“…Until now, miPEPs have been shown to be encoded by the first open reading frame (miORF) after the transcription start site (TSS) located in the 5 0 region of the pri-miRNA and they enhance pri-miRNA transcription from which they originate (Lauressergues et al, 2015;Sharma et al, 2020;Chen et al, 2020). Initially characterized in Arabidopsis thaliana, Medicago truncatula, and Glycine max (Lauressergues et al, 2015;Couzigou et al, 2016Couzigou et al, , 2017, recent studies revealed the presence of miPEPs in other plant species (Chen et al, 2020;Zhang et al, 2020;Ormancey et al, 2021) and even in animals (Kang et al, 2020;Niu et al, 2020;Prel et al, 2021;Montigny et al, 2021;Immarigeon et al, 2021). This suggests that the number of miPEPs is probably far to be fully determined, and that miPEPs might be a common feature in both plant and animal kingdoms.…”
MicroRNAs (miRNAs) are transcribed as long primary transcripts (pri-miRNAs) by RNA polymerase II. Plant pri-miRNAs encode regulatory peptides called miPEPs, which specifically enhance the transcription of the pri-miRNA from which they originate. However, paradoxically, whereas miPEPs have been identified in different plant species, they are poorly conserved, raising the question of the mechanisms underlying their specificity. To address this point, we identify and re-annotate multiple Arabidopsis thaliana pri-miRNAs in order to identify ORF encoding miPEPs. The study of several identified miPEPs in different species show that non-conserved miPEPs are only active in their plant of origin, whereas conserved ones are active in different species. Finally, we find that miPEP activity relies on the presence of its own miORF, explaining both the lack of selection pressure on miPEP sequence and the ability for non-conserved peptides to play a similar role, i.e., to activate the expression of their corresponding miRNA.
“…Until now, miPEPs have been shown to be encoded by the first open reading frame (miORF) after the transcription start site (TSS) located in the 5 0 region of the pri-miRNA and they enhance pri-miRNA transcription from which they originate (Lauressergues et al, 2015;Sharma et al, 2020;Chen et al, 2020). Initially characterized in Arabidopsis thaliana, Medicago truncatula, and Glycine max (Lauressergues et al, 2015;Couzigou et al, 2016Couzigou et al, , 2017, recent studies revealed the presence of miPEPs in other plant species (Chen et al, 2020;Zhang et al, 2020;Ormancey et al, 2021) and even in animals (Kang et al, 2020;Niu et al, 2020;Prel et al, 2021;Montigny et al, 2021;Immarigeon et al, 2021). This suggests that the number of miPEPs is probably far to be fully determined, and that miPEPs might be a common feature in both plant and animal kingdoms.…”
MicroRNAs (miRNAs) are transcribed as long primary transcripts (pri-miRNAs) by RNA polymerase II. Plant pri-miRNAs encode regulatory peptides called miPEPs, which specifically enhance the transcription of the pri-miRNA from which they originate. However, paradoxically, whereas miPEPs have been identified in different plant species, they are poorly conserved, raising the question of the mechanisms underlying their specificity. To address this point, we identify and re-annotate multiple Arabidopsis thaliana pri-miRNAs in order to identify ORF encoding miPEPs. The study of several identified miPEPs in different species show that non-conserved miPEPs are only active in their plant of origin, whereas conserved ones are active in different species. Finally, we find that miPEP activity relies on the presence of its own miORF, explaining both the lack of selection pressure on miPEP sequence and the ability for non-conserved peptides to play a similar role, i.e., to activate the expression of their corresponding miRNA.
“…The first step consisted of identifying A. thaliana pri‐miRNAs, by crossing the data from EST sequences ( www.ncbi.nlm.nih.gov/genbank/ ), Illumina RNA‐seq data (Wang et al ., 2019 ) and RACE‐PCR data (Xie et al ., 2005 ). Several examples previously established that the first ORF after the transcription start site corresponded to a translated ORF coding a miPEP able to increase pri‐miRNA expression (Chen et al ., 2020 ; Couzigou et al ., 2016 , 2017 ; Lauressergues et al ., 2015 ; Sharma et al ., 2020 ; Zhang et al ., 2020 ). Therefore, we selected the first ORF of each identified pri‐miRNA as a high confident candidate to produce functional miPEPs and synthesized the 87 miPEPs corresponding to the 87 conserved A. thaliana miRNAs, from miR156a to miR399f.…”
“…D and E : Insensitivity of miR-8 sensor to miPEP-8 over-expression in S2 transfected cells (n=16) (D) or in wing imaginal discs when miPEP-8 is expressed under the ptc -GAL4 promoter (E). In D, a miR-8 construct (n=12) [17] was used as a positive control repressing the miR-8 luciferase sensor [20]. Of note, pri-miR-8 (n=21) also repressed the miR-8 luciferase sensor.…”
Section: Resultsmentioning
confidence: 99%
“…In plants, miPEPs specifically increase transcription of their primary transcript impacting the level of the mature miR produced and consequently affecting the control of the entire miR Gene Regulatory Network (GRN). To date, this regulation has been extended to several miRs in various plants [14–17]. In human cells, only few reports present evidences of pri-miR translation [18–21].…”
Background: In the last decades, genome-wide studies of many species have revealed the existence of a myriad of RNAs differing in size, coding potential and function. Among these are the long non-coding RNAs (lncRNAs), some of them producing functional small peptides via the translation of short ORFs (sORFs). It now appears that any kind of RNA presumably has a potential to encode small peptides. Accordingly, our team recently discovered that plant primary transcripts of microRNAs (pri-miRNAs) produce small regulatory peptides (miPEPs) involved in auto-regulatory feedback loops enhancing their cognate microRNA expression which in turn controls plant development. Here we investigate whether this regulatory feedback loop is conserved in Drosophila melanogaster.
Results: We performed a survey of ribosome profiling data and revealed that many pri-miRNAs exhibit ribosome translation marks. Focusing on miR-8, we showed that pri-miR-8 can produce a miPEP-8. Functional assays performed in Drosophila revealed that miPEP-8 affects development when over-expressed or knocked down. Combining genetic and molecular approaches as well as genome-wide transcriptomic analyses, we showed that miR-8 expression is independent of miPEP-8 activity and that miPEP-8 acts in parallel of miR-8 to regulate the expression of hundreds of genes.
Conclusion: Taken together, these results reveal that several Drosophila pri-miRNAs exhibit translation potential. Contrasting with the mechanism described in plants, these data shed light on the function of yet un-described microRNA encoded peptides in Drosophila and their regulatory potential on genome expression.
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