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Parental conflict driven regulation of endosperm cellularization by a family of Auxin Response Factors

ABSTRACT: The endosperm is a reproductive tissue supporting embryo development. In most flowering plants, the initial divisions of endosperm nuclei are not succeeded by cellularization; this process occurs only after a specific number of mitotic cycles have taken place. The timing of cellularization significantly influences seed viability and size. Previous research implicated auxin as a key factor in initiating nuclear divisions and determining the timing of cellularization. Here we uncover the involvement of a family of clustered auxin response factors (cARFs) as dosage-sensitive regulators of endosperm cellularization. cARFs, maternally expressed and paternally silenced, are shown to induce cellularization, thereby restricting seed growth. Our findings align with the predictions of the parental conflict theory, suggesting that cARFs represent major molecular targets in this conflict. We further demonstrate a recurring amplification of cARFs in the Brassicaceae, suggesting an evolutionary response to parental conflict by reinforcing maternal control over endosperm cellularization. Our study highlights that antagonistic parental control on endosperm cellularization converges on auxin biosynthesis and signalling.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE232803 | GEO | 2024/03/22

REPOSITORIES: GEO

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Auxin regulates endosperm cellularization in Arabidopsis

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Parental conflict driven regulation of endosperm cellularization by a family of Auxin Response Factors

Project description:Parental conflict driven regulation of endosperm cellularization by a family of Auxin Response Factors

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OsbZIP76 interacts with OsNF-YBs and regulates endosperm cellularization in rice (Oryza sativa)

Project description:Cellularization is a key event during the development of the endosperm. Our understanding of the developmental regulation of cellularization has been limited for plants other than Arabidopsis. We found that the activation of OsbZIP76 coincided with the initiation of cellularization of rice. Either knockdown or knockout of OsbZIP76 led to precocious cellularization. Many genes involved in endosperm development or starch biosynthesis were prematurely activated in the caryopsis at two days after fertilization. The results implied that OsbZIP76 is involved in the regulation of cellularization in rice. As a putative transcription factor, OsbZIP76 alone lacked transcriptional activation activity. However, it was able to interact with OsNF-YB9 and OsNF-YB1, two nuclear factor Y (NF-Y) family transcription factors, both in yeast and in planta. OsbZIP76 and OsNF-YB9 showed similar endosperm-preferential expression patterns and the transiently expressed proteins were colocalized in the epidermal cells of tobacco. As with osnf-yb1 mutants, the osbzip76 mutants showed reduced seed size and reduced apparent amylose content of the seeds. We also confirmed that OsbZIP76 is an imprinted gene in rice, the expression of which depended on the genetic background. Our results suggested that OsbZIP76 is an endosperm-expressed imprinted gene to regulate development of the endosperm in rice.

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Project description:MADS-box transcription factors (TFs) are subdivided into type-I and II based on phylogenetic analysis. The type II’s regulate floral organ identity and flowering time, but type I’s are relatively less characterized. Here, we report functional characterization of two type-I MADS-box TFs in rice (Oryza sativa), MADS78 and MADS79. Transcript abundance of both these genes in developing seed peaked at 48 hours after fertilization (HAF) and was suppressed by 96 HAF, corresponding to syncytial and cellularized stages of endosperm development, respectively. Seeds overexpressing (OE) MADS78 and 79 exhibited delayed endosperm cellularization, while CRISPR-Cas9 mediated single knock-out mutants showed precocious endosperm cellularization. MADS78 and 79 were indispensable for seed development, as a double knock-out mutant failed to make viable seeds. Both MADS78 and 79 interacted with MADS89, another type-I MADS-box, which enhances nuclear localization. The expression analysis of Fie1, a rice FERTILIZATION-INDEPENDENT SEED–polycomb repressor complex 2 (FIS-PRC2) component, in MADS78 and 79 mutants and vice versa established an antithetical relation, suggesting Fie1 could be involved in negative regulation of MADS78 and 79. Mis-regulation of MADS78 and 79 perturbed auxin homeostasis and carbon metabolism, as evident by mis-regulation of genes involved in auxin transport and signaling as well as starch biosynthesis genes causing structural abnormalities in starch granules at maturity. Collectively, we show MADS78 and 79 are essential regulators of early seed developmental transition and impact both seed size and quality in rice.

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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

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

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

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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.

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