Intradiol ring cleavage dioxygenases from herbivorous spider mites as a new detoxification enzyme family in animals
- Author
- Christine Njiru (UGent) , Wenxin Xue, Sander De Rouck (UGent) , Juan M. Alba, Merijn R. Kant, Maksymilian Chruszcz, Bartel Vanholme (UGent) , Wannes Dermauw (UGent) , Nicky Wybouw (UGent) and Thomas Van Leeuwen (UGent)
- Organization
- Project
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- POLYADAPT (Molecular-genetic mechanisms of extreme adaptation in a polyphagous agricultural pest)
- The eco-evolutionary drivers of the Wolbachia pandemic in garden spider mites
- SuperPests (Innovative tools for rational control of the most difficult-to-manage pests (super pests) and the diseases they transmit)
- Abstract
- Background Generalist herbivores such as the two-spotted spider mite Tetranychus urticae thrive on a wide variety of plants and can rapidly adapt to novel hosts. What traits enable polyphagous herbivores to cope with the diversity of secondary metabolites in their variable plant diet is unclear. Genome sequencing of T. urticae revealed the presence of 17 genes that code for secreted proteins with strong homology to "intradiol ring cleavage dioxygenases (DOGs)" from bacteria and fungi, and phylogenetic analyses show that they have been acquired by horizontal gene transfer from fungi. In bacteria and fungi, DOGs have been well characterized and cleave aromatic rings in catecholic compounds between adjacent hydroxyl groups. Such compounds are found in high amounts in solanaceous plants like tomato, where they protect against herbivory. To better understand the role of this gene family in spider mites, we used a multi-disciplinary approach to functionally characterize the various T. urticae DOG genes. Results We confirmed that DOG genes were present in the T. urticae genome and performed a phylogenetic reconstruction using transcriptomic and genomic data to advance our understanding of the evolutionary history of spider mite DOG genes. We found that DOG expression differed between mites from different plant hosts and was induced in response to jasmonic acid defense signaling. In consonance with a presumed role in detoxification, expression was localized in the mite's gut region. Silencing selected DOGs expression by dsRNA injection reduced the mites' survival rate on tomato, further supporting a role in mitigating the plant defense response. Recombinant purified DOGs displayed a broad substrate promiscuity, cleaving a surprisingly wide array of aromatic plant metabolites, greatly exceeding the metabolic capacity of previously characterized microbial DOGs. Conclusion Our findings suggest that the laterally acquired spider mite DOGs function as detoxification enzymes in the gut, disarming plant metabolites before they reach toxic levels. We provide experimental evidence to support the hypothesis that this proliferated gene family in T. urticae is causally linked to its ability to feed on an extremely wide range of host plants.
- Keywords
- TETRANYCHUS-URTICAE, CATECHOL 1, 2-DIOXYGENASE, MOLECULAR ANALYSIS, CRYSTAL-STRUCTURE, GENE-EXPRESSION, SECONDARY METABOLITES, TRANSCRIPTION, FACTOR, PLANT DEFENSE, KEY ENZYME, RESISTANCE, Tetranychidae, Plant-herbivore interactions, Dioxygenases, Ortho-cleavage, Aromatic compounds
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Citation
Please use this url to cite or link to this publication: http://hdl.handle.net/1854/LU-8759947
- MLA
- Njiru, Christine, et al. “Intradiol Ring Cleavage Dioxygenases from Herbivorous Spider Mites as a New Detoxification Enzyme Family in Animals.” BMC BIOLOGY, vol. 20, no. 1, 2022, doi:10.1186/s12915-022-01323-1.
- APA
- Njiru, C., Xue, W., De Rouck, S., Alba, J. M., Kant, M. R., Chruszcz, M., … Van Leeuwen, T. (2022). Intradiol ring cleavage dioxygenases from herbivorous spider mites as a new detoxification enzyme family in animals. BMC BIOLOGY, 20(1). https://doi.org/10.1186/s12915-022-01323-1
- Chicago author-date
- Njiru, Christine, Wenxin Xue, Sander De Rouck, Juan M. Alba, Merijn R. Kant, Maksymilian Chruszcz, Bartel Vanholme, Wannes Dermauw, Nicky Wybouw, and Thomas Van Leeuwen. 2022. “Intradiol Ring Cleavage Dioxygenases from Herbivorous Spider Mites as a New Detoxification Enzyme Family in Animals.” BMC BIOLOGY 20 (1). https://doi.org/10.1186/s12915-022-01323-1.
- Chicago author-date (all authors)
- Njiru, Christine, Wenxin Xue, Sander De Rouck, Juan M. Alba, Merijn R. Kant, Maksymilian Chruszcz, Bartel Vanholme, Wannes Dermauw, Nicky Wybouw, and Thomas Van Leeuwen. 2022. “Intradiol Ring Cleavage Dioxygenases from Herbivorous Spider Mites as a New Detoxification Enzyme Family in Animals.” BMC BIOLOGY 20 (1). doi:10.1186/s12915-022-01323-1.
- Vancouver
- 1.Njiru C, Xue W, De Rouck S, Alba JM, Kant MR, Chruszcz M, et al. Intradiol ring cleavage dioxygenases from herbivorous spider mites as a new detoxification enzyme family in animals. BMC BIOLOGY. 2022;20(1).
- IEEE
- [1]C. Njiru et al., “Intradiol ring cleavage dioxygenases from herbivorous spider mites as a new detoxification enzyme family in animals,” BMC BIOLOGY, vol. 20, no. 1, 2022.
@article{8759947, abstract = {{Background Generalist herbivores such as the two-spotted spider mite Tetranychus urticae thrive on a wide variety of plants and can rapidly adapt to novel hosts. What traits enable polyphagous herbivores to cope with the diversity of secondary metabolites in their variable plant diet is unclear. Genome sequencing of T. urticae revealed the presence of 17 genes that code for secreted proteins with strong homology to "intradiol ring cleavage dioxygenases (DOGs)" from bacteria and fungi, and phylogenetic analyses show that they have been acquired by horizontal gene transfer from fungi. In bacteria and fungi, DOGs have been well characterized and cleave aromatic rings in catecholic compounds between adjacent hydroxyl groups. Such compounds are found in high amounts in solanaceous plants like tomato, where they protect against herbivory. To better understand the role of this gene family in spider mites, we used a multi-disciplinary approach to functionally characterize the various T. urticae DOG genes. Results We confirmed that DOG genes were present in the T. urticae genome and performed a phylogenetic reconstruction using transcriptomic and genomic data to advance our understanding of the evolutionary history of spider mite DOG genes. We found that DOG expression differed between mites from different plant hosts and was induced in response to jasmonic acid defense signaling. In consonance with a presumed role in detoxification, expression was localized in the mite's gut region. Silencing selected DOGs expression by dsRNA injection reduced the mites' survival rate on tomato, further supporting a role in mitigating the plant defense response. Recombinant purified DOGs displayed a broad substrate promiscuity, cleaving a surprisingly wide array of aromatic plant metabolites, greatly exceeding the metabolic capacity of previously characterized microbial DOGs. Conclusion Our findings suggest that the laterally acquired spider mite DOGs function as detoxification enzymes in the gut, disarming plant metabolites before they reach toxic levels. We provide experimental evidence to support the hypothesis that this proliferated gene family in T. urticae is causally linked to its ability to feed on an extremely wide range of host plants.}}, articleno = {{131}}, author = {{Njiru, Christine and Xue, Wenxin and De Rouck, Sander and Alba, Juan M. and Kant, Merijn R. and Chruszcz, Maksymilian and Vanholme, Bartel and Dermauw, Wannes and Wybouw, Nicky and Van Leeuwen, Thomas}}, issn = {{1741-7007}}, journal = {{BMC BIOLOGY}}, keywords = {{TETRANYCHUS-URTICAE,CATECHOL 1,2-DIOXYGENASE,MOLECULAR ANALYSIS,CRYSTAL-STRUCTURE,GENE-EXPRESSION,SECONDARY METABOLITES,TRANSCRIPTION,FACTOR,PLANT DEFENSE,KEY ENZYME,RESISTANCE,Tetranychidae,Plant-herbivore interactions,Dioxygenases,Ortho-cleavage,Aromatic compounds}}, language = {{eng}}, number = {{1}}, pages = {{23}}, title = {{Intradiol ring cleavage dioxygenases from herbivorous spider mites as a new detoxification enzyme family in animals}}, url = {{http://doi.org/10.1186/s12915-022-01323-1}}, volume = {{20}}, year = {{2022}}, }
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