Abstract
Balanced maternal and paternal genome contributions are a requirement for successful seed development. Unbalanced contributions often cause seed abortion, a phenomenon that has been termed “triploid block.” Misregulation of imprinted regulatory genes has been proposed to be the underlying cause for abnormalities in growth and structure of the endosperm in seeds with deviating parental contributions. We identified a mutant forming unreduced pollen that enabled us to investigate direct effects of unbalanced parental genome contributions on seed development and to reveal the underlying molecular mechanism of dosage sensitivity. We provide evidence that parent-of-origin–specific expression of the Polycomb group (PcG) gene
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is causally responsible for seed developmental aberrations in Arabidopsis seeds with increased paternal genome contributions. We propose that imprinted expression of PcG genes is an evolutionary conserved mechanism to balance parental genome contributions in embryo nourishing tissues.
Crosses between plants of different ploidy often fail because seed development does not proceed normally and non-viable seeds are produced. It is assumed that abnormalities in growth and structure of the endosperm (the nutritional tissue of the seed) are the cause of triploid seed failure, consistent with the proposed role of the endosperm in reproductive isolation and angiosperm speciation. In many species, the ratio of maternal to paternal genomes in the endosperm is important for normal seed development, giving rise to the hypothesis that parent-of-origin–specific gene expression (imprinting) of regulatory genes in the endosperm is the underlying cause for developmental failure in seeds with deviating parental contributions. We tested this hypothesis using the
jason
mutant that forms unreduced male gametes and triploid seeds with increased paternal genome dosage. Based on the results of our study, we propose that imprinting of the FIS component
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serves as a dosage sensor for increasing paternal genome contributions, establishing the molecular basis for dosage sensitivity. Our study provides strong evidence supporting the hypothesis that misbalanced expression of imprinted genes is the cause of seed development defects after interploidy crosses and demonstrates that
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imprinting is a major origin of developmental defects caused by increased paternal genome contributions.