The molecular evolution of cytochrome P450 genes within and between Drosophila species

Robert T Good, Lydia Gramzow, Paul Battlay, Tamar Esther Sztal, Philip Batterham, Charles Robin

Research output: Contribution to journalArticleResearchpeer-review

33 Citations (Scopus)

Abstract

We map 114 gene gains and 74 gene losses in the P450 gene family across the phylogeny of 12Drosophila species by examining the congruence of gene trees and species trees. Although the number of P450 genes varies from 74 to 94 in the species examined, we we infer that there were at least 77 P450 genes in the ancestral Drosophila genome. One of the most striking observations in the data set is the elevated loss of P450 genes in the Drosophila sechelila lineage. The gain and loss events are not evenly distributed among the P450 genes with 30 genes showing no gene gains or losses whereas others show as many as2O copy number changes among the species examined.The P450 gene clades showing the fewest number of gene gain and loss events tend to be those evolving with the most purifying selection acting on the protein sequences, although there are exceptions, such as the rapid rate of amino acid replacement observed in the single copy phantom (Cyp306a1) gene. WithinD. melanogaster, we observe gene copy numberpolymorphism in ten P450 genes including multiple cases of interparalog chimeras. Nonallelic homologous recombination (NAHR) has been associated with deleterious mutations in humans, but here we provide a second possible example of an NAHR event in insect P450s being adaptive. Specifically, we find that a polymorphic Cyp12a4/Cyp12a5 chimera correlates with resistance to an insecticide. Although we observe such interparalog exchange in our within-species data sets, we have little evidence of it between species, raising the possibility that such events may occur more frequently than appreciated but are masked by subsequent sequence change.
Original languageEnglish
Pages (from-to)1118 - 1134
Number of pages17
JournalGenome Biology and Evolution
Volume6
Issue number5
DOIs
Publication statusPublished - 2014
Externally publishedYes

Keywords

  • cytochrome P450
  • Cyp12a4
  • phantom
  • Cyp6a20
  • Drosophila Genetic Reference Panel
  • nonallelic homologous recombination

Cite this

Good, Robert T ; Gramzow, Lydia ; Battlay, Paul ; Sztal, Tamar Esther ; Batterham, Philip ; Robin, Charles. / The molecular evolution of cytochrome P450 genes within and between Drosophila species. In: Genome Biology and Evolution. 2014 ; Vol. 6, No. 5. pp. 1118 - 1134.
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The molecular evolution of cytochrome P450 genes within and between Drosophila species. / Good, Robert T; Gramzow, Lydia; Battlay, Paul; Sztal, Tamar Esther; Batterham, Philip; Robin, Charles.

In: Genome Biology and Evolution, Vol. 6, No. 5, 2014, p. 1118 - 1134.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - The molecular evolution of cytochrome P450 genes within and between Drosophila species

AU - Good, Robert T

AU - Gramzow, Lydia

AU - Battlay, Paul

AU - Sztal, Tamar Esther

AU - Batterham, Philip

AU - Robin, Charles

PY - 2014

Y1 - 2014

N2 - We map 114 gene gains and 74 gene losses in the P450 gene family across the phylogeny of 12Drosophila species by examining the congruence of gene trees and species trees. Although the number of P450 genes varies from 74 to 94 in the species examined, we we infer that there were at least 77 P450 genes in the ancestral Drosophila genome. One of the most striking observations in the data set is the elevated loss of P450 genes in the Drosophila sechelila lineage. The gain and loss events are not evenly distributed among the P450 genes with 30 genes showing no gene gains or losses whereas others show as many as2O copy number changes among the species examined.The P450 gene clades showing the fewest number of gene gain and loss events tend to be those evolving with the most purifying selection acting on the protein sequences, although there are exceptions, such as the rapid rate of amino acid replacement observed in the single copy phantom (Cyp306a1) gene. WithinD. melanogaster, we observe gene copy numberpolymorphism in ten P450 genes including multiple cases of interparalog chimeras. Nonallelic homologous recombination (NAHR) has been associated with deleterious mutations in humans, but here we provide a second possible example of an NAHR event in insect P450s being adaptive. Specifically, we find that a polymorphic Cyp12a4/Cyp12a5 chimera correlates with resistance to an insecticide. Although we observe such interparalog exchange in our within-species data sets, we have little evidence of it between species, raising the possibility that such events may occur more frequently than appreciated but are masked by subsequent sequence change.

AB - We map 114 gene gains and 74 gene losses in the P450 gene family across the phylogeny of 12Drosophila species by examining the congruence of gene trees and species trees. Although the number of P450 genes varies from 74 to 94 in the species examined, we we infer that there were at least 77 P450 genes in the ancestral Drosophila genome. One of the most striking observations in the data set is the elevated loss of P450 genes in the Drosophila sechelila lineage. The gain and loss events are not evenly distributed among the P450 genes with 30 genes showing no gene gains or losses whereas others show as many as2O copy number changes among the species examined.The P450 gene clades showing the fewest number of gene gain and loss events tend to be those evolving with the most purifying selection acting on the protein sequences, although there are exceptions, such as the rapid rate of amino acid replacement observed in the single copy phantom (Cyp306a1) gene. WithinD. melanogaster, we observe gene copy numberpolymorphism in ten P450 genes including multiple cases of interparalog chimeras. Nonallelic homologous recombination (NAHR) has been associated with deleterious mutations in humans, but here we provide a second possible example of an NAHR event in insect P450s being adaptive. Specifically, we find that a polymorphic Cyp12a4/Cyp12a5 chimera correlates with resistance to an insecticide. Although we observe such interparalog exchange in our within-species data sets, we have little evidence of it between species, raising the possibility that such events may occur more frequently than appreciated but are masked by subsequent sequence change.

KW - cytochrome P450

KW - Cyp12a4

KW - phantom

KW - Cyp6a20

KW - Drosophila Genetic Reference Panel

KW - nonallelic homologous recombination

U2 - 10.1093/gbe/evu083

DO - 10.1093/gbe/evu083

M3 - Article

VL - 6

SP - 1118

EP - 1134

JO - Genome Biology and Evolution

JF - Genome Biology and Evolution

SN - 1759-6653

IS - 5

ER -