MicroRNA Superfamilies Descended from miR390 and Their Roles in Secondary Small Interfering RNA Biogenesis in Eudicots

Abstract

Trans-acting small interfering RNAs (tasiRNAs) are a major class of small RNAs performing essential biological functions in plants. The first reported tasiRNA pathway, that of miR173-TAS1/2, produces tasiRNAs regulating a set of pentatricopeptide repeat (PPR) genes and has been characterized only in Arabidopsis thaliana to date. Here, we demonstrate that the microRNA (miRNA)-trans-acting small interfering RNA gene (TAS)-pentatricopeptide repeat-containing gene (PPR)-small interfering RNA pathway is a highly dynamic and widespread feature of eudicots. Nine eudicot plants, representing six different plant families, have evolved similar tasiRNA pathways to initiate phased small interfering RNA (phasiRNA) production from PPR genes. The PPR phasiRNA production is triggered by different 22-nucleotide miRNAs, including miR7122, miR1509, and fvePPRtri1/2, and through distinct mechanistic strategies exploiting miRNA direct targeting or indirect targeting through TASlike genes (TASL), one-hit or two-hit, or even two layers of tasiRNA-TASL interactions. Intriguingly, although those miRNA triggers display high sequence divergence caused by the occurrence of frequent point mutations and splicing shifts, their corresponding MIRNA genes show pronounced identity to the Arabidopsis MIR173, implying a common origin of this group of miRNAs (super-miR7122). Further analyses reveal that super-miR7122 may have evolved from a newly defined miR4376 superfamily, which probably originated from the widely conserved miR390. The elucidation of this evolutionary path expands our understanding of the course of miRNA evolution, especially for relatively conserved miRNA families.

Novel and Recently Evolved MicroRNA Clusters Regulate Expansive F-BOX Gene Networks through Phased Small Interfering RNAs in Wild Diploid Strawberry

“…7B; Supplemental Table S8) leading to phasiRNAs, some of which target transcripts from cognate MYB genes. Copies of fve-MIR11285a/b (previously named as fve-PPRtri1/2) were described to target PPR genes directly or via cleavage of an intergenic noncoding locus named as a TAS-LIKE gene (TASL; Xia et al, 2013). This was confirmed by our PARE data, and the ensuing phasiRNAs were detected in many small RNA libraries (Fig.…”

“…Three major conserved tasiRNA pathways have been characterized in plants; their biogenesis is initiated by three distinct miRNAs: miR390, miR828, and the miR7122 superfamilies (Fei et al, 2013;Xia et al, 2013). All three tasiRNA pathways are also found in F. vesca (Fig.…”

“…Recently, genome-wide small RNA sequencing and analyses of an ever-expanding number of plant species have revealed the production of 21-nucleotide secondary small interfering RNAs (siRNAs) from hundreds of genes through a mechanism like tasiRNAs. These siRNAs may function in trans (tasiRNAs) or in cis (cis-acting siRNAs) to cleave their target genes (Johnson et al, 2009;Zhai et al, 2011;Xia et al, 2012Xia et al, , 2013Fei et al, 2013). Collectively, these tasiRNAs and cis-acting siRNAs, which are produced via progressive 21-nucleotide cleavage from the trigger miRNA cleavage site, are termed phased small interfering RNAs (phasiRNAs).…”

“…Accordingly, phasiRNA-producing loci are termed PHAS loci (Zhai et al, 2011). In dicots, phasiRNAs have been found to be generated from and presumably to regulate large and conserved gene families such as those coding for the NUCLEOTIDE-BINDING AND LEUCINE-RICH REPEAT (NB-LRR) proteins, MYB transcription factors, and PENTATRICOPEPTIDE REPEAT (PPR) proteins (Zhai et al, 2011;Xia et al, 2012Xia et al, , 2013. The vast phasiRNA networks in higher plant genomes are just beginning to be recognized and discovered, and the functional roles of these phasiRNA networks are yet to be illuminated.…”

Sample sequencing of vascular plants demonstrates widespread conservation and divergence of microRNAs

“…5), eight of these corresponding to known tasiRNA triggers, including miR167 (ref. 27), the miR472/ 482/2118 superfamily 16,28 , and the miR7122 and the related miR4376/1432/391 superfamilies 29 . Interestingly, a prevalence of 22-nucleotide species was also observed for miR479, whose Figure 3 | Sequence abundance and conservation across Tracheophyta species.…”