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Comparative Analysis of the pIgR Gene from the Antarctic Teleost Trematomus bernacchii Reveals Distinctive Features of Cold-Adapted Notothenioidei

ABSTRACT: The IgM and IgT classes were previously identified and characterized in the Antarctic teleost Trematomus bernacchii, a species belonging to the Perciform suborder Notothenoidei. Herein, we characterized the gene encoding the polymeric immunoglobulin receptor (pIgR) in the same species and compared it to the pIgR of multiple teleost species belonging to five perciform suborders, including 11 Antarctic and 1 non-Antarctic (Cottoperca gobio) notothenioid species, the latter living in the less-cold peri-Antarctic sea. Antarctic pIgR genes displayed particularly long introns marked by sites of transposable elements and transcription factors. Furthermore, analysis of T. bernacchii pIgR cDNA unveiled multiple amino acid substitutions unique to the Antarctic species, all introducing adaptive features, including N-glycosylation sequons. Interestingly, C. gobio shared most features with the other perciforms rather than with the cold-adapted relatives. T. bernacchii pIgR transcripts were predominantly expressed in mucosal tissues, as indicated by q-PCR and in situ hybridization analysis. These results suggest that in cold-adapted species, pIgR preserved its fundamental role in mucosal immune defense, although remarkable gene structure modifications occurred.

SUBMITTER: Ametrano A

PROVIDER: S-EPMC9321927 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND:Chromosomal rearrangements are thought to be an important driving force underlying lineage diversification, but their link to speciation continues to be debated. Antarctic teleost fish of the family Nototheniidae (Notothenioidei) diversified in a changing environmental context, which led to ecological, morphological, and genetic differentiation among populations. In addition, extensive chromosomal repatterning accompanied species divergence in several clades. The most striking karyotypic changes involved the recent species radiation (about 10 My) of the genus Trematomus, with chromosomal pair numbers ranging between 29 and 12. These dramatic reductions in chromosome number resulted mostly from large-scale chromosome fusions. Multiple centric and/or tandem fusions have been hypothesized in at least seven of the twelve recognized Trematomus species. To reconstruct their evolutionary history, we employed comparative cytogenomics (BAC-FISH and chromosome painting) to reveal patterns of interspecific chromosomal orthologies across several notothenioid clades. RESULTS:We defined orthologous chromosomal segments of reference, termed Structural Units (SUs). SUs were identified in a total of 18 notothenioid species. We demonstrated for the first time that SUs were strongly conserved across every specimen examined, with chromosomal syntenies highlighting a paucity of intrachromosomal macro-rearrangements. Multiple independent fusions of these SUs were inferred in the Trematomus species, in contrast to the shared SU fusions in species of the sister lineage Notothenia. CONCLUSIONS:The SU segments were defined units of chromosomal rearrangement in the entire family Nototheiidae, which diverged from the other notothenioid families 20 My ago. Some of the identified chromosomal syntenies within the SUs were even conserved in their closest relatives, the family Eleginopsidae. Comparing the timing of acquisition of the fusions in the closely related genera Notothenia and Trematomus of the nototheniid species family, we conclude that they exhibit distinct chromosomal evolutionary histories, which may be relevant to different speciation scenarios.

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Comparative Analysis of the pIgR Gene from the Antarctic Teleost Trematomus bernacchii Reveals Distinctive Features of Cold-Adapted Notothenioidei

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