Transcriptomic insights into triploid seed failure in Arabidopsis arenosa natural populations

Polyploidy is a key evolutionary force in plants; among its many consequences, hybridization between diploids and polyploids is restricted due to the "triploid block". While the molecular mechanisms of this postzygotic barrier are extensively studied in the model species Arabidopsis thaliana, our understanding of the triploid block in natural systems remains limited. Here, we investigated the transcriptome of failing triploid seeds in Arabidopsis arenosa, a close relative of A. thaliana with diploid and autotetraploid populations meeting in nature. We also identified A. arenosa imprinted genes. Triploid seeds showed preferential misregulation of imprinted genes, which parallels the parent-of-origin features of the triploid block. Tissue-specific transcriptomic analyses revealed pathogen defense-like response being recurrently affected in the endosperm and seed coat. This pathway is commonly misregulated in all species with triploid seed transcriptomes studied to date. The associated genes, however, are likely more involved in cell-cell signaling rather than pathogen defense per se. Altogether, this study depicts a thorough molecular landscape of the triploid block for the first time in natural systems. Combining data on the understudied maternal excess transcriptome, a new imprintome, a tissue-specific focus, and a cross-species comparison, this study also advances our understanding of the triploid block and seed development.