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  • Review Article
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The expanding world of small RNAs in plants

Key Points

  • Functional diversification and expansion of silencing pathways in plants relies on duplication of DICER-LIKE proteins (DCLs) and ARGONAUTE proteins (AGOs).

  • The main small-RNA classes in plants are microRNAs (miRNAs), 21–22-nucleotide secondary siRNAs and 24-nucleotide heterochromatic siRNAs (hetsiRNAs).

  • All small RNAs in plants are modified at their 3′-end by 2′-O-methylation, including miRNAs, which lack this modification in animals. This modification confers stability and protection from degradation.

  • Plant miRNAs are mainly involved in post-transcriptional gene silencing (PTGS) by transcript cleavage or translational repression, and also trigger secondary siRNA production from RNA polymerase II (Pol II) transcripts.

  • Secondary small RNAs of 21 and 22 nucleotides in length are involved in cleavage or translational repression of target transcripts in cis and in trans. They are also able to initiate TGS by establishing DNA methylation at particular loci.

  • The majority of siRNAs in plants are 24-nucleotide hetsiRNAs and are involved in silencing repeats and transposable elements by RNA-directed DNA methylation (RdDM).

  • Small RNAs in plants are involved in reproductive transitions, including meiosis and gametogenesis, and regulate important epigenetic mechanisms such as genomic imprinting and paramutation.

Abstract

Plant genomes encode various small RNAs that function in distinct, yet overlapping, genetic and epigenetic silencing pathways. However, the abundance and diversity of small-RNA classes varies among plant species, suggesting coevolution between environmental adaptations and gene-silencing mechanisms. Biogenesis of small RNAs in plants is well understood, but we are just beginning to uncover their intricate regulation and activity. Here, we discuss the biogenesis of plant small RNAs, such as microRNAs, secondary siRNAs and heterochromatic siRNAs, and their diverse cellular and developmental functions, including in reproductive transitions, genomic imprinting and paramutation. We also discuss the diversification of small-RNA-directed silencing pathways through the expansion of RNA-dependent RNA polymerases, DICER proteins and ARGONAUTE proteins.

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Figure 1: Main pathways for biogenesis of endogenous small RNAs in plants.
Figure 2: 2′-O-methylation, uridylation and degradation of microRNAs (miRNAs) in Arabidopsis thaliana.
Figure 3: Triggers of secondary siRNA biogenesis.
Figure 4: The transition from post-transcriptional gene silencing (PTGS) to TGS in transgenes, epialleles and active transposons.
Figure 5: Small-RNA functions in meiosis and cell fate specification.

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Acknowledgements

The authors thank J.-S. Parent for critically reading the manuscript, and all the members of the Martienssen laboratory for discussions. Research in the Martienssen laboratory is supported by the US National Institutes of Health (NIH) grant R01 GM067014 and by the Howard Hughes Medical Institute and Gordon and Betty Moore Foundation Plant Biology Investigator Program.

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Glossary

DICER-LIKE proteins

(DCLs). Plant orthologues of other eukaryotic ribonuclease III Dicer enzymes; required for small-RNA processing.

ARGONAUTE proteins

(AGOs). The main effector proteins of gene silencing, which bind to small-RNA duplexes and promote small-RNA-mediated target recognition and cleavage.

Paramutation

An inter-chromosomal sensing mechanism that initiates heritable epigenetic changes in trans. Small RNAs are often involved in this process by mediating RNA-directed DNA methylation.

PIWI-interacting RNAs

(piRNAs). Members of a large class of small RNAs produced in animal cells that form functional silencing complexes by loading onto PIWI proteins. piRNA complexes are mainly involved in the post-transcriptional gene silencing of retrotransposons in the germ line.

RNA-induced silencing complexes

Protein complexes that include Argonaute proteins and small RNAs. The small RNAs hybridize to complementary arget RNAs, which then undergo cleavage or translational repression, or recruit other factors such as chromatin modifiers.

Exosome

A multi-protein complex involved in 3′–5′ degradation of RNA molecules such as mRNAs or ribosomal RNAs.

Processing bodies

(P-bodies). Cytoplasmic foci that have essential roles in most mRNA-decay mechanisms, including decapping and nonsense-mediated decay, as well as in storing processed mRNAs to postpone their translation.

siRNA-bodies

Cytoplasmic foci in plant cells, at which RNA-DEPENDENT RNA POLYMERASE 6 (RDR6) and SUPPRESSOR OF GENE SILENCING 3 (SGS3) synthesize double-stranded RNA from single-stranded RNA.

Epiallele

A genetic locus at which transcriptional activity is regulated by epigenetic silencing marks, such as DNA methylation and histone modification.

Interspecific allopolyploids

Polyploid organisms with two or more sets of genetically distinct chromosomes, resulting from crosses between different species.

Intraspecific hybrids

Genetically divergent plants from the same species.

Introgression lines

Populations containing genetic material derived from similar species or wild relatives, generally produced through successive backcrossing and selection of single introgressed genomic segments from one of the parental lines.

Transgressive phenotypes

Phenotypes in a hybrid progeny that are either superior or inferior to both parents. Transgressive phenotypes might facilitate hybrid specialization and are particularly important in crops when hybrid yields are higher than those of each parent.

Wide crosses

Crosses of related species or genera that naturally do not sexually reproduce with each other.

Apomixis

The natural ability of certain plant species to reproduce asexually through seed, producing offspring that are genetically identical to the parent plant

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Borges, F., Martienssen, R. The expanding world of small RNAs in plants. Nat Rev Mol Cell Biol 16, 727–741 (2015). https://doi.org/10.1038/nrm4085

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