Dataset Information

Expansion of vomeronasal receptor genes (OlfC) in the evolution of fright reaction in Ostariophysan fishes.

ABSTRACT: Ostariophysans are the most diverse group of freshwater fishes and feature a pheromone-elicited fright reaction. However, the genetic basis of fright reaction is unclear. Here, we compared vomeronasal type 2 receptor-like (OlfC) genes from fishes having and lacking fright reaction, to provide insight into evolution of pheromonal olfaction in fishes. We found OlfC genes expanded remarkably in ostariophysans having fright reaction compared with fishes lacking fright reaction. Phylogenetic analysis indicates OlfC subfamily 9 expanded specifically in ostariophysans having fright reaction. Principle component and phylogenetic logistic regression analysis partitioned fishes by ecotype (having or lacking fright reaction) and identified OlfC subfamily 9 as being an important factor for fright reaction. Expression levels of expanded OlfC subfamily genes after fright reaction in zebrafish changed more than did genes that had not expanded. Furthermore, evidence of positive selection was found in the expanded OlfC proteins in ostariophysan fishes having fright reaction. These results provide new insight into the genetic basis of fright reaction in ostariophysan fish and will enable future research into the mechanism of action of OlfC proteins.

SUBMITTER: Yang L

PROVIDER: S-EPMC6588630 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Publications

Expansion of vomeronasal receptor genes (OlfC) in the evolution of fright reaction in Ostariophysan fishes.

Yang Liandong L Jiang Haifeng H Wang Ying Y Lei Yi Y Chen Juan J Sun Ning N Lv Wenqi W Wang Cheng C Near Thomas J TJ He Shunping S

Communications biology 20190621

Ostariophysans are the most diverse group of freshwater fishes and feature a pheromone-elicited fright reaction. However, the genetic basis of fright reaction is unclear. Here, we compared vomeronasal type 2 receptor-like (OlfC) genes from fishes having and lacking fright reaction, to provide insight into evolution of pheromonal olfaction in fishes. We found OlfC genes expanded remarkably in ostariophysans having fright reaction compared with fishes lacking fright reaction. Phyloge ...[more]

PMID: 31263779

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Project description:BackgroundIn teleost fishes that lack a vomeronasal organ, both main odorant receptors (ORs) and vomeronasal receptors family 2 (V2Rs) are expressed in the olfactory epithelium, and used for perception of water-soluble chemicals. In zebrafish, it is known that both ORs and V2Rs formed multigene families of about a hundred copies. Whereas the contribution of V2Rs in zebrafish to olfaction has been found to be substantially large, the composition and structure of the V2R gene family in other fishes are poorly known, compared with the OR gene family.ResultsTo understand the evolutionary dynamics of V2R genes in fishes, V2R sequences in zebrafish, medaka, fugu, and spotted green pufferfish were identified from their draft genome sequences. There were remarkable differences in the number of intact V2R genes in different species. Most V2R genes in these fishes were tightly clustered in one or two specific chromosomal regions. Phylogenetic analysis revealed that the fish V2R family could be subdivided into 16 subfamilies that had diverged before the separation of the four fishes. Genes in two subfamilies in zebrafish and another subfamily in medaka increased in their number independently, suggesting species-specific evolution in olfaction. Interestingly, the arrangements of V2R genes in the gene clusters were highly conserved among species in the subfamily level. A genomic region of tetrapods corresponding to the region in fishes that contains the V2R cluster was found to have no V2R gene in any species.ConclusionOur results have indicated that the evolutionary dynamics of fish V2Rs are characterized by rapid gene turnover and lineage-specific phylogenetic clustering. In addition, the present phylogenetic and comparative genome analyses have shown that the fish V2Rs have expanded after the divergence between teleost and tetrapod lineages. The present identification of the entire V2R repertoire in fishes would provide useful foundation to the future functional and evolutionary studies of fish V2R gene family.

Project description:BackgroundGene and genome duplication play important roles in the evolution of gene function. Compared to individual duplicated genes, gene clusters attract particular attention considering their frequent associations with innovation and adaptation. Here, we report for the first time the expansion of the apolipoprotein D (ApoD) ligand-transporter genes in a cluster manner specific to teleost fishes.ResultsBased on comparative genomic and transcriptomic analyses, protein 3D structure comparison, positive selection detection and breakpoints detection, the single ApoD gene in the ancestor expanded into two clusters following a dynamic evolutionary pattern in teleost fishes. Orthologous genes show conserved expression patterns, whereas lineage-specific duplicated genes show tissue-specific expression patterns and even evolve new gene expression profiles. Positive selection occurred in branches before and after gene duplication, especially for lineage-specific duplicated genes. Cluster analyses based on protein 3D structure comparisons, especially comparisons of the four loops at the opening side, show gene duplication-segregating patterns. Duplicated ApoD genes are predicted to be associated with forkhead transcription factors and MAPK genes. ApoD clusters are located next to the breakpoints of genome rearrangements.ConclusionsHere, we report the expansion of ApoD genes specific to teleost fishes in a cluster manner for the first time. Neofunctionalization and subfunctionalization were observed at both the protein and expression levels after duplication. Evidence from different aspects-i.e., abnormal expression-induced disease in humans, fish-specific expansion, predicted associations with forkhead transcription factors and MAPK genes, specific expression patterns in tissues related to sexual selection and adaptation, duplicated genes under positive selection and their location next to the breakpoints of genome rearrangements-suggests the potentially advantageous roles of ApoD genes in teleost fishes. The cluster expansion of ApoD genes specific to teleost fishes provides thus an ideal evo-devo model for studying gene duplication, cluster maintenance and new gene function emergence.

Dataset Information

Expansion of vomeronasal receptor genes (OlfC) in the evolution of fright reaction in Ostariophysan fishes.

Publications

Expansion of vomeronasal receptor genes (<i>OlfC</i>) in the evolution of fright reaction in Ostariophysan fishes.

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