期刊
MOLECULAR BIOLOGY AND EVOLUTION
卷 31, 期 9, 页码 2441-2456出版社
OXFORD UNIV PRESS
DOI: 10.1093/molbev/msu201
关键词
plant-herbivore interactions; glutathione S-transferase; detoxification; gene duplication; Drosophila; isothiocyanate
资金
- National Institutes of Health [R01 HL062969, S10 RR025485, 5K12GM000708-13]
- National Science Foundation [DEB-1256758, DEB-1405966, DGE-1143953]
- National Science Foundation (University of Arizona IGERT Genomics Fellowship) [DGE-0654435]
- John Templeton Foundation [41855]
- National Geographic Society [9097-12]
- University of Arizona
- Rocky Mountain Biological Laboratory
- Max Planck Society
- Department of Energy Office of Biological and Environmental Research
- National Institutes of Health, National Institute of General Medical Sciences [P41GM103393]
- National Center for Research Resources [P41RR001209]
- Direct For Biological Sciences
- Division Of Environmental Biology [1256758] Funding Source: National Science Foundation
- Division Of Environmental Biology
- Direct For Biological Sciences [1405966] Funding Source: National Science Foundation
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.
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