Abstract
Trans-acting small interfering RNAs (ta-siRNAs) are transcribed from protein non-coding genomic TAS loci and belong to a plant-specific class of endogenous small RNAs. These siRNAs have been found to regulate gene expression in most taxa including seed plants, gymnosperms, ferns and mosses. In this study, bioinformatic and experimental PCR-based approaches were used as tools to analyze TAS3 and TAS6 loci in transcriptomes and genomic DNAs from representatives of evolutionary distant non-vascular plant taxa such as Bryophyta, Marchantiophyta and Anthocerotophyta. We revealed previously undiscovered TAS3 loci in plant classes Sphagnopsida and Anthocerotopsida, as well as TAS6 loci in Bryophyta classes Tetraphidiopsida, Polytrichopsida, Andreaeopsida and Takakiopsida. These data further unveil the evolutionary pathway of the miR390-dependent TAS3 loci in land plants. We also identified charophyte alga sequences coding for SUPPRESSOR OF GENE SILENCING 3 (SGS3), which is required for generation of ta-siRNAs in plants, and hypothesized that the appearance of TAS3-related sequences could take place at a very early step in evolutionary transition from charophyte algae to an earliest common ancestor of land plants.
Highlights
Plant chromosomal loci of trans-acting small interfering RNAs and microRNAs encode non-protein-coding and protein-coding precursor transcripts, which are synthesized by RNA polymerase II and include cap-structures and poly-(A) tails
Primary miRNA transcripts forming internal imperfect hairpins are processed by a protein complex including Dicer-like protein 1 (DCL1), HYL1 and SERRATE to give RNA duplexes with 2-nucleotide 3 -overhangs, which are terminally methylated by specific RNA methylase HEN1
The further process is dependent on plant RNA-dependent RNA polymerase 6 (RDR6) and SUPPRESSOR OF GENE SILENCING 3 (SGS3) proteins participating in the formation of dsRNA, which is cleaved in a sequential and phased manner by DCL4 with assistance of DRB4
Summary
Plant chromosomal loci of trans-acting small interfering RNAs (ta-siRNAs) and microRNAs (miRNAs) encode non-protein-coding and protein-coding precursor transcripts, which are synthesized by RNA polymerase II and include cap-structures and poly-(A) tails. Some specific microRNAs are able to initiate production of ta-siRNAs (and other secondary phased RNAs—phasiRNAs) by an step-by-step processing of long doublestranded RNA by DCL4 from a start point defined by miRNA-directed cleavage of a single-stranded RNA precursor in a ‘‘phased’’ pattern These PHAS loci include noncoding TAS genes and genes encoding penta-tricopeptide repeat-containing proteins (PPRs), nucleotide-binding and leucine-rich repeat-containing proteins (NB-LRRs), or MYB transcription factors (Allen & Howell, 2010; Zhai et al, 2011; Xia et al, 2013; Fei, Xia & Meyers, 2013; Axtell, 2013; Yoshikawa, 2013; Zheng et al, 2015; Komiya, 2017; Liu et al, 2018; Deng et al, 2018). The resulting ta-siRNAs (mostly of 21 bp in length), similar to miRNAs, are methylated by HEN1 protein (Allen & Howell, 2010; Axtell, 2013; Fei, Xia & Meyers, 2013; Yoshikawa, 2013; Bologna & Voinnet, 2014; Komiya, 2017; Deng et al, 2018)
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