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The poly(A) polymerase PAPS1 interacts with the RNA-directed DNA methylation pathway in sporophyte and pollen development [small RNA]

ABSTRACT: RNA-based processes play key roles in the regulation of eukaryotic gene expression. This includes both the processing of pre-mRNAs into mature mRNAs ready for translation and RNA-based silencing processes, such as RNA-directed DNA methylation (RdDM). Polyadenylation of pre-mRNAs is one important step in their processing and is carried out by three functionally specialized canonical nuclear poly(A) polymerases in Arabidopsis thaliana. Null-mutations in one of these, termed PAPS1, result in a male gametophytic defect. Using a fluorescence-labelling strategy, we have characterized this defect in more detail using RNA and small-RNA sequencing. In addition to global defects in expression of pollen-differentiation genes, paps1 null mutant pollen show a strong overaccumulation of transposable-element transcripts, yet a depletion of 21- and particularly 24-nucleotide long short interfering RNAs (siRNAs) and microRNAs (miRNAs) targeting the corresponding transposable elements. Double-mutant analyses support a specific functional interaction between PAPS1 and components of the RdDM pathway, as evident from strong synergistic phenotypes in mutant combinations involving paps1, but not paps2 paps4 mutations. In particular, the double mutant of paps1 and rna-dependent rna polymerase 6 (rdr6) shows a synergistic developmental phenotype disrupting the formation of the transmitting tract in the female gynoecium. Thus, our findings in A. Thaliana uncover a potentially general link between canonical poly(A) polymerases as components of mRNA processing and RdDM, reflecting an analogous interaction in fission yeast.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE127992 | GEO | 2019/12/31

REPOSITORIES: GEO

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The poly(A) polymerase PAPS1 interacts with the RNA-directed DNA methylation pathway in sporophyte and pollen development [RNA-seq]

Project description:RNA-based processes play key roles in the regulation of eukaryotic gene expression. This includes both the processing of pre-mRNAs into mature mRNAs ready for translation and RNA-based silencing processes, such as RNA-directed DNA methylation (RdDM). Polyadenylation of pre-mRNAs is one important step in their processing and is carried out by three functionally specialized canonical nuclear poly(A) polymerases in Arabidopsis thaliana. Null-mutations in one of these, termed PAPS1, result in a male gametophytic defect. Using a fluorescence-labelling strategy, we have characterized this defect in more detail using RNA and small-RNA sequencing. In addition to global defects in expression of pollen-differentiation genes, paps1 null mutant pollen show a strong overaccumulation of transposable-element transcripts, yet a depletion of 21- and particularly 24-nucleotide long short interfering RNAs (siRNAs) and microRNAs (miRNAs) targeting the corresponding transposable elements. Double-mutant analyses support a specific functional interaction between PAPS1 and components of the RdDM pathway, as evident from strong synergistic phenotypes in mutant combinations involving paps1, but not paps2 paps4 mutations. In particular, the double mutant of paps1 and rna-dependent rna polymerase 6 (rdr6) shows a synergistic developmental phenotype disrupting the formation of the transmitting tract in the female gynoecium. Thus, our findings in A. Thaliana uncover a potentially general link between canonical poly(A) polymerases as components of mRNA processing and RdDM, reflecting an analogous interaction in fission yeast.

2019-12-31 | GSE127991 | GEO

Transcriptomic analyses to estimated poly(A)-tail lengths in paps1-1 mutant pollen tubes

Project description:Polyadenylation of mRNAs is critical for their export from the nucleus, stability and efficient translation. The Arabidopsis thaliana genome encodes three isoforms of canonical nuclear poly(A) polymerase (PAPS) that redundantly polyadenylate the bulk of pre-mRNAs. However, their distinct mutant phenotypes and transcriptome studies have indicated that subsets of pre-mRNAs are preferentially polyadenylated by either PAPS1 or the two very similar PAPS2 and PAPS4 proteins. Such functional specialization raises the possibility of modulating the balance of activities between the isoforms to alter poly(A) lengths of sets of transcripts, providing an additional level of gene-expression control in plants. Here we test this notion by studying the function of PAPS1 in pollen-tube growth and guidance. Pollen tubes growing through female tissue acquire the competence to find ovules efficiently and upregulate PAPS1 expression more strongly than in vitro grown pollen tubes. Using the temperature-sensitive paps1-1 allele we show that PAPS1 activity during pollen-tube growth is required for full acquisition of competence, resulting in inefficient fertilization by paps1-1 mutant pollen tubes. While these mutant pollen tubes germinate and grow at the same rates as wild-type pollen tubes, they are compromised in locating the micropyles of ovules. Transcriptomic analyses indicate that previously identified competence-associated genes are less expressed in paps1-1 mutant than in wild-type pollen tubes. Estimating the poly(A)-tail lengths of transcripts in mutant and wild-type pollen tubes suggests that polyadenylation by PAPS1 is associated with reduced transcript abundance. Our results therefore suggest that PAPS1 upregulation during pollen-tube growth through the style plays a key role in the acquisition of competence and support the notion that plants can modulate the balance of activity between PAPS isoforms to regulate gene expression.

2023-02-21 | GSE207509 | GEO

Transcriptomic analyzes of paps1 pollen tube/style complexes

2023-02-21 | GSE207285 | GEO

Genome-wide analysis of PAPS1-dependent polyadenylation identifies novel roles for functionally specialized poly(A) polymerases in Arabidopsis thaliana

Project description:The poly(A) tail at 3' ends of eukaryotic mRNAs promotes their nuclear export, stability and translational efficiency, and changes in its length can strongly impact gene expression. The Arabidopsis thaliana genome encodes three canonical nuclear poly(A) polymerases, PAPS1, PAPS2 and PAPS4. As shown by their different mutant phenotypes, these three isoforms are functionally specialized, with PAPS1 modifying organ growth and suppressing a constitutive immune response. However, the molecular basis of this specialization is largely unknown. Here, we have estimated poly(A)-tail lengths on a transcriptome-wide scale in wild-type and paps1 mutants. This identified categories of genes as particularly strongly affected in paps1 mutants, including genes encoding ribosomal proteins, cell-division factors and major carbohydrate-metabolic proteins. We experimentally verified two novel functions of PAPS1 in ribosome biogenesis and redox homoeostasis that were predicted based on the analysis of poly(A)-tail length changes in paps1 mutants. When overlaying the PAPS1-dependent effects observed here with coexpression analysis based on independent microarray data, the two clusters of transcripts that are most closely coexpressed with PAPS1 show the strongest change in poly(A)-tail length and transcript abundance in paps1 mutants in our analysis. This suggests that their coexpression reflects at least partly the preferential polyadenylation of these transcripts by PAPS1 versus the other two poly(A)-polymerase isoforms. Thus, transcriptomewide analysis of poly(A)-tail lengths identifies novel biological functions and likely target transcripts for polyadenylation by PAPS1. Data integration with large-scale coexpression data suggests that changes in the relative activities of the isoforms are used as an endogenous mechanism to co-ordinately modulate plant gene expression. Analysing long and short poly(A)-tail fractions from 4 paps1 mutant and 4 Ler samples.

2015-07-30 | E-GEOD-57690 | biostudies-arrayexpress

RIP-seq of the Arabidopsis mRNA export mutant aly1 and associated controls.

Project description:RNA-directed DNA methylation (RdDM) is a set of mechanisms by which transcriptionally-repressive DNA methylation and histone modifications are targeted de novo to transposable element and transgene regions of the genome. We identified a mutant in which all forms of RdDM are deficient, leading to the transcriptional activation of some transposable elements and the complete inability to initiate transgene silencing. The mutated gene, ALY1, encodes an RNA-binding nuclear export protein belonging to a family of four ALY proteins in Arabidopsis. ALY proteins function together to export a large number of mRNAs from the nucleus for translation, but we found that ALY1 is unique in its ability to enable RdDM. We sequenced methylomes (via MethylC-seq) to identify the genome-wide loss of CHH methylation targeted by RdDM in aly1 mutants. We sequenced small RNAs and determined that ALY1 functions in RdDM downstream of small RNA production and export. We sequenced total, nuclear and cytoplasmic mRNAs to determine that ALY1 functions in the nuclear export directly or indirectly on 2,612 mRNAs. Additionally, we sequenced RNAs bound to the ALY1 protein using RNA-immunoprecipitation followed by high throughput sequencing.

2019-05-15 | GSE123648 | GEO

Transcriptome of the Arabidopsis mRNA export mutant aly1 and associated controls

2019-05-15 | GSE118708 | GEO

Small RNA-seq of the Arabidopsis mRNA export mutant aly1 and associated controls

2019-05-15 | GSE118705 | GEO

Methylome of the Arabidopsis mRNA export mutant aly1 and associated controls

2019-05-15 | GSE118695 | GEO

Genome-wide analysis of PAPS1-dependent polyadenylation identifies novel roles for functionally specialized poly(A) polymerases in Arabidopsis thaliana

2015-07-30 | GSE57690 | GEO

DNA Topoisomerase 1a Promotes RNA-directed DNA Methylation and Histone Lysine 9 Dimethylation at Transposable Elements in Arabidopsis [RNA-Seq]

Project description:RNA-directed DNA methylation (RdDM) is a transcriptional silencing mechanism mediated by small and long noncoding RNAs produced by the plant-specific RNA polymerases Pol IV and Pol V, respectively. Through a chemical genetics screen with a luciferase-based DNA methylation reporter, LUCL, we found that camptothecin, a compound with anti-cancer properties that targets DNA topoisomerase 1a (TOP1a) was able to de-repress LUCL by reducing its DNA methylation and H3K9 dimethylation (H3K9me2) levels. Further studies with Arabidopsis top1a mutants showed that TOP1a promotes RdDM by facilitating the production of Pol V-dependent long non-coding RNAs, AGONAUTE4 recruitment and H3K9me2 deposition at transposable elements (TEs). 5 small RNA libraries were sequenced

2014-07-08 | E-GEOD-50719 | biostudies-arrayexpress

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