Differences in effective ploidy as drivers of genome-wide endosperm expression asymmetries and seed failure in wild tomato hybrids

Abstract

Endosperm misdevelopment leading to hybrid seed failure is a common cause of postzygotic isolation in angiosperms and is observed in both interploidy and homoploid crosses between closely related lineages. Moreover, parental dosage is critical for successful endosperm and seed development, typically requiring a ratio of two maternal to one paternal genome(s) in within-species crosses. The recently revived concept of effective ploidy can largely explain the outcome of experimental crosses that (partly) ameliorate hybrid seed failure by manipulating the actual ploidy in one of the parents. However, genome-wide expression perturbations concomitant with levels of hybrid seed failure have yet to be reported. The tomato clade (Solanum section Lycopersicon), encompassing closely related diploids with partial-to-complete hybrid seed failure and diverse mating systems, provides outstanding opportunities to study these issues. Here we compared replicated endosperm transcriptomes from six crosses within and among three wild tomato lineages. Strikingly, both strongly inviable hybrid crosses displayed conspicuous, asymmetric expression perturbations with strong signatures of cross direction. In particular, Solanum peruvianum, the species inferred to have evolved higher effective ploidy than the other two, drove hybrid expression landscapes in both maternal and paternal roles. This global expression divergence was mirrored in functionally important gene families such as transcription factors and E3 ubiquitin ligases, and revealed differences in cell-cycle tuning between lineages that match phenotypic differences in developing endosperm and mature seed size between reciprocal crosses. Our work initiates the exploration of links between parental conflict, genomic imprinting, expression dosage and hybrid seed failure in flowering plants.