The evolutionary puzzle solution for the origins of the partial loss of the Cτ2 exon in notothenioid fishes. Issue 116 (September 2021)

• Record Type: Journal Article
• Authors: Ametrano, Alessia; Gerdol, Marco; Vitale, Maria; Greco, Samuele; Oreste, Umberto; Coscia, Maria Rosaria
• Is Part Of: Fish & shellfish immunology. Issue 116(2021)
• Page Start: 124
• Page End: 139
• Publication Date: 2021-09
• Subjects: Teleost fish -- Notothenioidei -- Genome modifications -- IgT -- Exonic remnant -- Immunoglobulin domain -- Antarctic marine environment -- Molecular evolution; Ig Immunoglobulin -- Ig VH Immunoglobulin heavy chain Variable region -- Ig CH Immunoglobulin heavy chain Constant domain -- Cτ IgT heavy chain constant exon -- TbeL Trematomus bernacchii IgT heavy chain Long variant -- TbeS Trematomus bernacchii IgT heavy chain Short variant -- TbeSts Trematomus bernacchii IgT heavy chain Shortest variant; Fishes -- Immunology -- Periodicals; Shellfish -- Immunology -- Periodicals; Poissons -- Immunologie -- Périodiques; Crustacés -- Immunologie -- Périodiques; 571.9617
• DOI: 10.1016/j.fsi.2021.05.015
• Languages: English
• ISSNs: 1050-4648

Abstract

Abstract: Cryonotothenioidea is the main group of fishes that thrive in the extremely cold Antarctic environment, thanks to the acquisition of peculiar morphological, physiological and molecular adaptations. We have previously disclosed that IgM, the main immunoglobulin isotype in teleosts, display typical cold-adapted features. Recently, we have analyzed the gene encoding the heavy chain constant region (CH) of the IgT isotype from the Antarctic teleost Trematomus bernacchii (family Nototheniidae), characterized by the near-complete deletion of the CH2 domain. Here, we aimed to track the loss of the CH2 domain along notothenioid phylogeny and to identify its ancestral origins. To this end, we obtained the IgT gene sequences from several species belonging to the Antarctic families Nototheniidae, Bathydraconidae and Artedidraconidae. All species display a CH2 remnant of variable size, encoded by a short Cτ2 exon, which retains functional splicing sites and therefore is included in the mature transcript. We also considered representative species from the three non-Antarctic families: Eleginopsioidea ( Eleginops maclovinus ), Pseudaphritioidea ( Pseudaphritis urvillii ) and Bovichtidae ( Bovichtus diacanthus and Cottoperca gobio ). Even though only E. maclovinus, the sister taxa of Cryonotothenioidea, shared the partial loss of Cτ2, the other non-Antarctic notothenioid species displayed early molecular signatures of this event. These results shed light on the evolutionary path that underlies the origins of this remarkable gene structural modification. Graphical abstract: Image 1 Highlights: All analyzed cryonotothenioid species have an IgT gene with a Cτ2 exonic remnant. Conserved donor/acceptor splice sites allow the expression of the exonic remnant. The exon loss event took place prior to the radiation of Cryonotothenioidea. The exon loss is shared by the non-Antarctic sister lineage of Cryonotothenioidea. The nearly total loss of the Cτ 2 exon occurred in a stepwise mode.