Genomic and epigenomic basis of transgressive segregation in rice



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In plant breeding, transgressive segregation refers to phenotypes of offspring that are beyond the parental range. Transgressive phenotypes are distinct from heterotic effects because they are stably inherited through generations. Evolutionary biology supports the theory that novel plant phenotypes (i.e., genetic novelties) such as those typical of transgressive segregation are important components of adaptive speciation through the formation of rare natural hybrids. While the genetic basis of transgressive segregation has long been attributed to complementation and epistatic interaction, the precise molecular underpinnings have not been fully elucidated, particularly the potential contributions of epigenetic regulation. In the recently proposed Omnigenic Theory, the molecular basis of polygenic traits has been defined to be due to the synergistic effects of core genes and peripheral genes. The core genes, which can be detected by genome-wide association studies (GWAS), account for only 20% of phenotypic variance, but the peripheral genes whose contributions are small, additive, and virtually indistinguishable from false positives have been shown to be responsible for the rest (80%) of overall phenotypic variance. Genomic variations in cis-elements are starting to be incorporated into the model as peripheral genes, but the epigenetic components (i.e. variation without primary DNA sequence variation) remains largely unaddressed.

In this study, we addressed the hypothesis that both genomic and epigenomic reconfigurations triggered by parental genome shock are contributory to the novel phenotypes of rare recombinants in a transgressive population. Using the indica x aus recombinant inbred line (RIL) population of rice displaying transgressive segregation for salinity tolerance as a model, we integrated multiple layers of investigation that included whole-genome sequencing, transcriptome, ncRNA and methylome profiling, and chromatin conformation capture to reveal the nature of genomic and epigenomic changes leading to genetic network rewiring in rare recombinants.

Our high-resolution recombination maps showed evidence of extensive genome shuffling during homologous recombination between the widely divergent parental genomes, leading to significant non-parental sequence variation. The genome sizes of RILs were significantly reduced. The majority of the genetic loss was in transposable elements that were unique in either parent. The majority of shared transposons were retained. Of the sequenced RILs, 60% of genomic inheritance profile was the same parental genomic blocks. Genome-wide methylome analysis revealed hypomethylation especially in the CHH context in the most salt tolerant (mega-tolerant) RIL relative to the parents. Despite of reduced level of methylation, the mega-tolerant line acquired new targets of RNA-directed DNA methylation (RdDM) contributing to both the reconciliation of parental confrontation and the overall genome integrity despite its hypomethylated profile. This salient feature of the mega-tolerant RIL contributed to novel patterns global chromatin interaction.

Altogether, these features enabled a higher sustained level of transcriptional activity in the transgressive RIL contributing to its growth and developmental novelties. This systems-level investigation reiterates the tremendous power of homologous recombination in creating novel genomic and epigenomic configurations that may be key to creating the next generation of ecologically resilient crops for the 21st century.



Transgressive segregation, Rice, Genotyping by sequencing, Recombination map, Transcriptome, Heterochromatin, Methylation, ncRNA, siRNA, RNA-directed DNA methylation, Transposable elements, Genome size, Hybridization