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Evolution in an ancient detoxification pathway is coupled with a transition to herbivory in the drosophilidae.
- Source :
-
Molecular biology and evolution [Mol Biol Evol] 2014 Sep; Vol. 31 (9), pp. 2441-56. Date of Electronic Publication: 2014 Jun 27. - Publication Year :
- 2014
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Abstract
- Chemically defended plant tissues present formidable barriers to herbivores. Although mechanisms to resist plant defenses have been identified in ancient herbivorous lineages, adaptations to overcome plant defenses during transitions to herbivory remain relatively unexplored. The fly genus Scaptomyza is nested within the genus Drosophila and includes species that feed on the living tissue of mustard plants (Brassicaceae), yet this lineage is derived from microbe-feeding ancestors. We found that mustard-feeding Scaptomyza species and microbe-feeding Drosophila melanogaster detoxify mustard oils, the primary chemical defenses in the Brassicaceae, using the widely conserved mercapturic acid pathway. This detoxification strategy differs from other specialist herbivores of mustard plants, which possess derived mechanisms to obviate mustard oil formation. To investigate whether mustard feeding is coupled with evolution in the mercapturic acid pathway, we profiled functional and molecular evolutionary changes in the enzyme glutathione S-transferase D1 (GSTD1), which catalyzes the first step of the mercapturic acid pathway and is induced by mustard defense products in Scaptomyza. GSTD1 acquired elevated activity against mustard oils in one mustard-feeding Scaptomyza species in which GstD1 was duplicated. Structural analysis and mutagenesis revealed that substitutions at conserved residues within and near the substrate-binding cleft account for most of this increase in activity against mustard oils. Functional evolution of GSTD1 was coupled with signatures of episodic positive selection in GstD1 after the evolution of herbivory. Overall, we found that preexisting functions of generalized detoxification systems, and their refinement by natural selection, could play a central role in the evolution of herbivory.<br /> (© The Author 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)
- Subjects :
- Animals
Drosophilidae classification
Drosophilidae genetics
Evolution, Molecular
Gene Duplication
Glutathione Transferase metabolism
Herbivory genetics
Insect Proteins metabolism
Mustard Plant chemistry
Mutation
Phylogeny
Selection, Genetic
Signal Transduction
Acetylcysteine metabolism
Drosophilidae physiology
Glutathione Transferase genetics
Insect Proteins genetics
Mustard Plant metabolism
Plant Oils metabolism
Subjects
Details
- Language :
- English
- ISSN :
- 1537-1719
- Volume :
- 31
- Issue :
- 9
- Database :
- MEDLINE
- Journal :
- Molecular biology and evolution
- Publication Type :
- Academic Journal
- Accession number :
- 24974374
- Full Text :
- https://doi.org/10.1093/molbev/msu201