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Long-distance transport of siRNAs with functional roles in pollen development [sRNA-seq]

ABSTRACT: Small interfering RNAs (siRNAs) play a crucial role in plant reproduction, yet their mobility and function remain incompletely understood. We report that a large proportion of siRNAs found in pollen of Capsella rubella relies on mobile siRNAs from maternal sporophytic tissues, highlighting the importance of non-cell-autonomous siRNAs in male gametophyte development. Unlike tapetal siRNAs, which guide DNA methylation and require CLASSY3 and DNA-dependent RNA polymerase IV (Pol IV) activity in the tapetum, we found that Pol IV-dependent mobile siRNAs (PMsiRNAs) mainly function post-transcriptionally and do not guide DNA methylation. Nevertheless, PMsiRNAs share key features with tapetal siRNAs, including Pol IV dependency, clustering and a size range of 21–24 nucleotides. Using a grafting approach, we show that sporophytic Pol IV-dependent siRNAs act as non-cell-autonomous mobile signals that trigger PMsiRNA formation through post-transcriptional gene silencing. This process parallels reproductive phased siRNA biogenesis, which is widespread across angiosperms but has been considered absent in Brassicaceae. Loss of PMsiRNAs causes pollen arrest, underscoring their essential role. Together, these findings highlight siRNAs as long-distance communication signals from maternal sporophytic tissues to the male gametophyte with critical functions in developmental regulation.

ORGANISM(S): Capsella rubella

PROVIDER: GSE291578 | GEO | 2026/02/02

REPOSITORIES: GEO

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Long-distance transport of siRNAs with functional roles in pollen development [RNA-seq]

Project description:Small interfering RNAs (siRNAs) play a crucial role in plant reproduction, yet their mobility and function remain incompletely understood. We report that a large proportion of siRNAs found in pollen of Capsella rubella relies on mobile siRNAs from maternal sporophytic tissues, highlighting the importance of non-cell-autonomous siRNAs in male gametophyte development. Unlike tapetal siRNAs, which guide DNA methylation and require CLASSY3 and DNA-dependent RNA polymerase IV (Pol IV) activity in the tapetum, we found that Pol IV-dependent mobile siRNAs (PMsiRNAs) mainly function post-transcriptionally and do not guide DNA methylation. Nevertheless, PMsiRNAs share key features with tapetal siRNAs, including Pol IV dependency, clustering and a size range of 21–24 nucleotides. Using a grafting approach, we show that sporophytic Pol IV-dependent siRNAs act as non-cell-autonomous mobile signals that trigger PMsiRNA formation through post-transcriptional gene silencing. This process parallels reproductive phased siRNA biogenesis, which is widespread across angiosperms but has been considered absent in Brassicaceae. Loss of PMsiRNAs causes pollen arrest, underscoring their essential role. Together, these findings highlight siRNAs as long-distance communication signals from maternal sporophytic tissues to the male gametophyte with critical functions in developmental regulation.

2026-02-02 | GSE291577 | GEO

Long-distance transport of siRNAs with functional roles in pollen development [BiSulfite-seq]

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Polymerase IV Plays a Crucial Role in Pollen Development in Capsella

Project description:In Arabidopsis thaliana, DNA-dependent RNA polymerase IV (Pol IV) is required for the formation of transposable element (TE)-derived small RNA (sRNA) transcripts. These transcripts are processed by DICER-LIKE3 into 24-nt small interfering RNAs (siRNAs) that guide RNA-directed DNA methylation. In the pollen grain, Pol IV is also required for the accumulation of 21/22-nt epigenetically activated siRNAs (easiRNAs), which likely silence TEs via post-transcriptional mechanisms. Despite this proposed role of Pol IV, its loss of function in Arabidopsis does not cause a discernable pollen defect. Here, we show that the knockout of NRPD1, encoding the largest subunit of Pol IV in the Brassicaceae species Capsella rubella, caused post-meiotic arrest of pollen development at the microspore stage. As in Arabidopsis, all TE-derived siRNAs were 2 depleted in Capsella nrpd1 microspores. In the wild-type background, the same TEs produced 21/22-nt and 24-nt siRNAs; these processes required Pol IV activity. Arrest of Capsella nrpd1 microspores was accompanied by the deregulation of genes targeted by Pol IV-dependent siRNAs. TEs were much closer to genes in Capsella rubella compared to Arabidopsis thaliana, perhaps explaining the essential role of Pol IV in pollen development in Capsella. Our discovery that Pol IV is functionally required in Capsella microspores emphasizes the relevance of investigating different plant models.

2020-01-23 | GSE136847 | GEO

CLSY docking to Pol IV requires a conserved domain critical for small RNA biogenesis and transposon silencing

Project description:RNA polymerase IV (Pol IV) transcribes transposable elements (TEs) into precursors for small interfering RNAs (siRNAs) that guide DNA methylation to silence these potentially dangerious mobile elements in plants. Pol IV is recruited to TEs via SNF2-like CLASSY (CLSY) proteins. How Pol IV evolved to partner with the CLSYs is unknown. Using phylogenetics, we identified a conserved CYC-YPMF motif that is specific to Pol IV’s largest subunit. Modeling predicts that this motif coordinates a zinc ion and is exposed near Pol IV’s surface in a domain contacting downstream DNA. Via immunoprecipitation and mass spectrometry we found that this motif is essential for the association of all four CLSYs with Pol IV and hereby designate it as a CLSY-docking motif. Consistent with these biochemical results, mutations in the CLSY-docking motif or in neighboring sites of the Pol IV clamp domain, phenocopy pol iv null mutants and display a near-total loss of siRNA biogenesis, resulting in defects in DNA methylation and TE silencing. Together, our findings provide structural and functional insights into a critical protein feature that distinguishes Pol IV from other RNA polymerases, allowing Pol IV to target, transcribe and limit the expression of TE regions, thereby protecting genome integrity.

2024-11-28 | PXD047743 | Pride

Separated Transcriptomes of Male Gametophyte and Tapetum in Rice

Project description:In flowering plants, the male gametophyte, the pollen, develops in the anther. Complex patterns of gene expression in both the gametophytic and sporophytic tissues of the anther regulate this process. The gene expression profiles of the microspore/pollen and the sporophytic tapetum are of particular interest. In this study, a microarray technique combined with laser microdissection (44K LM-microarray) was developed and used to characterize separately the transcriptomes of the microspore/pollen and tapetum in rice. Expression profiles of 11 known tapetum specific-genes were consistent with previous reports. Based on the spatiotemporal expression patterns and gene ontology (GO) categories of anther-expressed genes, some noteworthy expression patterns are discussed in connection with various important biological events of anther development.

2011-05-12 | GSE29217 | GEO

Arabidopsis RNA Polymerase IV generates 21-22 nucleotide small RNAs that can participate in RNA-directed DNA methylation and may regulate genes

Project description:Canonically, Arabidopsis RNA Polymerase IV (Pol IV) is known to produce heterochromatic small RNAs (typically 23-24 nucleotide in length) that maintain silencing of transposable elements (TEs). In contrast, when TEs are transcriptionally activated and produce Pol II transcripts, these transcripts are degraded into 21-22 nt small RNAs (sRNAs) known to participate in post transcriptional gene silencing. Recently, it was reported that Pol IV can also produce 21-22 nt sRNAs in pollen. We investigated the mechanism of Pol IV dependent 21-22 nt sRNAs and show that this mechanism is not specific to pollen. Additionally, we show that these 21-22 nt sRNAs can participate in RNA-directed DNA methylation, are incorporated into ARGONAUTE 1 (AGO1) and may guide AGO1 to cleave genic mRNAs to regulate their expression.

2020-02-24 | GSE133618 | GEO

Separated Transcriptomes of Male Gametophyte and Tapetum in Rice

2011-05-12 | E-GEOD-29217 | biostudies-arrayexpress

Naa50 regulates tapetum degradation

Project description:N-terminal acetylation of proteins is a key modification in eukaryotes; however, our understanding of its biological function in plants is limited. Naa50 is the catalytic subunit of the protein N-terminal acetyltransferase NatE complex. We previously showed that the absence of Naa50 led to sterility in Arabidopsis thaliana. In the present study, we show that a lack of Naa50 in Arabidopsis resulted in collapsed and sterile pollen grains. Further study revealed that the mutation of Naa50 accelerated programmed cell death in the tapetum. Expression pattern analysis showed that Naa50 was specifically expressed in tapetal cells from anthers at stages 9–11 of pollen development, when tapetal programmed cell death occurs. Reciprocal cross analyses indicated that the male sterility of naa50 plants was due to sporophytic effects. Transcriptome sequencing of closed buds showed that the deletion of Naa50 resulted in up-regulation of the cysteine protease-coding gene CEP1 and impaired the expression of several genes that function in pollen wall deposition and pollen mitosis. Our findings suggest that Naa50 regulates cell degradation in the tapetum during anther development and plays an important role in pollen development by affecting several pathways.

2022-05-31 | GSE175392 | GEO

The Arabidopsis DRYK, AtYAK1 regulates the development of the male gametophyte

Project description:Pollen is the male gametophyte of land plants. Proper development and maturation of pollen is necessary for the successful reproduction of seed plants. This process involves sophisticated coordination between sporophytic and gametophytic tissues in anthers. To advance the mechanistic studies of anther development, additional players need to be discovered for a comprehensive understanding of the underlying regulatory network. Here we show that the Arabidopsis dual specificity tyrosine phophorylated and regulated kinase (DRYK), AtYAK1, is essential for development of rosette leaves and the male but not female gametophyte in Arabidopsis. Arabidopsis mutant plants carrying a mutation in AtYAK1 produce developmentally stalled microspores, likely because of the defects in the two consecutive mitosis steps in the post-meiotic maturation process of pollen. The mutation of AtYAK1 has a significant effect on gene expression programs in developing pollen. Transcritpome analysis of atyak1 revealed downstream genes in families of protein kinases, transporters and transcription factors, which potentially contribute to pollen development. This study represents the first molecular characterization of DYRK in the plant kingdom. Our results also imply that the regulation of cytokinesis by DYRKs is evolutionally conserved in fungus, fruit fly, animals and plants.

2015-12-31 | GSE15971 | GEO

CLSY docking to Pol IV requires a conserved domain critical for small RNA biogenesis and transposon silencing

Project description:Eukaryotes must balance the need for gene transcription by RNA polymerase II (Pol II) against the danger of mutations caused by transposable element (TE) proliferation. In plants, these gene expression and TE silencing activities are divided between different RNA polymerases. Specifically, RNA polymerase IV (Pol IV), which evolved from Pol II, transcribes TEs to generate small interfering RNAs (siRNAs) that guide DNA methylation and block TE transcription by Pol II. While the Pol IV complex is recruited to TEs via SNF2-like CLASSY (CLSY) proteins, how Pol IV partners with the CLSYs remains unknown. Here, we identified a conserved CYC-YPMF motif that is specific to Pol IV and is positioned on the complex exterior. Furthermore, we found that this motif is essential for the co-purification of all four CLSYs with Pol IV, but that only one CLSY is present in any given Pol IV complex. These findings support a "one CLSY per Pol IV" model where the CYC-YPMF motif acts as a CLSY-docking site. Indeed, mutations in and around this motif phenocopy pol iv null and clsy quadruple mutants. Together, these findings provide structural and functional insights into a critical protein feature that distinguishes Pol IV from other RNA polymerases, allowing it to promote genome stability by targeting TEs for silencing.

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