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

ABSTRACT: 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.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE25280 | GEO | 2011/11/11

SECONDARY ACCESSION(S): PRJNA134821

REPOSITORIES: GEO

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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.

2010-08-26 | GSE20005 | GEO

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

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

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

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

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Maternal siRNAs mediate spatial and temporal regulation of gene expression and seed development in Arabidopsis

Project description:In Arabidopsis seed development involves maternal small interfering RNAs (siRNAs) that induce RNA-directed DNA methylation (RdDM) through the NRPD1 pathway. To investigate their biological functions we characterized siRNAs in the endosperm and seed coat that were separated by laser capture microdissection (LCM) in reciprocal genetic crosses with an nrpd1 mutant. We also monitored the spatio-temporal activity of the NRPD1 pathway on seed development using AGO4:GFP::AGO4 (promoter:GFP::protein) reporter and promoter:GUS sensors of siRNA-mediated silencing. From these approaches we identified four distinct groups of siRNA loci that were dependent on or independent of the maternal NRPD1 allele in the endosperm or seed coat. A group of maternally expressed NRPD1-siRNA loci targets endosperm-preferred genes, including those encoding AGAMOUS-LIKE (AGL) transcription factors. Using the sensor AGL40:GUS and AGL91:GUS constructs we demonstrate that spatial and temporal expression patterns of these genes in the endosperm were regulated by the NRPD1-mediated pathway irrespective of complete silencing (AGL91) or incomplete silencing (AGL40) of these target genes. Modified expression of these siRNA-targeted genes affects seed size and we propose that the corresponding maternal siRNAs could account for parent-of-origin effects on the endosperm in interploidy and hybrid crosses. These analyses reconcile previous studies on siRNAs and imprinted gene expression during seed development.

2018-12-31 | GSE47722 | GEO

Rice interploidy crosses disrupt epigenetic regulation, gene expression, and seed development

Project description:Seed development in angiosperms requires a 2:1 maternal-to-paternal genome ratio (2m:1p) in the endosperm. When the ratio is disrupted, the seed development is impaired. Rice interploidy crosses result in endosperm failures. Here we report that the defective endosperm was associated with nonadditive expression of small RNAs and protein-coding genes. Interestingly, 24-nt siRNAs were enriched in the 5’ and 3’ flanking sequences of nonadditively expressed genes in the interploidy crosses and negatively associated with the expression of imprinted genes. Furthermore, some PRC2 gene family members and the genes for DNA methylation including OsMET1b and OsCMT3a were upregulated in the 2X4 cross but repressed in the reciprocal cross. These different epigenetic effects could lead to precocious or delayed cellularization during endosperm development. Notably, many endosperm-preferred genes including starch metabolic and storage protein genes during grain filling were associated with DNA methylation or H3K27me3 and repressed in both 2X4 and 4X2 crosses. WUSCHEL homeobox2 (WOX2)-like (WOX2L), an endosperm-preferred gene, was expressed specifically in the rice endosperm, on contrary to WOX2 expression in the Arabidopsis embryo. CRISPR/Cas9 editing of WOX2L in transgenic rice blocked starch and protein accumulation, resulting in seed abortion. In addition to gene repression, disrupting epigenetic process in the interploidy crosses also induced expression of stress-responsive genes. Thus, maintaining the 2m:1p genome ratio in the endosperm is essential for normal grain development in rice and other cereal crops.

2018-08-31 | GSE65149 | GEO

Dosage-sensitive maternal siRNAs determine hybridization success in Capsella

Project description:Hybrid seed failure arising from wide crosses between plant species is a recurring obstacle in plant breeding, impeding the transfer of desirable traits. This postzygotic reproductive barrier primarily occurs in the endosperm, a tissue that nourishes the embryo and functions similarly to the placenta in mammals. We found that incompatible seeds show a loss of DNA methylation and chromatin condensation in the endosperm, similar to seeds lacking maternal RNA polymerase IV activity. This similarity is linked to a decrease in small interfering RNAs in the endosperm (sirenRNAs), maternal RNA polymerase IV-dependent short interfering RNAs that regulate DNA methylation. Several AGAMOUS-like MADS-box transcription factor genes (AGLs), key regulators of endosperm development, are targeted by sirenRNAs in cis and in trans. This finding aligns with the enrichment of AGL target genes among deregulated genes. We propose that hybrid seed failure results from reduced maternal sirenRNAs combined with increased AGL expression, leading to abnormal gene regulation in the endosperm.

2024-09-12 | GSE246468 | GEO

Genome-wide Transcript Profiling of Endosperm without Paternal Contribution Identifies Parent-of-origin Dependent Regulation of AGAMOUS-LIKE 36

Project description:Seed development is dependent on a well-orchestrated interplay between different transcriptional programs operating in the embryo, the endosperm and the maternally derived seed coat. In angiosperms, the embryo and the endosperm are products of double fertilization during which the two pollen sperm cells fuse with the egg cell and the central cell of the female gametophyte. In Arabidopsis, mutation of the cell cycle regulator CYCLIN DEPENDENT KINASE A;1 (CKDA;1) results in pollen that only successfully fertilizes the egg cell. Seeds generated from crosses with cdka;1 pollen develop endosperm with solely maternal and no paternal contribution. Here we have exploited cdka;1 fertilization as a novel tool for genomic dissection of parental effects during seed development. We have generated genome-wide transcription profiles of cdka;1 fertilized seeds. By this approach, we identified 11 differentially expressed AGAMOUS-LIKE (AGL) genes encoding Type-I MADS-box transcription factors. Here, AGL36 was chosen for an in-depth study. We show that AGL36 is imprinted and only expressed from the maternal genome. In addition, we demonstrate that AGL36 imprinting is controlled by the activity of METHYLTRANSFERASE1 (MET1) maintenance DNA methyltransferase and DEMETER (DME) DNA glycosylase. Interestingly, our data also show that the active maternal allele of AGL36 is regulated throughout endosperm development by components of the FIS Polycomb Repressive Complex 2 (PRC2). These findings shed novel light on the interplay between maternal and paternal genomes in the seed and how imprinting is coordinated by different mechanisms.

2010-10-20 | GSE24809 | GEO

Seed development

Project description:Reciprocal crosses of a diploid Arabidopsis with different ploidies results in different endosperm development patterns and phenotype. Typically if the ploidy is higher on the maternal side, there are fewer endosperm cells which cellularize early, and conversely, if the paternal ploidy is higher, there is more number of endosperm cells which cellularize late. Crosses involving diploid and tetraploid Arabidopsis (C24) are viable, whereas crosses involving the diploid and hexaploid, even though exhibit the above mentioned directional trend in endosperm development, abort (Scott et al 1998). The 'maternalised' and 'paternalised' development of endosperm is also observed in crosses involving some Arabidopsis mutants. Mutants in the fis class of genes, e.g. fis1-medea, when crossed with a diploid Arabidopsis (pollen parent) show endosperm development-seed development similar to a diploid (seed parent) crossed with hexaploid pollen parent. Reciprocal crosses of homozygous met1 and diploid Arabidopsis also exhibit reciprocal trends in endosperm development, where a homozygous met1 mutant (seed parent) crossed with diploid is similar in phenotype to a diploid (seed parent) - tetraploid cross. Endosperm development in the reciprocal cross has phenotypic similarity to the tetraploid (seed parent)-diploid cross (Adams et al 2000). We are interested in understanding gene profiles and trends in expression underlying the endosperm development in the interploidy crosses as well as the fis and met1 mutant. 11 samples were used in this experiment.

2010-01-09 | E-GEOD-19259 | biostudies-arrayexpress

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