A dynamic evolutionary and functional landscape of plant phased small interfering RNAs

Abstract

BackgroundSecondary, phased small interfering RNAs (phasiRNAs) derived from protein-coding or noncoding loci (PHAS) are emerging as a new type of regulators of gene expression in plants. However, the evolution and function of these novel siRNAs in plant species remain largely unexplored.ResultsWe systematically analyzed PHAS loci in 23 plant species covering major phylogenetic groups spanning alga, moss, gymnosperm, basal angiosperm, monocot, and dicot. We identified over 3,300 PHAS loci, among which ~1,600 were protein-coding genes. Most of these PHAS loci were novel and clade- or species-specific and showed distinct expression patterns in association with particular development stages, viral infection, or abiotic stresses. Unexpectedly, numerous PHAS loci produced phasiRNAs from introns or exon–intron junction regions. Our comprehensive analysis suggests that phasiRNAs predominantly regulate protein-coding genes from which they are derived and genes from the same families of the phasiRNA-deriving genes, in contrast to the dominant trans-regulatory mode of miRNAs. The stochastic occurrence of many PHAS loci in the plant kingdom suggests their young evolutionary origins.ConclusionsOur study discovered an unprecedented diversity of protein-coding genes that produce phasiRNAs in a wide variety of plants, and set a kingdom-wide foundation for investigating the novel roles of phasiRNAs in shaping phenotype diversities of plants.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-015-0142-4) contains supplementary material, which is available to authorized users.

Most microRNAs in the single-cell alga Chlamydomonas reinhardtii are produced by Dicer-like 3-mediated cleavage of introns and untranslated regions of coding RNAs

“…A role under starvation of sulphate and/or phosphate is possible because these conditions affect sRNA profiles in Chlamydomonas (Shu and Hu 2012;Zheng et al 2015). The DCL3-dependent silencing might also act redundantly with other silencing systems as indicated by the loss of transposon silencing in C. reinhardtii that was dependent on loss of function at both DCL1 and of a histone methyltransferase (Casas-Mollano et al 2008).…”

Biogenesis of diverse plant phasiRNAs involves an miRNA-trigger and Dicer-processing

“…1). Recently, many types of phasiRNAs that are arranged at regular 21-, 22-, or 24-nt phased intervals have been identified in various plant species (International Brachypodium Initiative 2010; Johnson et al 2009; Xia et al 2015; Zhai et al 2011; Zheng et al 2015). Plant phasiRNA biogenesis generally involves 22-nt miRNA cleavage of a phasiRNA precursor RNA, dsRNA synthesis by RDR6, and processing by DCLs.…”

TAS3 miR390-dependent loci in non-vascular land plants: Towards a comprehensive reconstruction of the gene evolutionary history

“…These PHAS 63 loci include non-coding TAS genes and genes encoding penta-tricopeptide repeat-containing 64 proteins (PPRs), nucleotide-binding and leucine-rich repeat-containing proteins (NB-LRRs), or 65 MYB transcription factors (Allen and Howell, 2010; Zhai et al, 2011;Xia et al, 2013; Fei et al, 66 2013;Axtell, 2013;Yoshikawa, 2013;Zheng et al, 2015;Komiya, 2017;Liu et al, 2018; Deng 67 et al, 2018). Biogenesis of ta-siRNAs includes initial AGO-dependent miRNA binding at single Axtell, 2013;Fei et al, 2013;Zheng et al, 2015;Xia et al, 2013; de 82 Felippes et al, 2017;Komiya, 2017;Deng et al, 2018). Moreover, miR390 may additionally 83 target and inhibit protein-coding gene transcripts, such as StCDPK1 related to auxin-responsive 84 pathway (Santin et al, 2017).…”