
Trans-driven variation in expression is common among detoxification genes in the extreme generalist herbivore Tetranychus urticae
- Author
- Andre Kurlovs (UGent) , Berdien De Beer, Meiyuan Ji, Marilou Vandenhole (UGent) , Tim De Meyer (UGent) , René Feyereisen (UGent) , Richard M. Clark and Thomas Van Leeuwen (UGent)
- Organization
- Project
-
- POLYADAPT (Molecular-genetic mechanisms of extreme adaptation in a polyphagous agricultural pest)
- SuperPests (Innovative tools for rational control of the most difficult-to-manage pests (super pests) and the diseases they transmit)
- Abstract
- The extreme adaptation potential of the generalist herbivore Tetranychus urticae (the two-spotted spider mite) to pesticides as well as diverse host plants has been associated with clade-specific gene expansions in known detoxifying enzyme families, and with extensive and rapid transcriptional responses. However, how this broad transcriptional potential is regulated remains largely unknown. Using a parental/F1 design in which four inbred strains were crossed to a common inbred strain, we assessed the genetic basis and inheritance of gene expression variation in T. urticae. Mirroring known phenotypic variation in the progenitor strains of the inbreds, we confirmed that the inbred strains we created were genetically distinct, varied markedly in pesticide resistance, and also captured variation in host plant fitness as is commonly observed in this species. By examining differences in gene expression between parents and allele-specific expression in F1s, we found that variation in RNA abundance was more often explained in trans as compared to cis, with the former associated with dominance in inheritance. Strikingly, in a gene ontology analysis, detoxification genes of the cytochrome P450 monooxygenase (CYP) family, as well as dioxygenases (DOGs) acquired from horizontal gene transfer from fungi, were specifically enriched at the extremes of trans-driven up- and downregulation. In particular, multiple CYPs and DOGs with broad substrate-specificities for pesticides or plant specialized compounds were exceptionally highly upregulated as a result of trans-regulatory variation, or in some cases synergism of cis and trans, in the most multi-pesticide resistant strains. Collectively, our findings highlight the potential importance of trans-driven expression variation in genes associated with xenobiotic metabolism and host plant use for rapid adaptation in T. urticae, and also suggests modular control of these genes, a regulatory architecture that might ameliorate negative pleiotropic effects.
- Keywords
- Cancer Research, Genetics (clinical), Genetics, Molecular Biology, Ecology, Evolution, Behavior and Systematics
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Citation
Please use this url to cite or link to this publication: http://hdl.handle.net/1854/LU-01GPBJ840DDHSJZ62DDG5KE04R
- MLA
- Kurlovs, Andre, et al. “Trans-Driven Variation in Expression Is Common among Detoxification Genes in the Extreme Generalist Herbivore Tetranychus Urticae.” PLOS GENETICS, vol. 18, no. 11, 2022, doi:10.1371/journal.pgen.1010333.
- APA
- Kurlovs, A., De Beer, B., Ji, M., Vandenhole, M., De Meyer, T., Feyereisen, R., … Van Leeuwen, T. (2022). Trans-driven variation in expression is common among detoxification genes in the extreme generalist herbivore Tetranychus urticae. PLOS GENETICS, 18(11). https://doi.org/10.1371/journal.pgen.1010333
- Chicago author-date
- Kurlovs, Andre, Berdien De Beer, Meiyuan Ji, Marilou Vandenhole, Tim De Meyer, René Feyereisen, Richard M. Clark, and Thomas Van Leeuwen. 2022. “Trans-Driven Variation in Expression Is Common among Detoxification Genes in the Extreme Generalist Herbivore Tetranychus Urticae.” PLOS GENETICS 18 (11). https://doi.org/10.1371/journal.pgen.1010333.
- Chicago author-date (all authors)
- Kurlovs, Andre, Berdien De Beer, Meiyuan Ji, Marilou Vandenhole, Tim De Meyer, René Feyereisen, Richard M. Clark, and Thomas Van Leeuwen. 2022. “Trans-Driven Variation in Expression Is Common among Detoxification Genes in the Extreme Generalist Herbivore Tetranychus Urticae.” PLOS GENETICS 18 (11). doi:10.1371/journal.pgen.1010333.
- Vancouver
- 1.Kurlovs A, De Beer B, Ji M, Vandenhole M, De Meyer T, Feyereisen R, et al. Trans-driven variation in expression is common among detoxification genes in the extreme generalist herbivore Tetranychus urticae. PLOS GENETICS. 2022;18(11).
- IEEE
- [1]A. Kurlovs et al., “Trans-driven variation in expression is common among detoxification genes in the extreme generalist herbivore Tetranychus urticae,” PLOS GENETICS, vol. 18, no. 11, 2022.
@article{01GPBJ840DDHSJZ62DDG5KE04R, abstract = {{The extreme adaptation potential of the generalist herbivore Tetranychus urticae (the two-spotted spider mite) to pesticides as well as diverse host plants has been associated with clade-specific gene expansions in known detoxifying enzyme families, and with extensive and rapid transcriptional responses. However, how this broad transcriptional potential is regulated remains largely unknown. Using a parental/F1 design in which four inbred strains were crossed to a common inbred strain, we assessed the genetic basis and inheritance of gene expression variation in T. urticae. Mirroring known phenotypic variation in the progenitor strains of the inbreds, we confirmed that the inbred strains we created were genetically distinct, varied markedly in pesticide resistance, and also captured variation in host plant fitness as is commonly observed in this species. By examining differences in gene expression between parents and allele-specific expression in F1s, we found that variation in RNA abundance was more often explained in trans as compared to cis, with the former associated with dominance in inheritance. Strikingly, in a gene ontology analysis, detoxification genes of the cytochrome P450 monooxygenase (CYP) family, as well as dioxygenases (DOGs) acquired from horizontal gene transfer from fungi, were specifically enriched at the extremes of trans-driven up- and downregulation. In particular, multiple CYPs and DOGs with broad substrate-specificities for pesticides or plant specialized compounds were exceptionally highly upregulated as a result of trans-regulatory variation, or in some cases synergism of cis and trans, in the most multi-pesticide resistant strains. Collectively, our findings highlight the potential importance of trans-driven expression variation in genes associated with xenobiotic metabolism and host plant use for rapid adaptation in T. urticae, and also suggests modular control of these genes, a regulatory architecture that might ameliorate negative pleiotropic effects.}}, articleno = {{e1010333}}, author = {{Kurlovs, Andre and De Beer, Berdien and Ji, Meiyuan and Vandenhole, Marilou and De Meyer, Tim and Feyereisen, René and Clark, Richard M. and Van Leeuwen, Thomas}}, issn = {{1553-7404}}, journal = {{PLOS GENETICS}}, keywords = {{Cancer Research,Genetics (clinical),Genetics,Molecular Biology,Ecology, Evolution, Behavior and Systematics}}, language = {{eng}}, number = {{11}}, pages = {{33}}, title = {{Trans-driven variation in expression is common among detoxification genes in the extreme generalist herbivore Tetranychus urticae}}, url = {{http://doi.org/10.1371/journal.pgen.1010333}}, volume = {{18}}, year = {{2022}}, }
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