CYP6B1 and CYP6B3 of the black swallowtail (Papilio polyxenes): Adaptive evolution through subfunctionalization

Zhimou Wen, Sanjeewa Rupasinghe, Guodong Niu, May R Berenbaum, Mary A Schuler

Research output: Contribution to journalArticle

Abstract

Gene duplication provides essential material for functional divergence of proteins and hence allows organisms to adapt to changing environments. Following duplication events, redundant paralogs may undergo different evolutionary paths via processes known as nonfunctionalization, neofunctionalization, or subfunctionalization. Studies of adaptive evolution at the molecular level have progressed rapidly by computationally analyzing nucleotide substitution patterns but such studies are limited by the absence of information relating to alterations of function of the encoded enzymes. In this respect, evolution of the Papilio polyxenes cytochrome P450 monooxygenases (P450s) responsible for the adaptation of this insect to furanocoumarin-containing host plants provides an excellent model for elucidating the evolutionary fate of duplicated genes. Evidence from sequence and functional analysis in combination with molecular modeling indicates that the paralogous CYP6B1 and CYP6B3 genes in P. polyxenes have probably evolved via subfunctionalization after the duplication event by which they arose. Both enzymes have been under independent purifying selection as evidenced by the low dN/dS ratio in both the coding region and substrate recognition sites. Both enzymes have maintained their ability to metabolize linear and angular furanocoumarins albeit at different efficiencies. Comparisons of molecular models developed for the CYP6B3 and CYP6B1 proteins highlight differences in their binding modes that account for their different activities toward linear and angular furanocoumarins. That P. polyxenes maintains these 2 furanocoumarin-metabolizing loci with somewhat different activities and expression patterns provides this species with the potential to acquire P450s with novel functions while maintaining those most critical to its exclusive feeding on its current range of host plants.

Original languageEnglish (US)
Pages (from-to)2434-2443
Number of pages10
JournalMolecular biology and evolution
Volume23
Issue number12
DOIs
StatePublished - Dec 1 2006

Fingerprint

Papilio polyxenes
psoralens
enzyme
host plant
gene
Genes
Mixed Function Oxygenases
protein
Enzymes
host plants
enzymes
molecular models
Functional analysis
Molecular Models
Gene Duplication
Molecular modeling
cytochrome
Molecular Evolution
substitution
gene duplication

Keywords

  • Adaptive evolution
  • Cytochrome P450 monooxygenases (P450s)
  • Molecular modeling of detoxification enzymes
  • Plant-insect interactions
  • Subfunctionalization

ASJC Scopus subject areas

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

Cite this

CYP6B1 and CYP6B3 of the black swallowtail (Papilio polyxenes) : Adaptive evolution through subfunctionalization. / Wen, Zhimou; Rupasinghe, Sanjeewa; Niu, Guodong; Berenbaum, May R; Schuler, Mary A.

In: Molecular biology and evolution, Vol. 23, No. 12, 01.12.2006, p. 2434-2443.

Research output: Contribution to journalArticle

@article{8b19988efdb847568b021e71315b7c13,
title = "CYP6B1 and CYP6B3 of the black swallowtail (Papilio polyxenes): Adaptive evolution through subfunctionalization",
abstract = "Gene duplication provides essential material for functional divergence of proteins and hence allows organisms to adapt to changing environments. Following duplication events, redundant paralogs may undergo different evolutionary paths via processes known as nonfunctionalization, neofunctionalization, or subfunctionalization. Studies of adaptive evolution at the molecular level have progressed rapidly by computationally analyzing nucleotide substitution patterns but such studies are limited by the absence of information relating to alterations of function of the encoded enzymes. In this respect, evolution of the Papilio polyxenes cytochrome P450 monooxygenases (P450s) responsible for the adaptation of this insect to furanocoumarin-containing host plants provides an excellent model for elucidating the evolutionary fate of duplicated genes. Evidence from sequence and functional analysis in combination with molecular modeling indicates that the paralogous CYP6B1 and CYP6B3 genes in P. polyxenes have probably evolved via subfunctionalization after the duplication event by which they arose. Both enzymes have been under independent purifying selection as evidenced by the low dN/dS ratio in both the coding region and substrate recognition sites. Both enzymes have maintained their ability to metabolize linear and angular furanocoumarins albeit at different efficiencies. Comparisons of molecular models developed for the CYP6B3 and CYP6B1 proteins highlight differences in their binding modes that account for their different activities toward linear and angular furanocoumarins. That P. polyxenes maintains these 2 furanocoumarin-metabolizing loci with somewhat different activities and expression patterns provides this species with the potential to acquire P450s with novel functions while maintaining those most critical to its exclusive feeding on its current range of host plants.",
keywords = "Adaptive evolution, Cytochrome P450 monooxygenases (P450s), Molecular modeling of detoxification enzymes, Plant-insect interactions, Subfunctionalization",
author = "Zhimou Wen and Sanjeewa Rupasinghe and Guodong Niu and Berenbaum, {May R} and Schuler, {Mary A}",
year = "2006",
month = "12",
day = "1",
doi = "10.1093/molbev/msl118",
language = "English (US)",
volume = "23",
pages = "2434--2443",
journal = "Molecular Biology and Evolution",
issn = "0737-4038",
publisher = "Oxford University Press",
number = "12",

}

TY - JOUR

T1 - CYP6B1 and CYP6B3 of the black swallowtail (Papilio polyxenes)

T2 - Adaptive evolution through subfunctionalization

AU - Wen, Zhimou

AU - Rupasinghe, Sanjeewa

AU - Niu, Guodong

AU - Berenbaum, May R

AU - Schuler, Mary A

PY - 2006/12/1

Y1 - 2006/12/1

N2 - Gene duplication provides essential material for functional divergence of proteins and hence allows organisms to adapt to changing environments. Following duplication events, redundant paralogs may undergo different evolutionary paths via processes known as nonfunctionalization, neofunctionalization, or subfunctionalization. Studies of adaptive evolution at the molecular level have progressed rapidly by computationally analyzing nucleotide substitution patterns but such studies are limited by the absence of information relating to alterations of function of the encoded enzymes. In this respect, evolution of the Papilio polyxenes cytochrome P450 monooxygenases (P450s) responsible for the adaptation of this insect to furanocoumarin-containing host plants provides an excellent model for elucidating the evolutionary fate of duplicated genes. Evidence from sequence and functional analysis in combination with molecular modeling indicates that the paralogous CYP6B1 and CYP6B3 genes in P. polyxenes have probably evolved via subfunctionalization after the duplication event by which they arose. Both enzymes have been under independent purifying selection as evidenced by the low dN/dS ratio in both the coding region and substrate recognition sites. Both enzymes have maintained their ability to metabolize linear and angular furanocoumarins albeit at different efficiencies. Comparisons of molecular models developed for the CYP6B3 and CYP6B1 proteins highlight differences in their binding modes that account for their different activities toward linear and angular furanocoumarins. That P. polyxenes maintains these 2 furanocoumarin-metabolizing loci with somewhat different activities and expression patterns provides this species with the potential to acquire P450s with novel functions while maintaining those most critical to its exclusive feeding on its current range of host plants.

AB - Gene duplication provides essential material for functional divergence of proteins and hence allows organisms to adapt to changing environments. Following duplication events, redundant paralogs may undergo different evolutionary paths via processes known as nonfunctionalization, neofunctionalization, or subfunctionalization. Studies of adaptive evolution at the molecular level have progressed rapidly by computationally analyzing nucleotide substitution patterns but such studies are limited by the absence of information relating to alterations of function of the encoded enzymes. In this respect, evolution of the Papilio polyxenes cytochrome P450 monooxygenases (P450s) responsible for the adaptation of this insect to furanocoumarin-containing host plants provides an excellent model for elucidating the evolutionary fate of duplicated genes. Evidence from sequence and functional analysis in combination with molecular modeling indicates that the paralogous CYP6B1 and CYP6B3 genes in P. polyxenes have probably evolved via subfunctionalization after the duplication event by which they arose. Both enzymes have been under independent purifying selection as evidenced by the low dN/dS ratio in both the coding region and substrate recognition sites. Both enzymes have maintained their ability to metabolize linear and angular furanocoumarins albeit at different efficiencies. Comparisons of molecular models developed for the CYP6B3 and CYP6B1 proteins highlight differences in their binding modes that account for their different activities toward linear and angular furanocoumarins. That P. polyxenes maintains these 2 furanocoumarin-metabolizing loci with somewhat different activities and expression patterns provides this species with the potential to acquire P450s with novel functions while maintaining those most critical to its exclusive feeding on its current range of host plants.

KW - Adaptive evolution

KW - Cytochrome P450 monooxygenases (P450s)

KW - Molecular modeling of detoxification enzymes

KW - Plant-insect interactions

KW - Subfunctionalization

UR - http://www.scopus.com/inward/record.url?scp=33750933169&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=33750933169&partnerID=8YFLogxK

U2 - 10.1093/molbev/msl118

DO - 10.1093/molbev/msl118

M3 - Article

C2 - 16984951

AN - SCOPUS:33750933169

VL - 23

SP - 2434

EP - 2443

JO - Molecular Biology and Evolution

JF - Molecular Biology and Evolution

SN - 0737-4038

IS - 12

ER -