| Title: | Intradiol ring cleavage dioxygenases from herbivorous spider mites as a new detoxification enzyme family in animals |
| Author(s): | Njiru C; Xue W; De Rouck S; Alba JM; Kant MR; Chruszcz M; Vanholme B; Dermauw W; Wybouw N; Van Leeuwen T; |
| Address: | "Laboratory of Agrozoology, Department of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium. Department of Evolutionary and Population Biology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands. Department of Chemistry and Biochemistry, University of South Carolina, Columbia, SC, 29208, USA. Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium. VIB Center for Plant Systems Biology, Ghent, Belgium. Flanders Research Institute for Agriculture, Fisheries and Food (ILVO), Plant Sciences Unit, Merelbeke, Belgium. Terrestrial Ecology Unit, Department of Biology, Faculty of Sciences, Ghent University, Ghent, Belgium. nicky.wybouw@ugent.be. Laboratory of Agrozoology, Department of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium. thomas.vanleeuwen@ugent.be" |
| DOI: | 10.1186/s12915-022-01323-1 |
| ISSN/ISBN: | 1741-7007 (Electronic) 1741-7007 (Linking) |
| 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: | Animals *Dioxygenases/genetics Herbivory *Solanum lycopersicum/genetics Phylogeny Plants *Tetranychidae/genetics Aromatic compounds Dioxygenases Ortho-cleavage Plant-herbivore interactions Tetranychidae; |
| Notes: | "MedlineNjiru, Christine Xue, Wenxin De Rouck, Sander Alba, Juan M Kant, Merijn R Chruszcz, Maksymilian Vanholme, Bartel Dermauw, Wannes Wybouw, Nicky Van Leeuwen, Thomas eng Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. England 2022/06/07 BMC Biol. 2022 Jun 4; 20(1):131. doi: 10.1186/s12915-022-01323-1" |
