The Expansion of the TRB and TRG Genes in Domestic Goats (Capra hircus) is Characteristic of the Ruminant Species

Abstract

<jats:title>Abstract</jats:title> <jats:p><jats:bold>Background</jats:bold>: Goats (<jats:italic>Capra hircus</jats:italic>), one of the first domesticated species, are economically important for milk and meat production, and their broad geographical distribution reflects their successful adaptation to diverse environmental conditions. Despite the relevance of this species, the genetic research on the goat traits is limited compared to other domestic species. Thanks to the latest goat reference genomic sequence (ARS1), which is considered to be one of the most continuous assemblies in livestock, we deduced the genomic structure of the T cell receptor beta (TRB) and gamma (TRG) loci in this ruminant species. <jats:bold>Results</jats:bold>: Our analyses revealed that although the organization of the goat TRB locus is broadly similar to that of the other artiodactyl species, with three in tandem D-J-C clusters located at the 3’ end, a complex and extensive series of duplications have occurred in the <jats:italic>V</jats:italic> genes at the 5’ end, leading to a marked expansion in the number of the <jats:italic>TRBV</jats:italic> genes. This phenomenon appears to be a feature of the ruminant lineage since similar gene expansions have also occurred in sheep and cattle.Likewise, the general organization of the goat <jats:italic>TRG</jats:italic> genes is typical of ruminant species studied so far, with two paralogous TRG loci, TRG1 and TRG2, located in two distinct and distant positions on the same chromosome as result of a split in the ancestral locus. Each TRG locus consists of reiterated V-J-J-C cassettes, with the goat TRG2 containing an additional cassette relative to the corresponding sheep and cattle loci.<jats:bold>Conclusions</jats:bold>: Taken together, these findings demonstrate that strong evolutionary pressures in the ruminant lineage have selected for the development of enlarged sets of <jats:italic>TRB</jats:italic> and <jats:italic>TRG</jats:italic> genes that contribute to a diverse T cell receptor repertoire. However, differences observed among the goat, sheep and cattle <jats:italic>TRB</jats:italic> and <jats:italic>TRG</jats:italic> genes indicate that distinct evolutionary histories, with independent expansions and/or contractions, have also affected each ruminant species.</jats:p>

The Organization of the Pig T-cell Receptor Gamma (TRG) Locus Provides Insights Into the Evolutionary Patterns of the TRG Genes Across Cetartiodactyla

“…The human, bovine, sheep, dolphin TRGV and TRGC gene sequences used for the phylogenetic analysis, as annotated, were retrieved from the IMGT® database (IMGT Repertoire, http://www.imgt.org, IMGT/GENE-DB, [22]. The goat, dromedary and pig gene sequences were retrieved from GenBank database with the following accession numbers: NC_030811.1 (goat TRG locus contig as characterized by Giannico et al [17]); GCA_000803125.1, JN165102 and JN172913 (dromedary TRG locus as characterized by Antonacci et al [23]); and NC_010451.4 (pig TRG locus as characterized in this work). We combined the nucleotide sequences of the V-REGION of the pig TRGV genes with the corresponding gene sequences of sheep, goats, cattle, dromedaries, dolphins and humans.…”

“…The TRG genes occupy about 113 kb and are flanked by the AMPH and STARD3NL genes at the 5' and 3' ends, respectively (Figure 1). Basically, the deduced genomic structure of the TRG locus in pigs reflects the peculiarity of the organization of this region in the other artiodactyl species, consisting of a set of closely related "cassettes", each containing the V−J−J−C basic unit arranged in the same transcriptional orientation [13,17]. Particularly, the pig TRG locus comprises eight TRGV, six TRGJ and four TRGC genes distributed in four V−J−(J)−C cassettes, which is fewer than the number of cassettes characterizing the ruminant TRG locus (seven in cattle and goats, and six in sheep) [13,17], but it is greater than the number present in the dromedary (three cassettes) [23] and dolphin (a single cassette) [36] loci.…”

“…Basically, the deduced genomic structure of the TRG locus in pigs reflects the peculiarity of the organization of this region in the other artiodactyl species, consisting of a set of closely related "cassettes", each containing the V−J−J−C basic unit arranged in the same transcriptional orientation [13,17]. Particularly, the pig TRG locus comprises eight TRGV, six TRGJ and four TRGC genes distributed in four V−J−(J)−C cassettes, which is fewer than the number of cassettes characterizing the ruminant TRG locus (seven in cattle and goats, and six in sheep) [13,17], but it is greater than the number present in the dromedary (three cassettes) [23] and dolphin (a single cassette) [36] loci. The total number of TRG genes in pigs is also lower than that of ruminants (36 in goats, 34 in cattle and 32 in sheep), but comparable to that in dromedaries (17 genes) and higher than that in dolphins (six genes).…”

“…Moreover, the potential diversity of the  and  chain repertoires is wider and more diverse in the artiodactyl species compared to the restricted and limited repertoire in humans and mice. In turn, the  and  chain repertoires depend on the gene organization, which interestingly shows high variability among different species [13,[15][16][17][18].…”

“…The genomic organization of the locus encoding for the TR  chain (TRG) is the most considerably different across vertebrates and seems to be related to the evolution of species [13,17].…”