Structural analysis of 3’UTRs in insect flaviviruses reveals novel determinants of sfRNA biogenesis and provides new insights into flavivirus evolution

Andrii Slonchak (), Rhys Parry, Brody Pullinger, Julian D. J. Sng, Xiaohui Wang, Teresa F. Buck, Francisco J. Torres, Jessica J. Harrison, Agathe M. G. Colmant, Jody Hobson-Peters, Roy A. Hall, Andrew Tuplin and Alexander A. Khromykh ()
Additional contact information
Andrii Slonchak: University of Queensland
Rhys Parry: University of Queensland
Brody Pullinger: University of Queensland
Julian D. J. Sng: University of Queensland
Xiaohui Wang: University of Queensland
Teresa F. Buck: University of Queensland
Francisco J. Torres: University of Queensland
Jessica J. Harrison: University of Queensland
Agathe M. G. Colmant: University of Queensland
Jody Hobson-Peters: University of Queensland
Roy A. Hall: University of Queensland
Andrew Tuplin: University of Leeds
Alexander A. Khromykh: University of Queensland

Nature Communications, 2022, vol. 13, issue 1, 1-16

Abstract: Abstract Subgenomic flaviviral RNAs (sfRNAs) are virus-derived noncoding RNAs produced by pathogenic mosquito-borne flaviviruses (MBF) to counteract the host antiviral response. To date, the ability of non-pathogenic flaviviruses to produce and utilise sfRNAs remains largely unexplored, and it is unclear what role XRN1 resistance plays in flavivirus evolution and host adaptation. Herein the production of sfRNAs by several insect-specific flaviviruses (ISFs) that replicate exclusively in mosquitoes is shown, and the secondary structures of their complete 3’UTRs are determined. The xrRNAs responsible for the biogenesis of ISF sfRNAs are also identified, and the role of these sfRNAs in virus replication is demonstrated. We demonstrate that 3’UTRs of all classical ISFs, except Anopheles spp-asscoaited viruses, and of the dual-host associated ISF Binjari virus contain duplicated xrRNAs. We also reveal novel structural elements in the 3’UTRs of dual host-associated and Anopheles-associated classical ISFs. Structure-based phylogenetic analysis demonstrates that xrRNAs identified in Anopheles spp-associated ISF are likely ancestral to xrRNAs of ISFs and MBFs. In addition, our data provide evidence that duplicated xrRNAs are selected in the evolution of flaviviruses to provide functional redundancy, which preserves the production of sfRNAs if one of the structures is disabled by mutations or misfolding.

Date: 2022
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DOI: 10.1038/s41467-022-28977-3

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