Primary transcripts of microRNAs encode regulatory peptides

Abstract

MicroRNAs (miRNAs) are small regulatory RNA molecules that inhibit the expression of specific target genes by binding to and cleaving their messenger RNAs or otherwise inhibiting their translation into proteins. miRNAs are transcribed as much larger primary transcripts (pri-miRNAs), the function of which is not fully understood. Here we show that plant pri-miRNAs contain short open reading frame sequences that encode regulatory peptides. The pri-miR171b of Medicago truncatula and the pri-miR165a of Arabidopsis thaliana produce peptides, which we term miPEP171b and miPEP165a, respectively, that enhance the accumulation of their corresponding mature miRNAs, resulting in downregulation of target genes involved in root development. The mechanism of miRNA-encoded peptide (miPEP) action involves increasing transcription of the pri-miRNA. Five other pri-miRNAs of A. thaliana and M. truncatula encode active miPEPs, suggesting that miPEPs are widespread throughout the plant kingdom. Synthetic miPEP171b and miPEP165a peptides applied to plants specifically trigger the accumulation of miR171b and miR165a, leading to reduction of lateral root development and stimulation of main root growth, respectively, suggesting that miPEPs might have agronomical applications.

Hidden Peptides Encoded by Putative Noncoding RNAs

“…1C) (Ambros, 2004;Bartel, 2004;Lauressergues et al, 2015). These RNA molecules are generated in both animals and plants by the same enzyme, RNA polymerase II (RNAPII), that mediates the synthesis of protein-coding mRNAs, and they are modified with a 5' cap and 3' polyadenylate tail.…”

The use of high-throughput sequencing methods for plant microRNA research

“…Although their biogenesis and action modes have been well depicted, 8,9 new features are being uncovered and added onto the miRNAs encoded by the precursors encompassing stem-loop structures. 10,11 Research on the discovery and the regulatory activities of the miRNA species will be greatly accelerated by integrative use of diverse sequencing approaches developed from HTS platform. In this review, we introduced several HTS methods valuable for plant miRNA studies, including RNA-seq, RNA-PET-seq, sRNA-seq, dsRNA-seq, ssRNA-seq and degradome-seq.…”

“…By increasing the transcription of the primiRNAs, the miRNA-encoded peptides (miPEPs) enhance the accumulation of the corresponding mature miRNAs, resulting in the down-regulation of the target genes. 10 Thus, the above discovery refreshed our traditional view that the "junk" regions of the miRNA precursors could play a coding role. 11 Considering the sequence features of the miRNAs, and the huge sRNA population existing in plants, 12 high-throughput approaches are desired for cloning, characterization and quantification of the miRNA genes.…”

“…Notably, a more complicated case was recently discovered for the "non-coding" pri-miRNAs in plant. Lauressergues and his colleagues 10 showed that several plant pri-miRNAs (such as primiR171b of Medicago truncatula and pri-miR165a of Arabidopsis thaliana) contained short open reading frame sequences encoding regulatory peptides. By increasing the transcription of the primiRNAs, the miRNA-encoded peptides (miPEPs) enhance the accumulation of the corresponding mature miRNAs, resulting in the down-regulation of the target genes.…”

Requirement of MIR165A primary transcript sequence for its activity pattern in Arabidopsis leaf primordia

“…The primary transcripts of MIRNA genes have been thought to be localized mainly in nucleus and are processed by DCL1. Recently, Lauressergues and co-authors 12 reported that some MIRNA primary transcripts encode short peptides, call miPEPs, and that these miPEPs have a role in enhancing transcription of their own primary transcripts. They also showed that the pri-miR165a is predicted to be translated into miPEP165a, which is composed of 18 amino acid residues, proposing that the pri-miR165a is exported form nucleus to cytoplasm.…”