

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Correspondence to Rakesh S. Joshi.

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The authors declare no competing financial interest.

Supplementary Information

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Supplementary file1 Supplementary Data 1: Recipe for insect artificial diet. (DOCX 14 KB)

Supplementary file2 Supplementary Data 2: Primer sequence list used for real-time PCR (XLSX 9 KB)

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Supplementary file3 Supplementary Data 3: Transcriptomic data analysis of control and sinigrin-fed insects. Details of all the transcripts including their significance values, annotations are given. (XLSX 13659 KB)

Supplementary file4 Supplementary Data 4: Top five upregulated and downregulated gene expression values. (XLSX 11KB)

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Supplementary file5 Supplementary Data 5: Myrosinase protein sequences, structural and binding site analysis. Sequence details of the 7 upregulated myrosinase, their protein models and binding site details are mentioned. (DOCX 315 KB)

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Supplementary file6 Supplementary Data 6: Myrosinase docking results and heatmap data. Docking of all 7 myrosinase with various aliphatic and indolic glucosinolates was done. The binding scores used to draw interaction maps are given. (XLSX 17 KB)

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Supplementary file7 Supplementary Data 7: Targeted metabolomics data analysis results. Details of metabolites selected for targeted analysis. It includes m/z and area under the peak for all the metabolites. (XLSX 49 KB)

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Jagdale, S., Tellis, M., Barvkar, V.T. et al. Glucosinolate induces transcriptomic and metabolic reprogramming in Helicoverpa armigera. 3 Biotech 11, 26 (2021). https://doi.org/10.1007/s13205-020-02596-5

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  • DOI: https://doi.org/10.1007/s13205-020-02596-5

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