The epigenome underlying a novel and non-parental stress-adaptive phenotype created by transgressive segregation

Transgressive segregation offers a non-reductionist strategy for breeding crops with novel mechanisms for complex adaptive traits through the omnigenic paradigm. While this phenomenon has been linked to complementation and epistatic effects, the contribution of the epigenome is unknown. We examined a well-characterized recombinant inbred population (F ₉ ) of Oryza sativa (rice) derived from parents of wide genetic contrast (IR29/ indica x Pokkali/ aus ) to understand the impact of mild genomic shock to the epigenomic and chromatin landscapes of a transgressive segregant with superior tolerance to hyper-salinity stress. Analysis of the genome, methylome, Topographically Associating Domain (TAD), and transcriptome across parents and recombinants revealed that the novelty of the outlier progeny is associated with peculiar features being an outcome of recombination between the longer chromatins of indica and shorter chromatins of aus . This is characterized by the downsizing of recombinant genome due to the shedding of transposon loci and other repetitive sequences. Transposon shedding was largely responsible for the most extreme hypomethylation of the transgressive epigenome in all of CG, CHG and CHH contexts but with the most peculiarity in the CHH context affecting both the intergenic and genic spaces. The consequence was a novel chromatin profile characterized by uniform segmentation of TADs in all affected chromosomes. This defining epigenomic profile of the transgressive segregant positively correlated with the reduction of stochastic variability in the salinity stress response transcriptome especially the genes affected by the non-parental TAD segmentation, many of which function in stress-related and growth-related responses.