No abstract

In F1 offspring from a cross between two Brassica napus plants of synthetic and natural origin, we demonstrate the occurrence of novel transgenerational structural genome variants. Long read sequencing in twelve F1 sister plants revealed five large-scale structural rearrangements where both parents carried different homozygous alleles but the heterozygous F1 genomes were not identical heterozygotes as expected. Such spontaneous rearrangements were part of homoeologous exchanges or segmental deletions and were identified in different, individual F1 plants. The variants caused deletions, gene copy-number variations, diverging methylation patterns and other structural changes in large numbers of genes and may have been causal for unexpected phenotypic variation between individual F1 sister plants, for example strong divergence of plant height and leaf area. This example suggests that the spontaneous occurrence of transgenerational de novo structural rearrangements could be a feasible model for how allopolyploid crops can rapidly overcome intense allopolyploidization bottlenecks to re-expand their genetic diversity for ecogeographical expansion and human selection. The strong implications of these findings for potentially widespread gene loss or neofunctionalization in individual polyploid plants also raises the intriguing possibility that natural genome restructuring in polyploid plants may have a considerably more drastic impact on genetic diversity in agricultural ecosystems than extremely precise, biotechnological genome modifications.

In a cross between two homozygous Brassica napus plants of synthetic and natural origin, we demonstrate that novel structural genome variants from the synthetic parent cause immediate genome diversification among F1 offspring. Long read sequencing in twelve F1 sister plants revealed five large-scale structural rearrangements where both parents carried different homozygous alleles but the heterozygous F1 genomes were not identical heterozygotes as expected. Such spontaneous rearrangements were part of homoeologous exchanges or segmental deletions and were identified in different, individual F1 plants. The variants caused deletions, gene copy-number variations, diverging methylation patterns and other structural changes in large numbers of genes and may have been causal for unexpected phenotypic variation between individual F1 sister plants, for example strong divergence of plant height and leaf area. This example supports the hypothesis that spontaneous de novo structural rearrangements after de novo polyploidization can rapidly overcome intense allopolyploidization bottlenecks to re-expand crops genetic diversity for ecogeographical expansion and human selection. The findings imply that natural genome restructuring in allopolyploid plants from interspecific hybridization, a common approach in plant breeding, can have a considerably more drastic impact on genetic diversity in agricultural ecosystems than extremely precise, biotechnological genome modifications.

The enhanced performance of hybrids though heterosis remains a key aspect in plant breeding; nonetheless, the transcriptomic and epigenomic mechanisms behind it are still not fully elucidated. In the present study, gene expression, small RNA abundance and genome-wide methylation patterns were evaluated in hybrids from two distant Brassica napus ecotypes during seed and seedling developmental stages using next generation sequencing technologies. A total of 71217, 773, 79518 and 31825 differentially expressed genes, microRNAs, small interfering RNAs and differentially methylated regions were identified respectively. Approximately 70% of the differential expression and methylation patterns observed could be explained due to parental dominance levels. Reproductive, developmental, and meiotic gene copies following transgressive and paternal dominance patterns were found through gene ontology enrichment and microRNA-target association analyses. Interestingly, maternal dominance was more prominent in hypermethylated and downregulated features during seed formation which contrasts strikingly with the general maternal gamete demethylation occurring during gametogenesis in most plant species. Linkages between methylation and gene expression allowed the identification of putative genetic epialleles with diverse pivotal biological functions. Furthermore, most differentially methylated regions, differentially expressed siRNAs and transposable elements were found near gene flanking regions that had no differential expression, hence, indicating their potential role in conserving essential genomic and transcriptomic loci across the parents and offspring.

Key message Transcriptomic and epigenomic profiling of gene expression and small RNAs during seed and seedling development reveals expression and methylation dominance levels with implications on early stage heterosis in oilseed rape. Abstract The enhanced performance of hybrids through heterosis remains a key aspect in plant breeding; however, the underlying mechanisms are still not fully elucidated. To investigate the potential role of transcriptomic and epigenomic patterns in early expression of hybrid vigor, we investigated gene expression, small RNA abundance and genome-wide methylation in hybrids from two distant Brassica napus ecotypes during seed and seedling developmental stages using next-generation sequencing. A total of 31117, 344, 36229 and 7399 differentially expressed genes, microRNAs, small interfering RNAs and differentially methylated regions were identified, respectively. Approximately 70% of the differentially expressed or methylated features displayed parental dominance levels where the hybrid followed the same patterns as the parents. Via gene ontology enrichment and microRNA-target association analyses during seed development, we found copies of reproductive, developmental and meiotic genes with transgressive and paternal dominance patterns. Interestingly, maternal dominance was more prominent in hypermethylated and downregulated features during seed formation, contrasting to the general maternal gamete demethylation reported during gametogenesis in angiosperms. Associations between methylation and gene expression allowed identification of putative epialleles with diverse pivotal biological functions during seed formation. Furthermore, most differentially methylated regions, differentially expressed siRNAs and transposable elements were in regions that flanked genes without differential expression. This suggests that differential expression and methylation of epigenomic features may help maintain expression of pivotal genes in a hybrid context. Differential expression and methylation patterns during seed formation in an F1 hybrid provide novel insights into genes and mechanisms with potential roles in early heterosis.