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Dosage-Dependent Deregulation of an AGAMOUS-LIKE Gene Cluster Contributes to Interspecific Incompatibility

Abstract

Postzygotic lethality of interspecies hybrids can result from differences in gene expression, copy number, or coding sequence and can be overcome by altering parental genome dosage. In crosses between Arabidopsis thaliana and A. arenosa, embryo arrest is associated with endosperm hyperproliferation and delayed development similar to paternal-excess interploidy crosses and polycomb-repressive complex (PRC) mutants. Failure is accompanied by parent-specific loss of gene silencing including the dysregulation of three genes suppressed by PRC. Increasing the maternal genome dosage rescues seed development and gene silencing. A gene set upregulated in the failing seed transcriptome encoded putative AGAMOUS-LIKE MADS domain transcription factors (AGL) that were expressed in normal early endosperm and were shown to interact in a previous yeast 2-hybrid analysis. Suppression of these AGL's expression upon cellularization required PRC. Preceding seed failure, expression of the PRC member FIS2 decreased concomitant with overexpression of the AGL cluster. Inactivating two members, AGL62 and AGL90, attenuated the postzygotic barrier between A. thaliana and A. arenosa. We present a model where dosage-sensitive loss of PRC function results in a dysregulated AGL network, which is detrimental for early seed development.

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