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Paternally-acting canonical RNA-directed DNA methylation pathway genes sensitizes Arabidopsis endosperm to paternal dosage [RNA-Seq]

ABSTRACT: Seed development is sensitive to parental dosage, with excess maternal or paternal genomes creating reciprocal phenotypes. Paternal genomic excess results in extensive endosperm proliferation without cellularization and eventual seed abortion. We previously showed that loss of the RNA POL IV gene nrpd1 in tetraploid fathers represses seed abortion in paternal excess crosses. Here we show genetically that RNA-directed DNA methylation (RdDM) pathway activity in the paternal parent is sufficient to determine the viability of paternal excess seeds. The status of the RdDM pathway in paternal excess endosperm does not impact seed viability. Comparison of endosperm transcriptomes, DNA methylation, and small RNAs from balanced and paternal excess endosperm demonstrates that paternal excess seed abortion is unlikely to be dependent on either transposable element or imprinted gene mis-regulation. We suggest instead that loss of paternal RdDM modulates expression at a small subset of genes and desensitizes endosperm to paternal excess. Finally, using allele-specific transcription data, we present evidence of a transcriptional buffering system that up37 regulates maternal alleles and represses paternal alleles in response to excess paternal genomic dosage. These findings prompt reconsideration of models for dosage sensitivity in endosperm.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE126931 | GEO | 2019/05/01

REPOSITORIES: GEO

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Paternally-acting canonical RNA-directed DNA methylation pathway genes sensitizes Arabidopsis endosperm to paternal dosage [miRNA-Seq]

Project description:Seed development is sensitive to parental dosage, with excess maternal or paternal genomes creating reciprocal phenotypes. Paternal genomic excess results in extensive endosperm proliferation without cellularization and eventual seed abortion. We previously showed that loss of the RNA POL IV gene nrpd1 in tetraploid fathers represses seed abortion in paternal excess crosses. Here we show genetically that RNA-directed DNA methylation (RdDM) pathway activity in the paternal parent is sufficient to determine the viability of paternal excess seeds. The status of the RdDM pathway in paternal excess endosperm does not impact seed viability. Comparison of endosperm transcriptomes, DNA methylation, and small RNAs from balanced and paternal excess endosperm demonstrates that paternal excess seed abortion is unlikely to be dependent on either transposable element or imprinted gene mis-regulation. We suggest instead that loss of paternal RdDM modulates expression at a small subset of genes and desensitizes endosperm to paternal excess. Finally, using allele-specific transcription data, we present evidence of a transcriptional buffering system that up37 regulates maternal alleles and represses paternal alleles in response to excess paternal genomic dosage. These findings prompt reconsideration of models for dosage sensitivity in endosperm.

2019-05-01 | GSE126930 | GEO

Paternally-acting canonical RNA-directed DNA methylation pathway genes sensitizes Arabidopsis endosperm to paternal dosage [Bisulfite-seq]

2019-05-01 | GSE126929 | GEO

An epigenetic role for disrupted paternal gene expression in postzygotic seed abortion in Arabidopsis interspecific hybrids

Project description:Interspecific hybrids in Arabidopsis result in seed abortion that causes reproductive barrier. To investigate the allelic expression pattern at transcriptome level during early seed abortion stage, we performed RNA-seq analysis in F1 interspecific hybrids with three different ecotypes in A. thaliana as maternal and A. arenosa as paternal and identified MEGs and PEGs. Interestingly, PEGs showed distinct expression pattern in several aspects, compared to MEGs: PEGs showed ecotype-specific expression pattern, suggesting a role for PEGs in ecotype-dependent seed lethality. 35% of previously known MEGs in non-lethal hybrids were found as PEGs in our lethal interspecific hybrids, implying the presence of abnormal paternal allelic upregulation. The correlation test between the upregulation of PEGs and previously reported paternal-excess interploidy cross (2X6) which exhibited seed abortion showed that dosage disruption by abnormal paternal upregulation is correlated with seed abortion. Moreover, epigenetic disruption appears to cause some of abnormal upregulation of paternal alleles in PEGs via mis-regulation of MEA-mediated PcG2 and MET1-mediated DNA methylation. The results provide clue on the critical role of PEGs in seed abortion via disruption of dosage balance and epigenetic regulation.

2015-10-01 | GSE41391 | GEO

A small RNA pathway mediates allelic dosage in endosperm [mRNA-seq]

Project description:Balance between maternal and paternal genomes within the triploid endosperm is necessary for normal seed development. The majority of endosperm genes are expressed in a 2:1 maternal:paternal ratio, reflecting genomic DNA content. Here we find that the 2:1 transcriptional ratio is, unexpectedly, actively regulated. In A. thaliana and A. lyrata, endosperm 24 nt small RNAs are reduced in TEs and enriched in genes compared to the embryo. We find an inverse relationship between the parent-of-origin of sRNAs and mRNAs, with genes more likely to be associated with maternally than paternally biased sRNAs. Disruption of the Pol IV sRNA pathway causes a shift toward maternal allele mRNA expression for many genes. Furthermore, paternal inheritance of an RNA Pol IV mutation is sufficient to rescue seed abortion caused by excess paternal genome dosage. Thus, RNA Pol IV mediates transcriptional balance between maternally and paternally inherited genomes in endosperm.

2017-12-15 | GSE94786 | GEO

A small RNA pathway mediates allelic dosage in endosperm [sRNA-seq]

2017-12-15 | GSE94787 | GEO

Maternal siRNAs as regulators of parental genome imbalance and gene expression in endosperm of Arabidopsis seeds.

Project description:Seed size is important to crop domestication and natural selection and is affected by the balance of maternal and paternal genomes in endosperm. Endosperm, like placenta in mammals, provides reserves to the developing embryo. Interploidy crosses disrupt the genome balance in endosperm and alter seed size. Specifically, paternal-excess crosses (2 M-CM-^W 4) delay endosperm cellularization (EC) and produce larger seeds, whereas maternal-excess crosses (4 M-CM-^W 2) promote precocious EC and produce smaller seeds. The mechanisms for responding to the parental genome dosage imbalance and for gene expression changes in endosperm are unknown. In plants, RNA polymerase IV (PolIV or p4) encoded by NRPD1a is required for biogenesis of a major class of 24-nt small interfering RNAs (also known as p4-siRNAs), which are predominately expressed in developing endosperm. Here we show that p4-siRNA accumulation depends on the maternal genome dosage, and maternal p4-siRNAs target transposable elements (TEs) and TE-associated genes (TAGs) in seeds. The p4-siRNAs correlate negatively with expression levels of AGAMOUS-LIKE (AGL) genes in endosperm of interploidy crosses. Moreover, disruption of maternal NRPD1a expression is associated with p4-siRNA reduction and AGL up-regulation in endosperm of reciprocal crosses. This is unique genetic evidence for maternal siRNAs in response to parental genome imbalance and in control of transposons and gene expression during endosperm development. 8 samples: 2x X 2x seed,leaf; 4x X 4x seed,leaf; 2x X 4x seed,leaf; 4x X 2x seed,leaf.

2011-11-11 | E-GEOD-25280 | biostudies-arrayexpress

Paternal easiRNAs establish the triploid block in Arabidopsis

Project description:Polyploidy, the presence of more than two sets of chromosomes within the nucleus, is a common phenomenon among plants that has shaped genome organization and is thought to be a major driver of speciation. The triploid block acts as a reproductive barrier that prevents successful backcrosses of newly formed polyploids with their progenitors. It is established in the endosperm, an ephemeral tissue that nurtures the developing embryo. Here we show that paternal 21/22 nucleotide epigenetically activated small interfering RNAs (easiRNAs) in Arabidopis thaliana are responsible for the establishment of the triploid block associated seed abortion. This dramatic phenotype is overcome when crosses are performed with a paternal mutant in the plant specific RNA polymerase IV (Pol IV). Loss of Pol IV reduces both easiRNAs and hetsiRNAs in the pollen grain. Seeds derived from crosses between wild type tetraploid fathers and diploid mothers have reduced levels of hetsiRNAs and cytosine methylation at transposable elements (TEs), indicating that they have suffered an excess of epigenetic reprogramming due to an excess of paternally derived easiRNAs. Paternal Pol IV mutants are able to buffer that easiRNA excess and rescue the abortion phenotype by rescuing both the cytosine methylation level at TEs and the 24 nt hetsiRNA accumulation levels. This mechanism highlights the elegant and important TE regulation mechanism controlled by the plant specific Pol IV that takes place pre-fertilization and regulates paternal easiRNAs and maternal hetsiRNAs, and determines the post-fertilization epigenetic stability and seed viability.

2017-12-14 | GSE84122 | GEO

Maternal siRNAs as regulators of parental genome imbalance and gene expression in endosperm of Arabidopsis seeds.

Project description:Seed size is important to crop domestication and natural selection and is affected by the balance of maternal and paternal genomes in endosperm. Endosperm, like placenta in mammals, provides reserves to the developing embryo. Interploidy crosses disrupt the genome balance in endosperm and alter seed size. Specifically, paternal-excess crosses (2 × 4) delay endosperm cellularization (EC) and produce larger seeds, whereas maternal-excess crosses (4 × 2) promote precocious EC and produce smaller seeds. The mechanisms for responding to the parental genome dosage imbalance and for gene expression changes in endosperm are unknown. In plants, RNA polymerase IV (PolIV or p4) encoded by NRPD1a is required for biogenesis of a major class of 24-nt small interfering RNAs (also known as p4-siRNAs), which are predominately expressed in developing endosperm. Here we show that p4-siRNA accumulation depends on the maternal genome dosage, and maternal p4-siRNAs target transposable elements (TEs) and TE-associated genes (TAGs) in seeds. The p4-siRNAs correlate negatively with expression levels of AGAMOUS-LIKE (AGL) genes in endosperm of interploidy crosses. Moreover, disruption of maternal NRPD1a expression is associated with p4-siRNA reduction and AGL up-regulation in endosperm of reciprocal crosses. This is unique genetic evidence for maternal siRNAs in response to parental genome imbalance and in control of transposons and gene expression during endosperm development.

2011-11-11 | GSE25280 | GEO

Chemically-induced epimutagenesis allows bypassing reproductive barriers in hybrid seeds [BiSulfite-seq]

Project description:The "triploid block" prevents interploidy hybridizations in flowering plants, and is characterized by failure in endosperm development and function, arrest in embryogenesis, and seed collapse. Many genetic components of triploid seed lethality have been successfully identified in the model plant Arabidopsis thaliana, most notably the paternally expressed imprinted genes (PEGs) that are up-regulated in the tetraploid endosperm with paternal excess. Previous studies have shown that the paternal epigenome is a key determinant of the triploid block response, as the loss of DNA methylation in diploid pollen suppresses the triploid block almost completely. Here, we demonstrate that triploid seed abortion is bypassed in plants treated with the DNA methyltransferase inhibitor 5-Azacytidine during seed germination and early plant growth. We have identified strong suppressor lines showing transgenerational inheritance of hypomethylation in CG context, as well as normalized expression of PEGs. Importantly, differentially methylated loci segregate in the progeny of "epimutagenized" plants, which may allow the identification of epialleles involved in the triploid block response in future studies. Finally, we demonstrate that chemically-induced epimutagenesis allows bypassing interploidy hybridizations in Arabidopsis and interspecific hybridization barriers in crosses between Capsella species, thus potentially emerging as a novel strategy for seed-based breeding of triploids and interspecific hybrids with agronomical interest.

2021-11-23 | GSE179702 | GEO

Chemically-induced epimutagenesis allows bypassing reproductive barriers in hybrid seeds [RNA-seq]

2021-11-23 | GSE179697 | GEO

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