Early disruption of maternal-zygotic interaction and activation of defense-like responses in Arabidopsis interspecific incompatibility

Seed death resulting from hybridization between Arabidopsis thaliana and Arabidopsis arenosa has complex genetic determination, and involves deregulation 5-8 days after pollination (DAP) of AGAMOUS-LIKE genes (AGLs) and retroelements. To identify causal mechanisms, we compared 3 DAP transcriptomes of compatible and incompatible hybrids and parents at 3 DAP. Hybrids misexpressed endosperm and seed coat regulators, and hyperactivated genes encoding ribosomal, photosynthetic, stress-related and immune response proteins. Regulatory disruption was more severe in Col-0 hybrids than in C24 hybrids, consistent with the degree of incompatibility. Maternal loss-of-function alleles for endosperm growth factor TRANSPARENT TESTA GLABRA 2 and HAIKU 1, and defense response regulators NON-EXPRESSOR OF PATHOGENESIS RELATED 1 and SALICYLIC ACID INDUCTION-DEFICIENT 2 , increased hybrid seed survival. The activation of presumed POLYCOMB REPRESSIVE COMPLEX (PRC) targets, together with a twenty-fold reduction in expression of FERTILIZATION INDEPENDENT SEED 2, indicated a PRC role. Proximity to transposable elements affected natural vartiation for gene regulation, but transposon activation did not differ from controls. Collectively, this investigation provides candidates for multigenic orchestration of the incompatibility response through disruption of endosperm development, a novel role for communication between endosperm and maternal tissues and for pathways previously connected to immunity, but, surprisingly, does not identify a role for transposons. Examination of differential gene expression of incompatible A. thaliana eco. Col-0 X A. arenosa and compatible A. thaliana eco. C24 X A. arenosa hybrid seeds plus corresponding A. thaliana and A. arenosa control crosses.