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Title: Expansion of amphibian intronless interferons revises the paradigm for interferon evolution and functional diversity

Author
item SANG, YONGMING - Kansas State University
item LIU, QINFANG - Kansas State University
item LEE, JINHWA - Kansas State University
item MA, WENJUN - Kansas State University
item McVey, David
item BLECHA, FRANK - Kansas State University

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/14/2016
Publication Date: 6/30/2016
Citation: Sang, Y., Liu, Q., Lee, J., Ma, W., Mcvey, D.S., Blecha, F. 2016. Expansion of amphibian intronless interferons revises the paradigm for interferon evolution and functional diversity. Nature Communications. 6(29072):1-17.

Interpretive Summary: Our identification of the coexistence and expansion of intronless IFNs in frogs revises the previous evolution model of antiviral IFNs in vertebrates in several aspects (Fig. 12 versus Fig. 1). Significant conclusions of these studies were: 1) the emergence of intronless IFNs occurred in amphibians before reptiles; 2) the coexistence of intron-containing IFN progenitors and expansion of intronless IFNs emphasizes the uniqueness of amphibians in evolutionary immunology; and 3) the most complicated IFN system (in both molecular types and total numbers of IFNs compared with other species) evolved in amphibians. This seems a surprise but should not be unexpected, which may partly reflect the most dramatic lifestyle revolution during vertebrate evolution, i.e. leaving water to adapt to terrestrial environments. Interestingly, amphibian intronless IFNs have less similarity than their intron-containing IFNs to the intronless type I IFNs in birds or mammals, indicating that the emergence and expansion of intronless IFNs in amphibians may not be an evolutionary continuum (but an independent bifurcation) leading to intronless IFNs that dominate in amniotes. It is likely that they shared the same origin but differed independently thereafter in frogs and other ammiotes species. Previously, type III IFNs identified in all vertebrate species primarily conserved their intron-containing gene structures.

Technical Abstract: Interferons (IFNs) are key cytokines identified in vertebrates, and evolutionary dominance of intronless IFN genes in amniotes is a signature event in IFN evolution. For the first time, we show that the emergence and expansion of intronless IFN genes is evident in amphibians, shown by 24-37 intronless IFN genes in each frog species. Amphibian IFNs represent a molecular complex more complicated than those in other vertebrate species, which revises the established model of IFN evolution to facilitate re-inspection of IFN molecular and functional diversity. We identified these intronless amphibian IFNs and their intron-containing progenitors, and functionally characterized constitutive/inductive expression and antimicrobial roles in infections caused by zoonotic pathogens, such as influenza viruses and Listeria monocytogenes. Amphibians therefore, may serve as overlooked vectors/hosts for zoonotic pathogens, and amphibian IFN system provides a model to study IFN evolution in molecular and functional diversity in coping with dramatic environmental changes during terrestrial adaption.