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Dosage sensitive maternal siRNAs determine hybridization success in Capsella

ABSTRACT: 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 dosage-sensitive tissue that nurtures the embryo and functions analogously to the placenta in mammals. Here, we show that the endosperm in incompatible seeds loses DNA methylation and chromatin condensation, resembling the endosperm of seeds depleted for maternal RNA Polymerase IV (PolIV) function. This similarity in phenotype corresponds with a concurrent reduction in small interfering RNAs in the endosperm (sirenRNAs), maternal PolIV-dependent siRNAs governing DNA methylation and regulating target genes. Notably, several AGAMOUS-LIKE MADS-BOX transcription factors (AGLs), known 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. Together, we propose that the response to interspecies hybridizations is triggered by a combination of reduced maternally derived sirenRNAs and heightened expression of AGLs targeting hypomethylated regions in the hybrid endosperm.

ORGANISM(S): Capsella bursa-pastoris x Capsella grandiflora Capsella grandiflora x Capsella rubella Capsella orientalis Capsella bursa-pastoris Capsella rubella Capsella orientalis x Capsella rubella Capsella rubella x Capsella grandiflora Capsella grandiflora

PROVIDER: GSE246468 | GEO | 2024/09/12

REPOSITORIES: GEO

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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. 3 biological replicates, each consisting of 35 siliques from 10 individual plants, were used. Arabidopsis thaliana wild type (ecotype Colombia-0 and Ler-0) and cdka;1 mutant (At3g48750 /SALK_109806) were sown out on soil and grown under the following conditions: 18oC day and 18oC night, 16 hr day length with 30 min adjustment of light to on and off, and 85 Î¼mol/m2/sek in light intensity. For each replica, 10 Ler plants were emasculated and pollinated after 48 hours, either with individual WT Col or with individual cdka;1 mutant pollen. Three days after pollination (3 DAP), the siliques of each biological replicate were dissected with hypodermic needles to remove carpel walls, the pistil with pollen attached to it and the pedicel with abcsission zone. The remaining seeds attached to the middle lamella were harvested in bulk in liquid nitrogen at the same time of the day. Biological replicas are dye-swapped between slides.

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Dosage sensitive maternal siRNAs determine hybridization success in Capsella

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