The Organization of the Pig T-Cell Receptor γ (TRG) Locus Provides Insights into the Evolutionary Patterns of the TRG Genes across Cetartiodactyla

Serafina Massari,Anna Caputi Jambrenghi,Giovanna Linguiti,Pietro D’Addabbo,Salvatrice Ciccarese,Angela Pala,Francesco Giannico,Rachele Antonacci

doi:10.3390/genes13020177

Serafina Massari, Anna Caputi Jambrenghi + Show 6 more

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https://doi.org/10.3390/genes13020177

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Abstract

The domestic pig (Sus scrofa) is a species representative of the Suina, one of the four suborders within Cetartiodactyla. In this paper, we reported our analysis of the pig TRG locus in comparison with the loci of species representative of the Ruminantia, Tylopoda, and Cetacea suborders. The pig TRG genomic structure reiterates the peculiarity of the organization of Cetartiodactyla loci in TRGC “cassettes”, each containing the basic V-J-J-C unit. Eighteen genes arranged in four TRGC cassettes, form the pig TRG locus. All the functional TRG genes were expressed, and the TRGV genes preferentially rearrange with the TRGJ genes within their own cassette, which correlates the diversity of the γ-chain repertoire with the number of cassettes. Among them, the TRGC5, located at the 5′ end of the locus, is the only cassette that retains a marked homology with the corresponding TRGC cassettes of all the analyzed species. The preservation of the TRGC5 cassette for such a long evolutionary time presumes a highly specialized function of its genes, which could be essential for the survival of species. Therefore, the maintenance of this cassette in pigs confirms that it is the most evolutionarily ancient within Cetartiodactyla, and it has undergone a process of duplication to give rise to the other TRGC cassettes in the different artiodactyl species in a lineage-specific manner.

Highlights

Artiodactyla represents the largest order of terrestrial mammals
We investigated the genomic organization of the TRG locus in Sus scrofa, a species that we considered representative of the Suina suborder, to understand the origin and evolutionary dynamics of the TRG loci in the cetartiodactyl group
According to the germline sequences, four TRGV genes are pseudogenes: TRGV4, TRGV6, TRGV11, and we have considered the TRGV6 and TRGV12-2 functional genes and modified their nucleotide sequence based on the sequence of productive cDNA clones (GenBank Accession N◦ AB185445 and AB185447) that retain the two genes

Summary

Introduction

Artiodactyla was considered monophyletic and was traditionally divided into three major lineages: Suina, Tylopoda, and Ruminantia [1]. The modern phylogeny, based on molecular and paleontological data [2,3,4], recognized that Cetacea, a highly specialized mammalian order that includes whales, dolphins, and porpoises, is a nested member of Artiodactyla. Cetartiodactyla has become the generally accepted name for the superorder containing both orders, and it currently includes over 330 species grouped into 23 families and 131 genera [5]. The phylogeny of this superorder is controversial regarding the relationships among the major clades of cetartiodactyls. Different studies indicate a certain instability at the root of the phylogeny, varying between Suina or Tylopoda in stating the first lineage to

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