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

ABSTRACT: 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.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE179697 | GEO | 2021/11/23

REPOSITORIES: GEO

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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

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

Auxin regulates endosperm cellularization in Arabidopsis

Project description:The endosperm is an ephemeral tissue that nourishes the developing embryo, similar to the placenta in mammals. In most angiosperms, endosperm development starts as a syncytium, in which nuclear divisions are not followed by cytokinesis. The timing of endosperm cellularization largely varies between species, and the event triggering this transition remains unknown. Here we show that increased auxin biosynthesis in the endosperm prevents its cellularization, leading to seed arrest. Auxin-overproducing seeds phenocopy paternal-excess triploid seeds derived from hybridizations of diploid maternal plants with tetraploid fathers. Concurrently, auxin-related genes are strongly overexpressed in triploid seeds, correlating with increased auxin activity. Reducing auxin biosynthesis and signaling reestablishes endosperm cellularization in triploid seeds and restores their viability, highlighting a causal role of increased auxin in preventing endosperm cellularization. We propose that auxin determines the time of endosperm cellularization, and thereby uncovered a central role of auxin in establishing hybridization barriers in plants.

2019-12-21 | GSE124108 | 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

Parent-of-origin effects in seeds of Arabidopsis thaliana: Affymetrix

Project description:Crossing plants of the same species but different ploidies can have dramatic effects on seed growth, but little is known about the alterations to transcriptional programmes responsible for this. Parental genomic imbalance particularly affects proliferation of the endosperm, with an increased ratio of paternally to maternally contributed genomes (‘paternal excess’) associated with overproliferation, while maternal excess inhibits endosperm growth. One interpretation is that interploidy crosses disrupt the balance in the seed of active copies of parentally imprinted genes. This is supported by the observation that mutations in imprinted FIS-class genes of Arabidopsis thaliana share many features of the paternal excess phenotype. Here we investigated gene expression underlying parent-of-origin effects in Arabidopsis through transcriptional profiling of siliques generated by interploidy crosses and FIS-class mutants. Two biological replicate samples each of 2xX2x, 2xX4x, 2xX6x, 6xX2x, 4xX2x and fis1X2x and a single sample of msi1. Each sample was hybridised to a separate array.

2010-08-26 | E-GEOD-20005 | biostudies-arrayexpress

Parent-of-origin effects in seeds of Arabidopsis thaliana: Agilent

Project description:Crossing plants of the same species but different ploidies can have dramatic effects on seed growth, but little is known about the alterations to transcriptional programmes responsible for this. Parental genomic imbalance particularly affects proliferation of the endosperm, with an increased ratio of paternally to maternally contributed genomes (‘paternal excess’) associated with overproliferation, while maternal excess inhibits endosperm growth. One interpretation is that interploidy crosses disrupt the balance in the seed of active copies of parentally imprinted genes. This is supported by the observation that mutations in imprinted FIS-class genes of Arabidopsis thaliana share many features of the paternal excess phenotype. Here we investigated gene expression underlying parent-of-origin effects in Arabidopsis through transcriptional profiling of siliques generated by interploidy crosses and FIS-class mutants. Six biological samples: 2xX2x, 2xX4x, 2xX6x, 6xX2x, 4xX2x and fis1X2x. Each non-2xX2x cross was co-hybridised with 2xX2x to a two-colour array (5 arrays). Dyes were then swapped and the hybridisations repeated using an additional 5 arrays.

2010-08-26 | E-GEOD-20006 | biostudies-arrayexpress

Transgenerational effect of mutants in the RNA-directed DNA methylation pathway on the triploid block

Project description:Hybridizations of plants that differ in number of chromosome sets (ploidy) frequently causes endosperm failure and seed arrest, a phenomenon referred to as triploid block. Unreduced diploid gametes generated by the omission of second division1 (osd1) mutant induce the triploid block, similar as tetraploid (4x) plants. We recently found that mutations in NRPD1, encoding the largest subunit of the plant-specific RNA Polymerase IV (Pol IV), can suppress the triploid block. Pol IV generates small RNAs required to guide de novo methylation in the RNA-directed DNA methylation (RdDM) pathway. Strikingly however, mutations in other components of the RdDM pathway like RDR2 and NRPE1 fail to suppress the triploid block when inherited in the osd1 background, but have a suppressive effect as 4x mutants. In this study, we aimed at understanding the cause for this discrepancy. We found that the ability of mutants in the RdDM pathway to suppress the triploid block depends on their degree of inbreeding. While nrpd1 is able to suppress in the first homozygous generation, mutants in RDR2, NRPE1, and DRM2 require at least one additional round of inbreeding to exert a suppressive effect. Our data thus reveal that loss of RdDM function differs in its effect in early and late generations and that Pol IV acts at an early stage of triploid block establishment.

2021-04-20 | GSE156597 | GEO

Both maternally and paternally imprinted genes regulate seed development in rice

Project description:Genetic imprinting is an epigenetic phenomenon that describes unequal expression of paternal and maternal alleles of a gene in sexually reproducing organisms including mammals and flowering plants. The function of imprinted genes was rarely reported. We report genome-wide analysis of gene expression, DNA methylation, and small RNAs in the rice endosperm and functional tests of five imprinted genes in seed development using CRISPR/Cas9 editing technology. We identified 162 maternally expressed genes(MEGs) and 95 paternally expressed genes (PEGs) in the rice endosperm, which were associated with miniature inverted-repeat transposable elements, imprinted differentially methylated loci, and some 21-22-siRNAs and lncRNAs. Remarkably, one-third of MEGs and nearly half of PEGs were associated with grain-yield quantitative trait loci and enriched in the endosperm-expressed genes. Disrupting two MEGs increased the amount of small starch granules and reduced grain size, weight, and embryo size, while mutating three PEGs reduced starch content and seed fertility. Our data support both MEGs and PEGs in rice are required for starch and nutrient accumulation, mediating offspring fitness and optimal seed size. This imprinting strategy provides potential means for improving grain yield of rice and other cereal crops.

2017-02-04 | GSE77710 | 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

DNA hypomethylation bypasses the interploidy hybridization barrier in Arabidopsis

Project description:Plants of different ploidy levels are separated by a strong postzygotic hybridization barrier that is established in the endosperm. Deregulated parent-of-origin specific genes are causal for the response to interploidy hybridizations, revealing an epigenetic basis of this phenomenon. In this study we present evidence that paternal hypomethylation can bypass the interploidy hybridization barrier by alleviating the requirement of the epigenetic Polycomb Repressive Complex 2 (PRC2) in the endosperm. Bypass of the barrier is mediated by suppressed expression of imprinted genes. We show that hypomethylated pollen causes redistribution of CHG methylation to PRC2 target genes, revealing that different epigenetic modifications can functionally substitute for each other. Our work presents a method and the underlying mechanism for the generation of viable triploids, providing an impressive example for the potential of epigenome manipulations for plant breeding.

2014-09-22 | GSE53642 | GEO

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