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A VEL3 histone deacetylase complex establishes a maternal epigenetic state controlling progeny seed dormancy

ABSTRACT: Mother plants play an important role in the control of dormancy and dispersal characters of their progeny. In Arabidopsis seed dormancy is imposed by the embryo-surrounding tissues of the endosperm and seed coat. Here we show that the VERNALIZATION5/VIN3-LIKE 3 (VEL3) gene maintains maternal control over progeny seed dormancy by establishing an epigenetic state early in endosperm development that primes the depth of primary seed dormancy later established during seed maturation. VEL3 relocates MSI1 to the nucleolus and associates with other components of the histone deacetylase complex (HDAC). Furthermore VEL3 preferentially associates with pericentromeric chromatin and is required for deacetylation and H3K27me3 deposition and is required for gene repression via PRC2 and HDAC at pericentromeric regions established in the central cell. Interestingly, the epigenetic state established by the maternal VEL3 is retained trans-generationally in mature seeds, and controls seed dormancy in part through the repression of programmed cell death-associated gene ORE1. Our data demonstrates a novel mechanism by which maternal control of progeny seed physiology persists post-shedding, maintaining parental control of seed behaviour.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE202802 | GEO | 2023/03/16

REPOSITORIES: GEO

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A VEL3 histone deacetylase complex establishes a maternal epigenetic state controlling progeny seed dormancy

Project description:Mother plants play an important role in the control of dormancy and dispersal characters of their progeny. In Arabidopsis seed dormancy is imposed by the embryo-surrounding tissues of the endosperm and seed coat. Here we show that VERNALIZATION5/VIN3-LIKE 3 (VEL3) maintains maternal control over progeny seed dormancy by establishing an epigenetic state in the central cell that primes the depth of primary seed dormancy later established during seed maturation. VEL3 colocalizes with MSI1 in the nucleolus and associates with a histone deacetylase complex. Furthermore, VEL3 preferentially associates with pericentromeric chromatin and is required for deacetylation and H3K27me3 deposition established in the central cell. The epigenetic state established by maternal VEL3 is retained in mature seeds, and controls seed dormancy in part through repression of programmed cell death-associated gene ORE1. Our data demonstrates a novel mechanism by which maternal control of progeny seed physiology persists post-shedding, maintaining parental control of seed behaviour.

2023-03-24 | PXD041094 | Pride

RNA-Seq of Arabidopsis thaliana developing siliques and seeds with temperature shifts

Project description:We investigated RNA involved in the maternal control of progeny seed dormancy. Basically, we grew Ler wild type plants at 22 and 16 degree Celsius before fertilization which were moved to 22 degree for seed maturation along with ft-1 plants at 22 degree through lifetime (which show decreased seed germinability). Various RNA fractions were prepared from developing siluqes (seeds removed) and seeds, and sequenced to identify genes involved in transducing maternal memory of temperature to progeny seeds.

2014-11-20 | E-MTAB-2869 | biostudies-arrayexpress

Combinations of maternal-specific repressive epigenetic marks in the endosperm control seed dormancy

Project description:Combinations of maternal-specific repressive epigenetic marks in the endosperm control seed dormancy

| PRJNA666927 | ENA

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

Penfield: Understanding the affect of maternal environment on seed dormancy

Project description:Maternal environment is an important regultor of seed dormancy, but the mechanisms underlying the process are poorly understood. We have found that genes in the circadian clock control dormancy, in part through their regulation of the canonical photoperiod pathway known from research into flowering time control. In this experiment we compare the affects of altering seed maturation temperature or maternal photoperiod on dry seed transcriptomes, and the photoperiod-insenstive ft-1 mutant to wt type Ler. In this way we are identifying gene expression programmes which result from the seed's response to maternal environmental experience. Keywords: Expression profilling by array

2011-04-21 | GSE28747 | GEO

Endosperm and maternal-specific expression of EIN2 affects endosperm cellularization and seed size in Arabidopsis

Project description:Seed size is related to plant evolution and crop yield and is affected by genetic mutations, imprinting, and genome dosage. Imprinting is a widespread epigenetic phenomenon in mammals and flowering plants. ETHYLENE INSENSITIVE2 (EIN2) encodes a membrane protein that links the ethylene perception to transcriptional regulation. Interestingly, during seed development EIN2 is maternally-expressed in Arabidopsis and maize, but the role of EIN2 in seed development is unknown. Here we show that EIN2 is expressed specifically in the endosperm, and the maternal-specific EIN2 expression affects temporal regulation of endosperm cellularization. As a result, seed size increases in the genetic cross using the ein2 mutant as the maternal parent or in the ein2 mutant. The maternal-specific expression of EIN2 in the endosperm is controlled by DNA methylation but not by H3K27me3 or by ethylene and several ethylene pathway genes tested. RNA-seq analysis in the endosperm isolated by laser-capture microdissection show upregulation of many endosperm-expressed genes such as AGAMOUS-LIKEs (AGLs) in the ein2 mutant or when the maternal EIN2 allele is not expressed. EIN2 does not interact with DNA and may act through ETHYLENE INSENSITIVE3 (EIN3), a DNA binding protein present in sporophytic tissues, to activate target genes like AGLs, which in turn mediate temporal regulation of endosperm cellularization and seed size. These results provide mechanistic insights into endosperm and maternal-specific expression of EIN2 on endosperm cellularization and seed development, which could help improve seed production in plants and crops.

2022-10-12 | GSE147587 | GEO

Penfield: Understanding the affect of maternal environment on seed dormancy

2011-04-21 | E-GEOD-28747 | biostudies-arrayexpress

Microarray data from barley aleurone

Project description:The phytohormone gibberellic acid (GA) is well known to promote seed germination in plants. One of its functions is to stimulate the production of hydrolytic enzymes in the aleurone and their secretion to the adjacent endosperm. The storage in the endosperm is thus degraded by these hydrolases into small molecules, which are utilized as nutrients for embryo growth to establish the young seedling. ABA in contrast plays antagonistic role to GA to keep seed in dormancy. Cereal aleurone has been established as a model system to investigate giberrellin (GA) and abscisic acid (ABA) responses. Using Barley 1 GeneChip, we examined the mRNA accumulation of over 22 000 genes in barley aleurone treated with GA, ABA, GA plus ABA, and sln1 mutant. Barley aleurone tissues were separated from half-seed without embryo. Three independent RNA samples for each treatment including the control without any hormone were extracted and hybridized onto Affymetrix microarrays. We also did microarray in three replications for sln1 mutant aleurone without hormone treatment.

2010-01-01 | E-GEOD-18758 | biostudies-arrayexpress

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

Parental epigenetic asymmetry of PRC2-mediated histone modifications in the Arabidopsis endosperm

Project description:Parental genomes in the endosperm are marked by differential DNA methylation and are therefore epigenetically distinct. This epigenetic asymmetry is established in the gametes and maintained after fertilization by unknown mechanisms. In this manuscript, we have addressed the key question whether parentally inherited differential DNA methylation affects de novo targeting of chromatin modifiers in the early endosperm. Our data reveal that polycomb-mediated H3 lysine 27 trimethylation (H3K27me3) is preferentially localized to regions that are targeted by the DNA glycosylase DEMETER (DME), mechanistically linking DNA hypomethylation to imprinted gene expression. Our data furthermore suggest an absence of de novo DNA methylation in the early endosperm, providing an explanation how DME-mediated hypomethylation of the maternal genome is maintained after fertilization. Lastly, we show that paternal-specific H3K27me3- marked regions are located at pericentromeric regions, suggesting that H3K27me3 and DNA methylation are not necessarily exclusive marks at pericentromeric regions in the endosperm.

2016-04-26 | GSE66585 | GEO

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