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Genetic and Functional Diversification of Small RNA Pathways in Plants [1]

['Zhixin Xie', 'Center For Gene Research', 'Biotechnology', 'Department Of Botany', 'Plant Pathology', 'Oregon State University', 'Corvallis', 'Oregon', 'United States Of America', 'Lisa K Johansen']

Date: 2023-08 

Multicellular eukaryotes produce small RNA molecules (approximately 21–24 nucleotides) of two general types, microRNA (miRNA) and short interfering RNA (siRNA). They collectively function as sequence-specific guides to silence or regulate genes, transposons, and viruses and to modify chromatin and genome structure. Formation or activity of small RNAs requires factors belonging to gene families that encode DICER (or DICER-LIKE [DCL]) and ARGONAUTE proteins and, in the case of some siRNAs, RNA-dependent RNA polymerase (RDR) proteins. Unlike many animals, plants encode multiple DCL and RDR proteins. Using a series of insertion mutants of Arabidopsis thaliana, unique functions for three DCL proteins in miRNA (DCL1), endogenous siRNA (DCL3), and viral siRNA (DCL2) biogenesis were identified. One RDR protein (RDR2) was required for all endogenous siRNAs analyzed. The loss of endogenous siRNA in dcl3 and rdr2 mutants was associated with loss of heterochromatic marks and increased transcript accumulation at some loci. Defects in siRNA-generation activity in response to turnip crinkle virus in dcl2 mutant plants correlated with increased virus susceptibility. We conclude that proliferation and diversification of DCL and RDR genes during evolution of plants contributed to specialization of small RNA-directed pathways for development, chromatin structure, and defense.

Copyright: © 2004 Xie et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Using a genetic approach, we show here the existence of three small RNA-generating pathways with unique requirements in Arabidopsis. Plants with point mutations or insertions in several members of the DCL and RDR gene families were examined. The data indicate that plants genetically diversified several factors involved in formation of functionally distinct small RNAs.

Eukaryotic small RNAs of approximately 21–24 nucleotides function as guide molecules in a remarkably wide range of biological processes, including developmental timing and patterning, formation of heterochromatin, genome rearrangement, and antiviral defense ( Carrington and Ambros 2003 ; Finnegan and Matzke 2003 ; Lai 2003 ). They belong to at least two general classes, microRNA (miRNA) and short interfering RNA (siRNA). miRNAs (approximately 21–22 nucleotides) are found in plants and animals and are often phylogenically conserved within their respective kingdoms. They arise from non-protein-coding genes through formation of a precursor transcript followed by one or more nucleolytic processing steps ( Lai 2003 ). Part of the precursor adopts a fold-back structure that interacts with a multidomain RNaseIII-like enzyme termed DICER or DICER-LIKE (DCL1 in Arabidopsis), which catalyzes accurate excision of the mature miRNA ( Denli and Hannon 2003 ). The miRNAs then associate with ribonucleoprotein complexes that function to negatively regulate target genes controlling a range of developmental events, such as timing of cell fate decisions, stem cell maintenance, apoptosis, organ morphogenesis and identity, and polarity ( Ambros 2003 ; Carrington and Ambros 2003 ).

Results

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[1] Url: https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.0020104

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