The evolution of controlled multitasked gene networks: The role of introns and other noncoding RNAs in the development of complex organisms

Mattick, J. S. and Gagen, M. J. (2001) The evolution of controlled multitasked gene networks: The role of introns and other noncoding RNAs in the development of complex organisms. Molecular Biology and Evolution, 18 9: 1611-1630. doi:10.1093/oxfordjournals.molbev.a003951


Author Mattick, J. S.
Gagen, M. J.
Title The evolution of controlled multitasked gene networks: The role of introns and other noncoding RNAs in the development of complex organisms
Journal name Molecular Biology and Evolution   Check publisher's open access policy
ISSN 0737-4038
Publication date 2001-01-01
Sub-type Critical review of research, literature review, critical commentary
DOI 10.1093/oxfordjournals.molbev.a003951
Open Access Status Not yet assessed
Volume 18
Issue 9
Start page 1611
End page 1630
Total pages 20
Publisher Society for Molecular Biology and Evolution
Language eng
Subject 1105 Ecology, Evolution, Behavior and Systematics
1312 Molecular Biology
1311 Genetics
Abstract Eukaryotic phenotypic diversity arises from multitasking of a core proteome of limited size. Multitasking is routine in computers, as well as in other sophisticated information systems, and requires multiple inputs and outputs to control and integrate network activity. Higher eukaryotes have a mosaic gene structure with a dual output, mRNA (protein-coding) sequences and introns, which are released from the pre-mRNA by posttranscriptional processing. Introns have been enormously successful as a class of sequences and comprise up to 95% of the primary transcripts of protein-coding genes in mammals. In addition, many other transcripts (perhaps more than half) do not encode proteins at all, but appear both to be developmentally regulated and to have genetic function. We suggest that these RNAs (eRNAs) have evolved to function as endogenous network control molecules which enable direct gene-gene communication and multitasking of eukaryotic genomes. Analysis of a range of complex genetic phenomena in which RNA is involved or implicated, including co-suppression, transgene silencing, RNA interference, imprinting, methylation, and transvection, suggests that a higher-order regulatory system based on RNA signals operates in the higher eukaryotes and involves chromatin remodeling as well as other RNA-DNA, RNA-RNA, and RNA-protein interactions. The evolution of densely connected gene networks would be expected to result in a relatively stable core proteome due to the multiple reuse of components, implying that cellular differentiation and phenotypic variation in the higher eukaryotes results primarily from variation in the control architecture. Thus, network integration and multitasking using trans-acting RNA molecules produced in parallel with protein-coding sequences may underpin both the evolution of developmentally sophisticated multicellular organisms and the rapid expansion of phenotypic complexity into uncontested environments such as those initiated in the Cambrian radiation and those seen after major extinction events.
Keyword Complexity
Evolution
Genetic programming
Introns
Noncoding RNA
RNAi
Q-Index Code C1
Q-Index Status Provisional Code
Institutional Status UQ

Document type: Journal Article
Sub-type: Critical review of research, literature review, critical commentary
Collection: Scopus Import
 
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Created: Fri, 22 Dec 2017, 10:39:20 EST