Trans-allelic Epigenetic Dominance Disrupts Hybrid Endosperm Development in Wild Tomatoes

Abstract

Background and AimsHybrid seed failure (HSF) is a common reproductive barrier in flowering plants, but how divergence in so-called effective ploidy translates into genome-wide allelic imbalance in hybrid endosperm remains unresolved. Using wild tomatoes (Solanum sect. Lycopersicon) as our model system, we test whether parent-of-origin expression shifts in hybrids are consistent with simple dosage effects or instead reflect lineage-specific trans regulation. MethodsUsing reciprocal interspecific crosses, we quantified parent-of-origin (allele-specific) expression in developing endosperm and analyzed patterns of differential parent-of-origin expression (DPE) across cross contexts. Guided by strong patterns in parental expression, we further classified DPE genes into four functional classes defined by their relationship to Solanum peruvianum (Per). This exercise captured distinct modes of trans-allelic regulation and guided functional interpretation. Key ResultsParental expression proportions are strongly asymmetric in hybrids, with the most pronounced and repeatable shifts occurring in crosses involving Per. These shifts recur across reciprocal contexts and include elevated maternal proportions even in crosses phenotypically classified as paternal-excess-like, arguing against a dosage-only model. Instead, we observed cross-consistent, coordinated DPE patterns corresponding to trans-acting dominance associated with Per. Functional enrichment of Per-associated DPE highlights chromatin regulation, including DNA methylation/RdDM- and chromatin remodeling-related factors, and Polycomb-linked regulators, implicating disruption of chromatin-based repression in hybrid endosperm. Concurrently, Per-associated activation of auxin- and cell-cycle regulatory pathways in non-Per alleles suggests mis-timed hormone-dependent developmental transitions that can destabilize proliferation-cellularization programs. ConclusionsOur findings support a model of trans-allelic epigenetic dominance in which Per-associated regulatory inputs reshape allelic expression landscapes in hybrid endosperm largely independent of parental origin. This provides a mechanistic link between effective ploidy divergence, genome-wide transcriptional imbalance, and HSF, and motivates reciprocal hybrid studies that integrate expression with chromatin-state and accessibility profiling.