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NOT2 proteins promote Pol II-dependent transcription and interact with multiple miRNA biogenesis factors in Arabidopsis

ABSTRACT: MicroRNAs (miRNAs) play key regulatory roles in numerous developmental and physiological processes in animals and plants. The elaborate mechanism of miRNA biogenesis involves transcription and multiple processing steps. Here, we report the identification of a pair of evolutionarily conserved NOT2_3_5 domain containing proteins, NOT2a and NOT2b (previously known as At-NOT2 and VIP2, respectively), as components involved in Arabidopsis miRNA biogenesis. NOT2 was identified by its interaction with the Piwi/Ago/Zwille (PAZ) domain of Dicer-like 1 (DCL1), an interaction that is conserved between rice and Arabidopsis. Inactivation of both NOT2 genes in Arabidopsis caused severe defects in male gametophytes, and weak lines show pleiotropic defects reminiscent of miRNA pathway mutants. Impairment of NOT2s decreases the accumulation of pri-miRNAs and mature miRNAs and increases DCL1-containing nuclear speckle number in vivo. In addition, NOT2b protein interacts with Pol II and other miRNA processing factors including two cap-binding proteins, CBP80/ABH1, CBP20 and SERRATE (SE). Therefore, these results suggest that NOT2 proteins promote MIR transcription and facilitate efficient DCL1 recruitment in Arabidopsis.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE42901 | GEO | 2013/01/30

SECONDARY ACCESSION(S): PRJNA183795

REPOSITORIES: GEO

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NOT2 proteins promote Pol II-dependent transcription and interact with multiple miRNA biogenesis factors in Arabidopsis

Project description:MicroRNAs (miRNAs) play key regulatory roles in numerous developmental and physiological processes in animals and plants. The elaborate mechanism of miRNA biogenesis involves transcription and multiple processing steps. Here, we report the identification of a pair of evolutionarily conserved NOT2_3_5 domain containing proteins, NOT2a and NOT2b (previously known as At-NOT2 and VIP2, respectively), as components involved in Arabidopsis miRNA biogenesis. NOT2 was identified by its interaction with the Piwi/Ago/Zwille (PAZ) domain of Dicer-like 1 (DCL1), an interaction that is conserved between rice and Arabidopsis. Inactivation of both NOT2 genes in Arabidopsis caused severe defects in male gametophytes, and weak lines show pleiotropic defects reminiscent of miRNA pathway mutants. Impairment of NOT2s decreases the accumulation of pri-miRNAs and mature miRNAs and increases DCL1-containing nuclear speckle number in vivo. In addition, NOT2b protein interacts with Pol II and other miRNA processing factors including two cap-binding proteins, CBP80/ABH1, CBP20 and SERRATE (SE). Therefore, these results suggest that NOT2 proteins promote MIR transcription and facilitate efficient DCL1 recruitment in Arabidopsis. Examination of transcriptome of not2 and wild type by RNA-seq.

2013-01-30 | E-GEOD-42901 | biostudies-arrayexpress

Dual roles of the nuclear cap binding complex and SERRATE in pre-mRNA splicing and microRNA processing in Arabidopsis

Project description:The processing of Arabidopsis thaliana microRNAs (miRNAs) from longer primary transcripts (pri-miRNAs) requires the activity of several proteins, including DICER-LIKE1 (DCL1), the double stranded RNA binding protein HYPONASTIC LEAVES1 (HYL1), and the zinc finger protein SERRATE (SE). It has been noted before that the morphological appearance of weak se mutants is reminiscent of plants with mutations in ABH1/CBP80 and CBP20, which encode the two subunits of the nuclear cap-binding complex. We report that, like SE, the cap-binding complex is necessary for proper processing of pri-miRNAs. Inactivation of either ABH1/CBP80 or CBP20 results in decreased levels of mature miRNAs accompanied by increased levels of pri-miRNAs. Whole genome tiling array analyses reveal that se, abh1/cbp80 and cbp20 mutants also share similar pre-mRNA splicing defects, leading to the accumulation of many partially spliced transcripts. This is unlikely to be an indirect consequence of improper miRNA processing or other mRNA turnover pathways, since introns retained in se, abh1/cbp80 and cbp20 mutants are not affected by mutations in other genes required for miRNA processing or for non-sense-mediated mRNA decay. Taken together, our results uncover dual roles in splicing and miRNA processing that distinguish SE and the cap-binding complex from specialized miRNA processing factors such as DCL1 and HYL1. Keywords: Tiling array analysis of RNA populations from wild type, se, abh1 and cbp20 mutants

2008-05-01 | GSE11043 | GEO

SMA1, a homolog of the splicing factor Prp28, has a multifaceted role in miRNA biogenesis in Arabidopsis

Project description:MicroRNAs (miRNAs) are a class of small non-coding RNAs that repress gene expression. In plants, the RNase III enzyme Dicer-like (DCL1) processes primary miRNAs (pri-miRNAs) into miRNAs. Here, we show that SMALL1 (SMA1), a homolog of the DEAD-box pre-mRNA splicing factor Prp28, plays essential roles in miRNA biogenesis in Arabidopsis. A hypomorphic sma1-1 mutation causes growth defects and reduces miRNA accumulation correlated with increased target transcript levels. SMA1 interacts with the DCL1 complex and positively influences pri-miRNA processing. Moreover, SMA1 binds the promoter region of genes encoding pri-miRNAs (MIRs) and is required for MIR transcription. Furthermore, SMA1 also enhances the abundance of the DCL1 protein levels through promoting the splicing of the DCL1 pre-mRNAs. Collectively, our data provide new insights into the function of SMA1/Prp28 in regulating miRNA abundance in plants.

2018-06-09 | GSE114073 | GEO

Spliceosome disassembly factors ILP1 and NTR1 promote microRNA biogenesis in Arabidopsis

Project description:A battery of spliceosome-associated proteins has been identified in microRNA (miRNA) biogenesis; however, the underlying mechanisms remain elusive. The intron lariat spliceosome (ILS) complex is highly conserved among eukaryotes and its disassembly marks the end of a canonical splicing cycle. In this study, we show that two conserved disassembly factors of the ILS complex, ILP1 and NTR1, positively regulate microRNA biogenesis through facilitating transcriptional elongation in Arabidopsis. ILP1 and NTR1 form a stable complex and co-regulate alternative splicing of more than a hundred genes across the genome including the core circadian gene LHY and some pri-miRNAs. Dysfunction in either ILP1 or NTR1 result in reduced RNA polymerase II occupancy at elongated regions of MIR chromatins, without affecting MIR promoter activity, pri-miRNA decay and DCL1 processing. Our results provide insights into the molecular mechanisms of spliceosomal machineries in non-coding RNA regulation.

2019-11-12 | PXD011542 | Pride

Coordinated regulation of Arabidopsis microRNA biogenesis and red light signaling through Dicer-like 1 and phytochrome-interacting factor 4

Project description:Light and microRNAs (miRNAs) are key external and internal signals for plant development respectively. However the relationship between light signaling and miRNA biogenesis pathways remains unknown. Here we found that miRNA processer DCL1/HYL1 interacts with a basic helix–loop–helix (bHLH) transcription factor, phytochrome-interacting factor 4 (PIF4), which mediates the destabilization of DCL1 during dark-red light transition. PIF4 acts as a transcription factor for some miRNA genes and is necessary for the proper accumulation of miRNAs. DCL1/HYL1 and mature miRNAs play roles in the regulation of plant hypocotyl growth. These results uncovered a previously unknown crosstalk between miRNA biogenesis and red light signaling through the PIF4-dependent regulation of miRNA transcription and processing to affect red light-directed plant photomorhogenesis.

2018-02-27 | GSE109038 | GEO

RACK1 function in the miRNA pathway

Project description:MicroRNAs (miRNAs) regulate plant development by post-transcriptional regulation of target genes. In Arabidopsis thaliana, DCL1 processes precursors (pri-miRNAs) to miRNA duplexes, which associate with AGO1. Additional proteins act in concert with DCL1 (e.g. HYL1 and SERRATE) or AGO1, respectively, to facilitate efficient and precise pri-miRNA processing and miRNA loading. In this study, we show that the accumulation of plant microRNAs depends on RECEPTOR FOR ACTIVATED C KINASE 1 (RACK1), a scaffold protein found in all higher eukaryotes. miRNA levels are reduced in rack1 mutants and our data suggest that RACK1 affects the microRNA pathway via several distinct mechanisms involving direct interactions with known microRNA factors: RACK1 ensures the accumulation and processing of some pri-miRNAs, directly interacts with SERRATE and is part of an AGO1 complex. As a result, mutations in RACK1 lead to misregulation of miRNA target genes, which is important for ABA responses and phyllotaxy. In conclusion, our study discovered complex functioning of RACK1 proteins in the Arabidopsis miRNA pathway, which are important for miRNA production and therefore plant development.

2013-07-01 | GSE40579 | GEO

RACK1 function in the miRNA pathway

Project description:MicroRNAs (miRNAs) regulate different aspects of plant development by post-transcriptional regulation of target genes. In Arabidopsis, DICER-LIKE 1 (DCL1) processes miRNA precursors (pri-miRNAs) to miRNA duplexes, which associate with ARGONAUTE 1 (AGO1). AGO1 together with the miRNA guide strand binds complementary RNA sequences within target mRNAs. Additional proteins act in concert with DCL1 (e.g. HYL1 and SERRATE) and AGO1, respectively, to facilitate efficient and precise pri-miRNA processing and loading into the effector protein. Here, we show that RECEPTOR OF ACTIVATED C KINASE 1 (RACK1) is a novel component of the Arabidopsis miRNA pathway. RACK1 is a seven-bladed WD-repeat protein that has previously been shown to act as a scaffold protein mediating multiple simultaneous protein-protein interactions. Our molecular analyses demonstrate that RACK1 function is required for controlling miRNA-mediated gene expression. rack1 mutants contain only low levels of mature miRNAs without affecting the first step of pri-miRNA processing. Physical and genetic interaction studies revealed that RACK1 acts in concert with AGO1 and also interacts with a SERRATE, a component of the miRNA processing machinery. These results suggest that RACK1 also functions as a scaffold protein in the miRNA pathway to orchestrates miRNA maturation steps after the initial events of pri-miRNA processing. sequencing of small RNAs from WT and rack1abc mutants (two biological replicates each)

2013-07-01 | E-GEOD-40579 | biostudies-arrayexpress

A Role for the RNA-Binding Protein MOS2 in MicroRNA Maturation in Arabidopsis

Project description:microRNAs (miRNAs) play important roles in the regulation of gene expression. In Arabidopsis, mature miRNAs are processed from primary miRNA transcripts (pri-miRNAs) by nuclear HYL1/SE/DCL1 complexes that form Dicing bodies (D-bodies). Here we report that a RNA-binding protein MOS2 bound to pri-miRNAs and was required for their efficient processing. MOS2 did not interact with HYL1, SE, and DCL1 and was not localized in D-bodies. Interestingly, in the absence of MOS2, the recruitment of pri-miRNAs by HYL1 was greatly reduced and the localization of HYL1 in D-bodies was compromised. These data suggest that MOS2 facilitates pri-miRNA processing through facilitating the recruitment of pri-miRNAs by the Dicing complexes.

2012-10-27 | GSE41843 | GEO

Global effects of the small RNA biogenesis machinery on the Arabidopsis thaliana transcriptome

Project description:In Arabidopsis thaliana, four different DICER-LIKE (DCL) proteins have distinct, but partially overlapping functions in the biogenesis of microRNAs (miRNAs) and small interfering RNAs (siRNAs) from longer, non-coding precursor RNAs. To analyze the impact of different components of the small RNA (sRNA) biogenesis machinery on the transcriptome, we subjected dcl and other mutants impaired in sRNA biogenesis to whole-genome tiling array analysis. We compared both protein-coding genes and noncoding transcripts, including most pri-miRNAs, in two tissues and several stress conditions. We discovered distinct effects of dcl1, hyl1 and se mutations on the transcriptome, as well as a number of common genes affected in dcl1 and dcl2 dcl3 dcl4 triple mutants. Our results furthermore suggest that the DCL1 is not only involved in miRNA action, but can also contribute to silencing of certain transposons, apparently through an effect on DNA methylation. Together, our findings contribute to the knowledge of both specialization and overlap between different RNA silencing pathways.

2010-05-08 | GSE21685 | GEO

Small RNAs in Arabidopsis hyl1 and hyl1 suppressor mutants

Project description:DCL1 and HYL1 are the core components of miRNA biogenesis machinery. hyl1-null mutants accumulate low levels of miRNAs and cause pleiotropic morphological phenotypes. Here, we reported that we identified 5 new alleles of DCL1 which are able to suppress the hyl1 morphological phenotypes and restore the miRNA accumulation level in hyl1 plants. These new alleles are located in the helicase and RNaseIIIa domains of DCL1, highlighting the critical functions of these domains. Biochemical analyses of these suppressors indicated that they process pri-miRNA more efficiently, with both higher Kcat and lower Km values. In addition, we investigated the functions of the DCL1 helicase domain. Our results indicated that the helicase domain is able to modulate the DCL1 processing activities. Based on these results, we proposed that HYL1 might exert its function through interaction with the DCL1 helicase domain. Small RNA sequencing from hyl1 and select hyl1/dcl1 suppressor mutants confirms thats suppression of the hyl1 phenotype is due to an increase in the accumulation, but not the precision, of miRNAs in the suppressor mutants. Wild-type, hyl1-2, hyl1-2/dcl1-20, and hyl1-2/dcl1-21 plants were sampled from both rosette leaves and flowers.

2012-04-24 | E-GEOD-29802 | biostudies-arrayexpress

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