The Major Adult α-Globin Gene of Antarctic Teleosts and Its Remnants in the Hemoglobinless Icefishes

Abstract

The icefishes of the Southern Ocean (family Channichthyidae, suborder Notothenioidei) are unique among vertebrates in their inability to synthesize hemoglobin. We have shown previously (Cocca, E., Ratnayake-Lecamwasam, M., Parker, S. K., Camardella, L., Ciaramella, M., di Prisco, G., and Detrich, H. W., III (1995) Proc. Natl. Acad. Sci. U. S. A. 92, 1817-1821) that icefishes retain inactive genomic remnants of adult notothenioid ␣-globin genes but have lost the gene that encodes adult ␤-globin. Here we demonstrate that loss of expression of the major adult ␣-globin, ␣1, in two species of icefish (Chaenocephalus aceratus and Chionodraco rastrospinosus) results from truncation of the 5 end of the notothenioid ␣1-globin gene. The wild-type, functional ␣1-globin gene of the Antarctic yellowbelly rockcod, Notothenia coriiceps, contains three exons and two A ؉ T-rich introns, and its expression may be controlled by two or three distinct promoters. Retained in both icefish genomes are a portion of intron 2, exon 3, and the 3-untranslated region of the notothenioid ␣1-globin gene. The residual, nonfunctional ␣-globin gene, no longer under positive selection pressure for expression, has apparently undergone random mutational drift at an estimated rate of 0.12-0.33%/million years. We propose that abrogation of hemoglobin synthesis in icefishes most likely resulted from a single mutational event in the ancestral channichthyid that deleted the entire ␤-globin gene and the 5 end of the linked ␣1-globin gene.

The Functionally Distinct Hemoglobins of the Arctic Spotted Wolffish Anarhichas minor

“…The characterization of gene clusters and the study of their organization and expression in the genome and of their regulation mediated by promoters and/or enhancers are important future developments, which will take advantage of the wealth of information available on the globin genes of cold-adapted Antarctic fish (47,48). In addition to the implications on cold adaptation, this study is offering an excellent model (i.e.…”

Molecular structure and functional adaptations of hemoglobins from Antarctic marine organisms

“…We have previously shown (Cocea et al, 1995(Cocea et al, , 1997b) that three of the 15 species of channichthyids (Chaenocephalus aceratus, Chionodraco rastrospinosus, and Champsocephalus gunnari) retain inactive genomic remnants of adult notothenioid oc-globin gene but have lost the gene that encodes adult β globin. Loss of expression of adult α globin in two closely related species from the Antarctica Peninsula, C. aceratus and C. rastrospinosus, results from truncation of the 5' end of the adult a-globin gene, an evolutionary event that must have occurred in an ancestral channichthyid (Zhao et al, 1998).…”

Antarctic notothenioid fish: what are the future consequences of ‘losses’ and ‘gains’ acquired during long-term evolution at cold and stable temperatures?

“…3). All 16 species within the Channichthyidae family lack the Hb protein as a consequence of a multi-step mutational process that has resulted in loss of the β-globin gene and partial omission of the α-globin gene from the αβ-globin complex, thereby rendering the locus functionally inactive (Cocca et al, 1995;Zhao et al, 1998;di Prisco et al, 2002;Near et al, 2006). Interestingly, one of the 16 icefish species, the phylogenetically derived Neopagetopsis ionah, retains a complete, although non-functional, αβ-globin complex that is similar to the ancestral condition seen in Hb-expressing species from the sister family Bathydraconidae (Near et al, 2006).…”