Expansion by whole genome duplication and evolution of the sox gene family in teleost fish.

Magali Naville,Delphine Galiana,Jean-Nicolas Volff,Emilien Voldoire,Frédéric Brunet

doi:10.1371/journal.pone.0180936

Abstract

It is now recognized that several rounds of whole genome duplication (WGD) have occurred during the evolution of vertebrates, but the link between WGDs and phenotypic diversification remains unsolved. We have investigated in this study the impact of the teleost-specific WGD on the evolution of the sox gene family in teleostean fishes. The sox gene family, which encodes for transcription factors, has essential role in morphology, physiology and behavior of vertebrates and teleosts, the current largest group of vertebrates. We have first redrawn the evolution of all sox genes identified in eleven teleost genomes using a comparative genomic approach including phylogenetic and synteny analyses. We noticed, compared to tetrapods, an important expansion of the sox family: 58% (11/19) of sox genes are duplicated in teleost genomes. Furthermore, all duplicated sox genes, except sox17 paralogs, are derived from the teleost-specific WGD. Then, focusing on five sox genes, analyzing the evolution of coding and non-coding sequences, as well as the expression patterns in fish embryos and adult tissues, we demonstrated that these paralogs followed lineage-specific evolutionary trajectories in teleost genomes. This work, based on whole genome data from multiple teleostean species, supports the contribution of WGDs to the expansion of gene families, as well as to the emergence of genomic differences between lineages that might promote genetic and phenotypic diversity in teleosts.

Highlights

The origin and evolution of biodiversity remain fundamental questions in biology [1]
On the nineteen vertebrate sox genes used as query, some seem to be absent in particular teleostean species or lineages, as no corresponding sequences have been identified for the vertebrate sox10 gene in the cavefish genome, for sox12 gene in the acanthopterygian genomes, and for sox30 gene in six teleost genomes
If we look solely at coding elements (CNEs) conserved through teleost and tetrapods, considered as highly important ones due to their ancientness, we remark that they are systematically found in the vicinity of less divergent paralogs as 2, 2 and 5 vCNEs are identified around sox4b, sox8b and sox11a, respectively

Summary

Introduction

The origin and evolution of biodiversity remain fundamental questions in biology [1]. The importance of gene duplication in innovation and diversification has been recognized for several decades [2,3,4]. The duplication of all genes through wholegenome duplications (WGDs) corresponding to polyploidization events could provide a remarkable opportunity for the emergence of evolutionary novelties and functional diversification [5, 6]. Even if paleopolyploidy events are rare [6], several rounds of ancient WGD have been inferred in vertebrates, including two WGDs at the base of the vertebrate lineage [4, 7]. It is well established that an additional WGD, known as the teleost-specific WGD, occurred in the lineage leading to teleostean fishes about 250 mya [8–.

Objectives

Methods

Results

Discussion

Conclusion