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Specialization and evolution of endogenous small RNA pathways

Nature Reviews Genetics volume 8, pages 884–896 (2007)Cite this article

Key Points

  • Eukaryotes have evolved small-RNA-guided regulatory systems for the control of RNA transcripts, chromatin, genome content and invasive agents.

  • Specialized silencing systems evolved in eukaryotic lineages through proliferation and specialization of small-RNA biogenesis and effector factors.

  • Genomes spawn new types of RNA silencing triggers through sequence duplications, bidirectional transcription and evolution of self-complementary foldbacks

  • Amplification of endogenous silencing signals occurs by distinct secondary small interfering RNA (siRNA)-biogenesis mechanisms that involve RNA-dependent RNA polymerases in various lineages.

  • Plant genomes can spawn new microRNA (miRNA)-generating loci de novo by inverted duplication of protein-coding sequences followed by accommodation by the specialized miRNA-biogenesis apparatus through sequence drift

  • miRNA families expand through gene duplication, yielding sets of miRNAs with redundant, overlapping and specific functions. miRNA specialization within families can result from miRNA sequence differences and differential regulation of family members.

Abstract

The specificity of RNA silencing is conferred by small RNA guides that are processed from structured RNA or dsRNA. The core components for small RNA biogenesis and effector functions have proliferated and specialized in eukaryotic lineages, resulting in diversified pathways that control expression of endogenous and exogenous genes, invasive elements and viruses, and repeated sequences. Deployment of small RNA pathways for spatiotemporal regulation of the transcriptome has shaped the evolution of eukaryotic genomes and contributed to the complexity of multicellular organisms.

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Figure 1: Endogenous siRNA-generating loci.
Figure 2: Models for amplification of silencing signals in Caenorhabditis elegans and Arabidopsis thaliana.
Figure 3: RNA biogenesis in plants and animals.
Figure 4: Model for Piwi-interacting RNA (piRNA) biogenesis.
Figure 5: The chromatin-associated small interfering RNA (siRNA) pathway in Arabidopsis thaliana.
Figure 6: Models for genesis and evolution of microRNA (miRNA) loci in plants.
Figure 7: The three-fate model for the evolution of new microRNA (miRNA) loci in plants.

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Acknowledgements

We thank members of the Carrington laboratory for productive discussions. E.J.C. was supported in part by a P.F. and Nellie Buck Yerex Fellowship. Research in the J.C.C. laboratory was supported by grants from the US National Institutes of Health, the US National Science Foundation and the US Department of Agriculture.

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Authors and Affiliations

  1. Department of Biology, Myers Hall, 915 East Third Street, Indiana University, Bloomington, 47405, Indiana, USA

    Elisabeth J. Chapman

  2. Center for Genome Research and Biocomputing, 3021 ALS, Oregon State University, Corvallis, 97331, USA, Oregon

    James C. Carrington

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  1. Elisabeth J. Chapman
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Correspondence to James C. Carrington.

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DATABASES

Entrez-Gene

AGO4

DCL3

DCL2

DCL4

DRB4

RRF-1

RDR6

AGO7

TRBP

HYL1

AUB

AGO1

CSR-1

SAGO-1

SAGO-2

FWA

CUC2

SE

HEN1

FURTHER INFORMATION

The Carrington laboratory

Glossary

LINE1 (L1) elements

A class of self-replicating retrotransposons that are highly abundant in the human genome.

RISC

(RNA-induced silencing complex). An Argonaute proteinsmall RNA complex that inhibits translation of target RNAs through degradative or non-degradative mechanisms.

Transitivity

The spreading of silencing to regions that flank the original target sequence.

Hybrid dysgenesis

Descibes phenotypes that result from a high rate of mutation in germline cells of Drosophila melanogaster, triggered by P-element transposition.

Epiallele

An allele for which variable methylation or chromatin states confer heritable variable expression among individuals.

Cajal bodies

Nuclear bodies that are associated with the assembly of the gene expression machinery.

Genetic drift

Fluctuations in gene frequencies in a population due to chance.

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Chapman, E., Carrington, J. Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet 8, 884–896 (2007). https://doi.org/10.1038/nrg2179

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