The expansion of the TRB and TRG genes in domestic goats (Capra hircus) is characteristic of the ruminant species

Abstract

Background Goats (Capra hircus), 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. Results 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 V genes at the 5′ end, leading to a marked expansion in the number of the TRBV 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 TRG 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. Conclusions Taken together, these findings demonstrate that strong evolutionary pressures in the ruminant lineage have selected for the development of enlarged sets of TRB and TRG genes that contribute to a diverse T cell receptor repertoire. However, differences observed among the goat, sheep and cattle TRB and TRG genes indicate that distinct evolutionary histories, with independent expansions and/or contractions, have also affected each ruminant species.

The T Cell Receptor (TRB) Locus in Tursiops truncatus: From Sequence to Structure of the Alpha/Beta Heterodimer in the Human/Dolphin Comparison

“…The structure of the dolphin D-J-C clusters region is similar to that of other artiodactyl species [ 24 , 25 , 26 , 27 , 32 , 53 , 54 ]. The TRBD, TRBJ, and TRBC genes are distributed within three in tandem D-J-C clusters located at the 3′ end of the TRB locus, with the numbers 1, 3, and 2 corresponding to their positions from 5′ to 3′ ( Figure 1 A, Supplementary Dataset S1 ).…”

“…The TRBD, TRBJ, and TRBC genes are distributed within three in tandem D-J-C clusters located at the 3′ end of the TRB locus, with the numbers 1, 3, and 2 corresponding to their positions from 5′ to 3′ ( Figure 1 A, Supplementary Dataset S1 ). The name D-J-C cluster 3 was attributed to the central cluster as in sheep, goat, dromedary, and pig [ 24 , 25 , 26 , 27 , 32 , 54 ].…”

“…The TRBV genes used for the phylogenetic analysis were retrieved from the following sequences deposited in the GEDI (for G enBank/ E NA/ D DBJ/ I MGT/LIGM-DB) databases: NW_011591622, NW_011593440, NW_011591151 ( Camelus dromedarius TRB locus contig as previously characterized [ 26 , 27 ]), NC_010460 ( Sus scrofa TRB locus contig as previously characterized [ 24 ]); and NC_030811.1 ( Capra hircus TRB locus contig as previously characterized [ 32 ]) ( Supplementary Table S3 ).…”

The Genomic Organisation of the TRA/TRD Locus Validates the Peculiar Characteristics of Dromedary δ-Chain Expression

“…Moreover, looking at the expressed γδ TR repertoire, the diversity is significantly higher in artiodactyl species than in humans and mice. This feature is favored by the large number of germline genes encoding for γ and δ chains, as proved by the genomic analysis of the TRG and TRD loci in the major livestock species (sheep, goat and cattle) [ 11 , 12 , 17 ].…”

“…In this context, the genomic organisation of the dromedary TRG locus has been recently completed by combining previous cloning data [ 6 ] with the analysis of genomic assemblies [ 10 ]. The locus is single with respect to ruminants’ TRG1 and TRG2 loci [ 11 , 12 ], and as in cows, sheep and goats it is organised in “cassettes”, each containing the basic V–J–J–C recombination unit. Only three cassettes with six functional TRGV germline genes compose the dromedary TRG locus.…”