Multispecies Analysis of Expression Pattern Diversification in the Recently Expanded Insect Ly6 Gene Family

Autoren

Kohtaro Tanaka
Yoan Diekmann
Alexis Hazbun
Assia Hijazi
Barbara Vreede
Fernando Roch
Élio Sucena

DOI

10.1093/molbev/msv052

eISSN

1537-1719

ISSN

0737-4038

Ausgabe der Veröffentlichung

7

Zeitschrift

Molecular Biology and Evolution

Sprache

en

Online publication date

2015

Paginierung

1730 - 1747

Datum der Veröffentlichung

2015

Status

Published

Herausgeber

Oxford University Press (OUP)

Herausgeber URL

http://dx.doi.org/10.1093/molbev/msv052

Datum der Datenerfassung

2022

Titel

Multispecies Analysis of Expression Pattern Diversification in the Recently Expanded Insect Ly6 Gene Family

Ausgabe der Zeitschrift

32

Data source: Crossref

Abstract

Gene families often consist of members with diverse expression domains reflecting their functions in a wide variety of tissues. However, how the expression of individual members, and thus their tissue-specific functions, diversified during the course of gene family expansion is not well understood. In this study, we approached this question through the analysis of the duplication history and transcriptional evolution of a rapidly expanding subfamily of insect Ly6 genes. We analyzed different insect genomes and identified seven Ly6 genes that have originated from a single ancestor through sequential duplication within the higher Diptera. We then determined how the original embryonic expression pattern of the founding gene diversified by characterizing its tissue-specific expression in the beetle Tribolium castaneum, the butterfly Bicyclus anynana, and the mosquito Anopheles stephensi and those of its duplicates in three higher dipteran species, representing various stages of the duplication history (Megaselia abdita, Ceratitis capitata, and Drosophila melanogaster). Our results revealed that frequent neofunctionalization episodes contributed to the increased expression breadth of this subfamily and that these events occurred after duplication and speciation events at comparable frequencies. In addition, at each duplication node, we consistently found asymmetric expression divergence. One paralog inherited most of the tissue-specificities of the founder gene, whereas the other paralog evolved drastically reduced expression domains. Our approach attests to the power of combining a well-established duplication history with a comprehensive coverage of representative species in acquiring unequivocal information about the dynamics of gene expression evolution in gene families.

Addresses

Instituto Gulbenkian de Ciência, Oeiras, Portugal ktanaka@igc.gulbenkian.pt.

Autoren

Kohtaro Tanaka
Yoan Diekmann
Alexis Hazbun
Assia Hijazi
Barbara Vreede
Fernando Roch
Élio Sucena

DOI

10.1093/molbev/msv052

eISSN

1537-1719

Externe Identifier

PubMed Identifier: 25743545
PubMed Central ID: PMC4476152

Open access

true

ISSN

0737-4038

Ausgabe der Veröffentlichung

7

Zeitschrift

Molecular biology and evolution

Schlüsselwörter

Embryo, Nonmammalian
Animals
Gene Expression Profiling
Evolution, Molecular
Phylogeny
Organ Specificity
Species Specificity
Gene Expression Regulation
Gene Duplication
Genes, Insect
Multigene Family
Insecta

Sprache

eng

Medium

Print-Electronic

Online publication date

2015

Open access status

Open Access

Paginierung

1730 - 1747

Datum der Veröffentlichung

2015

Status

Published

Publisher licence

CC BY-NC

Datum der Datenerfassung

2015

Titel

Multispecies Analysis of Expression Pattern Diversification in the Recently Expanded Insect Ly6 Gene Family.

Sub types

Research Support, Non-U.S. Gov't
research-article
Journal Article

Ausgabe der Zeitschrift

32

Files

https://academic.oup.com/mbe/article-pdf/32/7/1730/13166245/msv052.pdf https://europepmc.org/articles/PMC4476152?pdf=render

Data source: Europe PubMed Central

Abstract

Gene families often consist of members with diverse expression domains reflecting their functions in a wide variety of tissues. However, how the expression of individual members, and thus their tissue-specific functions, diversified during the course of gene family expansion is not well understood. In this study, we approached this question through the analysis of the duplication history and transcriptional evolution of a rapidly expanding subfamily of insect Ly6 genes. We analyzed different insect genomes and identified seven Ly6 genes that have originated from a single ancestor through sequential duplication within the higher Diptera. We then determined how the original embryonic expression pattern of the founding gene diversified by characterizing its tissue-specific expression in the beetle Tribolium castaneum, the butterfly Bicyclus anynana, and the mosquito Anopheles stephensi and those of its duplicates in three higher dipteran species, representing various stages of the duplication history (Megaselia abdita, Ceratitis capitata, and Drosophila melanogaster). Our results revealed that frequent neofunctionalization episodes contributed to the increased expression breadth of this subfamily and that these events occurred after duplication and speciation events at comparable frequencies. In addition, at each duplication node, we consistently found asymmetric expression divergence. One paralog inherited most of the tissue-specificities of the founder gene, whereas the other paralog evolved drastically reduced expression domains. Our approach attests to the power of combining a well-established duplication history with a comprehensive coverage of representative species in acquiring unequivocal information about the dynamics of gene expression evolution in gene families.

Autoren

Kohtaro Tanaka
Yoan Diekmann
Alexis Hazbun
Assia Hijazi
Barbara Vreede
Fernando Roch
Élio Sucena

Autoren-URL

https://www.ncbi.nlm.nih.gov/pubmed/25743545

DOI

10.1093/molbev/msv052

eISSN

1537-1719

Externe Identifier

PubMed Central ID: PMC4476152

Ausgabe der Veröffentlichung

7

Zeitschrift

Mol Biol Evol

Schlüsselwörter

Drosophila
Ly6 protein
gene duplication
gene family evolution
regulatory evolution
Animals
Embryo, Nonmammalian
Evolution, Molecular
Gene Duplication
Gene Expression Profiling
Gene Expression Regulation
Genes, Insect
Insecta
Multigene Family
Organ Specificity
Phylogeny
Species Specificity

Sprache

eng

Country

United States

Paginierung

1730 - 1747

PII

msv052

Datum der Veröffentlichung

2015

Status

Published

Datum, an dem der Datensatz öffentlich gemacht wurde

2016

Titel

Multispecies Analysis of Expression Pattern Diversification in the Recently Expanded Insect Ly6 Gene Family.

Sub types

Journal Article
Research Support, Non-U.S. Gov't

Ausgabe der Zeitschrift

32

Data source: PubMed

Multispecies Analysis of Expression Pattern Diversification in the Recently Expanded Insect Ly6 Gene Family

Files

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