Transcription polymerase-catalyzed emergence of novel RNA replicons

Transcription polymerases can exhibit an unusual mode of regenerating certain RNA templates from RNA, yielding systems that can replicate and evolve with RNA as the information carrier. Two classes of pathogenic RNAs (hepatitis delta virus in animals and viroids in plants) are copied by host transcr...

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Published inScience (American Association for the Advancement of Science) Vol. 368; no. 6487
Main Authors Jain, Nimit, Blauch, Lucas R, Szymanski, Michal R, Das, Rhiju, Tang, Sindy K Y, Yin, Y Whitney, Fire, Andrew Z
Format Journal Article
LanguageEnglish
Published United States The American Association for the Advancement of Science 10.04.2020
Subjects
Biocatalysis
Bioinformatics
Deoxyribonucleic acid
DNA
DNA-Directed RNA Polymerases - metabolism
Genetics
Hepatitis
Hepatitis delta virus
Microfluidics
Replicon
Ribonucleic acid
RNA
RNA - biosynthesis
RNA polymerase
Seeds
Transcription
Transcription, Genetic
Vector-borne diseases
Viral Proteins - metabolism
Viruses
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Summary:Transcription polymerases can exhibit an unusual mode of regenerating certain RNA templates from RNA, yielding systems that can replicate and evolve with RNA as the information carrier. Two classes of pathogenic RNAs (hepatitis delta virus in animals and viroids in plants) are copied by host transcription polymerases. Using in vitro RNA replication by the transcription polymerase of T7 bacteriophage as an experimental model, we identify hundreds of new replicating RNAs, define three mechanistic hallmarks of replication (subterminal de novo initiation, RNA shape-shifting, and interrupted rolling-circle synthesis), and describe emergence from DNA seeds as a mechanism for the origin of novel RNA replicons. These results inform models for the origins and replication of naturally occurring RNA genetic elements and suggest a means by which diverse RNA populations could be propagated as hereditary material in cellular contexts.
Bibliography:Author contributions: N.J. and A.Z.F. conceived the study; N.J., A.Z.F., L.R.B., M.R.S., Y.W.Y., S.K.Y.T. and R.D. designed experiments; N.J., L.R.B. and M.R.S. performed experiments; N.J. performed data analysis; N.J. and A.Z.F. wrote the manuscript with inputs from all authors.
ISSN:0036-8075
1095-9203
DOI:10.1126/science.aay0688