The evolution of RNAs with multiple functions

Dinger, Marcel E., Gascoigne, Dennis K. and Mattick, John S. (2011) The evolution of RNAs with multiple functions. Biochimie, 93 11: 2013-2018. doi:10.1016/j.biochi.2011.07.018

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Author Dinger, Marcel E.
Gascoigne, Dennis K.
Mattick, John S.
Title The evolution of RNAs with multiple functions
Journal name Biochimie   Check publisher's open access policy
ISSN 0300-9084
Publication date 2011-11-01
Sub-type Article (original research)
DOI 10.1016/j.biochi.2011.07.018
Open Access Status File (Author Post-print)
Volume 93
Issue 11
Start page 2013
End page 2018
Total pages 6
Place of publication Cedex, France
Publisher Elsevier Masson
Language eng
Formatted abstract
Increasing numbers of transcripts have been reported to transmit both protein-coding and regulatory information. Apart from challenging our conception of the gene, this observation raises the question as to what extent this phenomenon occurs across the genome and how and why such dual encoding of function has evolved in the eukaryotic genome. To address this question, we consider the evolutionary path of genes in the earliest forms of life on Earth, where it is generally regarded that proteins evolved from a cellular machinery based entirely within RNA. This led to the domination of protein-coding genes in the genomes of microorganisms, although it is likely that RNA never lost its other capacities and functionalities, as evidenced by cis-acting riboswitches and UTRs. On the basis that the subsequent evolution of a more sophisticated regulatory architecture to provide higher levels of epigenetic control and accurate spatiotemporal expression in developmentally complex organisms is a complicated task, we hypothesize: (i) that mRNAs have been and remain subject to secondary selection to provide trans-acting regulatory capability in parallel with protein-coding functions; (ii) that some and perhaps many protein-coding loci, possibly as a consequence of gene duplication, have lost protein-coding functions en route to acquiring more sophisticated trans-regulatory functions; (iii) that many transcripts have become subject to secondary processing to release different products; and (iv) that novel proteins have emerged within loci that previously evolved functionality as regulatory RNAs. In support of the idea that there is a dynamic flux between different types of informational RNAs in both evolutionary and real time, we review recent observations that have arisen from transcriptomic surveys of complex eukaryotes and reconsider how these observations impact on the notion that apparently discrete loci may express transcripts with more than one function. In conclusion, we posit that many eukaryotic loci have evolved the capacity to transact a multitude of overlapping and potentially independent functions as both regulatory and protein-coding RNAs.
Keyword Dual functional RNAs
Long noncoding RNAs
Evolution of genes
Origin of new genes
Complex loci
Q-Index Code C1
Q-Index Status Confirmed Code
Institutional Status UQ

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