Evolution in an ancient detoxification pathway is coupled with a transition to herbivory in the drosophilidae

Andrew D. Gloss, Daniel G. Vassão, Alexander L. Hailey, Anna C. Nelson Dittrich, Katharina Schramm, Michael Reichelt, Timothy J. Rast, Andrzej Weichsel, Matthew G. Cravens, Jonathan Gershenzon, William "Bill" Montfort, Noah K Whiteman

Research output: Contribution to journalArticle

37 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)2441-2456
Number of pages16
JournalMolecular Biology and Evolution
Volume31
Issue number9
DOIs
StatePublished - 2014

Fingerprint

Drosophilidae
Mustard Plant
Herbivory
Scaptomyza
mustard (condiment)
detoxification
herbivory
mustard oil
herbivores
Acetylcysteine
Glutathione Transferase
glutathione transferase
plant defense
oil
Brassicaceae
herbivore
acid
acids
chemical defense
microorganisms

Keywords

  • Detoxification
  • Drosophila
  • Gene duplication
  • Glutathione S-transferase
  • Isothiocyanate
  • Plant-herbivore interactions

ASJC Scopus subject areas

  • Genetics
  • Molecular Biology
  • Ecology, Evolution, Behavior and Systematics

Cite this

Evolution in an ancient detoxification pathway is coupled with a transition to herbivory in the drosophilidae. / Gloss, Andrew D.; Vassão, Daniel G.; Hailey, Alexander L.; Nelson Dittrich, Anna C.; Schramm, Katharina; Reichelt, Michael; Rast, Timothy J.; Weichsel, Andrzej; Cravens, Matthew G.; Gershenzon, Jonathan; Montfort, William "Bill"; Whiteman, Noah K.

In: Molecular Biology and Evolution, Vol. 31, No. 9, 2014, p. 2441-2456.

Research output: Contribution to journalArticle

Gloss, AD, Vassão, DG, Hailey, AL, Nelson Dittrich, AC, Schramm, K, Reichelt, M, Rast, TJ, Weichsel, A, Cravens, MG, Gershenzon, J, Montfort, WB & Whiteman, NK 2014, 'Evolution in an ancient detoxification pathway is coupled with a transition to herbivory in the drosophilidae', Molecular Biology and Evolution, vol. 31, no. 9, pp. 2441-2456. https://doi.org/10.1093/molbev/msu201
Gloss, Andrew D. ; Vassão, Daniel G. ; Hailey, Alexander L. ; Nelson Dittrich, Anna C. ; Schramm, Katharina ; Reichelt, Michael ; Rast, Timothy J. ; Weichsel, Andrzej ; Cravens, Matthew G. ; Gershenzon, Jonathan ; Montfort, William "Bill" ; Whiteman, Noah K. / Evolution in an ancient detoxification pathway is coupled with a transition to herbivory in the drosophilidae. In: Molecular Biology and Evolution. 2014 ; Vol. 31, No. 9. pp. 2441-2456.
@article{2671ff1e558d455696f2c42a58f1781b,
title = "Evolution in an ancient detoxification pathway is coupled with a transition to herbivory in the drosophilidae",
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.",
keywords = "Detoxification, Drosophila, Gene duplication, Glutathione S-transferase, Isothiocyanate, Plant-herbivore interactions",
author = "Gloss, {Andrew D.} and Vass{\~a}o, {Daniel G.} and Hailey, {Alexander L.} and {Nelson Dittrich}, {Anna C.} and Katharina Schramm and Michael Reichelt and Rast, {Timothy J.} and Andrzej Weichsel and Cravens, {Matthew G.} and Jonathan Gershenzon and Montfort, {William {"}Bill{"}} and Whiteman, {Noah K}",
year = "2014",
doi = "10.1093/molbev/msu201",
language = "English (US)",
volume = "31",
pages = "2441--2456",
journal = "Molecular Biology and Evolution",
issn = "0737-4038",
publisher = "Oxford University Press",
number = "9",

}

TY - JOUR

T1 - Evolution in an ancient detoxification pathway is coupled with a transition to herbivory in the drosophilidae

AU - Gloss, Andrew D.

AU - Vassão, Daniel G.

AU - Hailey, Alexander L.

AU - Nelson Dittrich, Anna C.

AU - Schramm, Katharina

AU - Reichelt, Michael

AU - Rast, Timothy J.

AU - Weichsel, Andrzej

AU - Cravens, Matthew G.

AU - Gershenzon, Jonathan

AU - Montfort, William "Bill"

AU - Whiteman, Noah K

PY - 2014

Y1 - 2014

N2 - 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.

AB - 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.

KW - Detoxification

KW - Drosophila

KW - Gene duplication

KW - Glutathione S-transferase

KW - Isothiocyanate

KW - Plant-herbivore interactions

UR - http://www.scopus.com/inward/record.url?scp=84906766044&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84906766044&partnerID=8YFLogxK

U2 - 10.1093/molbev/msu201

DO - 10.1093/molbev/msu201

M3 - Article

C2 - 24974374

AN - SCOPUS:84906766044

VL - 31

SP - 2441

EP - 2456

JO - Molecular Biology and Evolution

JF - Molecular Biology and Evolution

SN - 0737-4038

IS - 9

ER -