Tian Y et al. (2019), Xenopus Interferon Complex: Inscribing the Amph...

XB-ART-56599

Cells 2019 Dec 26;91:. doi: 10.3390/cells9010067.

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Xenopus Interferon Complex: Inscribing the Amphibiotic Adaption and Species-Specific Pathogenic Pressure in Vertebrate Evolution?

Tian Y , Jennings J , Gong Y , Sang Y .

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Several recent studies have revealed previously unknown complexity of the amphibian interferon (IFN) system. Being unique in vertebrate animals, amphibians not only conserve and multiply the fish-like intron-containing IFN genes, but also rapidly evolve amniote-like intronless IFN genes in each tested species. We postulate that the amphibian IFN system confers an essential model to study vertebrate immune evolution in molecular and functional diversity to cope with unprecedented pathophysiological requirement during terrestrial adaption. Studies so far have ascribed a potential role of these IFNs in immune regulation against intracellular pathogens, particularly viruses; however, many knowledge gaps remain elusive. Based on recent reports about IFN's multifunctional properties in regulation of animal physiological and defense responses, we interpret that amphibian IFNs may evolve novel function pertinent to their superior molecular diversity. Such new function revealed by the emerging studies about antifungal and developmental regulation of amphibian IFNs will certainly promote our understanding of immune evolution in vertebrates to address current pathogenic threats causing amphibian decline.

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Species referenced: Xenopus laevis
Genes referenced: cope

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Figure 1. Schematic of vertebrate interferon (IFN) evolution and recent discovery about amphibian IFN complex. Evolutionary analyses were conducted in MEGA X [17]. The minimum evolution (ME) method was used to infer the molecular phylogeny, and the evolutionary distances were computed using the p-distance method, shown in the units of the number of amino acid differences per site. The ME tree was searched (search level of 1) using the close-neighbor-interchange (CNI) algorithm. The analysis used 108 amino acid sequences. All ambiguous positions were removed for each sequence pair. There was a total of 437 positions in the final dataset. In contrast to the previously known several fish-like intron-containing amphibian IFNs, recent studies revealed that amphibians are unique to have both fish-like intron-containing and amniotic intronless IFNs, which molecularly and immunologically stamp their amphibiotic position in vertebrate evolution [12,13,16]. Legends and Abbreviations: IFN-I, type I IFNs (including amniotic intronless IFNA, IFNB, IFNE, IFNK, IFNW, respectively, for the genes of IFN-Î±, -Î², -Îµ, -Îº, -Ï; and diverse amphibian intron-containing, XaIFN or XtIFN, and intronless XaIFNX or XtIFNX, listed here); IFN-III, type III IFNs (including amniotic intron-containing IFNL gene for IFN-Î»; and amphibian intron-containing XaIFNL or XtIFNL, and intronless XaIFNLX or XtIFNLX, listed here); SCCA 1, Scyliorhinus canicula (catshark) ancestral IFN-I; SCCA L, Scyliorhinus canicula (catshark) ancestral IFN-III; Dr, Danio rerio (zebrafish); Gg, Gallus gallus (chicken); Hs, Homo sapiens; Xa, Xenopus laevis; Xt, Xenopus tropicalis; Group designation: 1 and 7 & 8, intron-containing ancestral IFN-I (7 & 8) and IFN-III (1); 2, intron-containing IFN-III in amniotes; 3 and 4, amphibian intron-containing IFN-III (3) and IFN-I(4); 3X and 4X, intronless amphibian IFN-III (3X) and IFN-I (4X); 5X and 6X, intronless IFN-I in amniotes.

Figure 2. An updated model for antiviral IFN (IFN-I and IFN-III) gene evolution in vertebrates. The ancestral genes of three type of IFNs (IFN-I, -II, and -III) have been identified in cartilaginous fish. All fish IFN genes are intron-containing ones generally with four introns (or five exons) [12]. In contrast, amniotic IFN-I genes are generally intronless. Co-existence of multiple intronless and intron-containing IFN genes were only detected independently in different species of amphibians [12,13,14,15,16,50,51]. The current evidences support that at least two retroposition events might have happened in amphibians, at about 180.70 MYA (million years ago) in Xenopus and 87.57 MYA in N. parkeri, for example [12,13,14,15,16,50,51]. These two independent retroposition events might have occurred much later than the divergence between amphibians and amniotes (i.e., ~350 MYA, orange dot). Another retroposition event leading to intronless IFN orthologs in amniotes could also happen in accompaniment to loss of intron-containing IFN genes in reptiles; however, it could be unlikely if an orthologous relationship exists between different intronless amphibian IFNs with amniotic ones [12]. The emergence and expansion of intronless amphibian IFNs likely reflect the increasing evolution pressure (especially the air-borne pathogens and physiological requirement for terrestrial adaptation, shown with broad curve arrows) during the transition period, when vertebrates migrated from aquatic to terrestrial environments. Retroposition defines a reverse-transcription process of cellular mRNA and reintegration into the genome to enhance gene copying and evolution in molecular evolution. Compared to intronless IFN-I genes, one paradox in IFN evolution is why IFN-II and âIII genes conserve the ancestral gene structures, and do not show gene expansion even after few intronless IFN-III genes originated in amphibians and other amniotes. Solid or dashed black arrows: Indicating certain or uncertain orthologous relationships discovered, respectively.

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