Frequent spontaneous structural rearrangements promote rapid genome diversification in a Brassica napus F1 generation

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.

Transgressive and parental dominant gene expression and cytosine methylation during seed development inBrassica napushybrids

“…Expression and methylation dominance levels are a fast way of interpretating -omics data, and to our knowledge, the present study is the first one to analyze expression and methylation dominance level patterns in hybrids derived from two Brassica napus parents. Recent advances in allele specific expression (Fan et al, 2020;Sands et al, 2021), isoform expression (Vitting-Seerup and Sandelin, 2019;Yao et al, 2020;Golicz et al, 2021), gene fusion and dosage (Mahmoud et al, 2019;Serin Harmanci et al, 2020;Bird et al, 2021b) as well as non-germline -omics variations among F1 plants and populations (Higgins et al, 2018;Cortijo et al, 2019;Orantes-Bonilla et al, 2022;Quezada-Martinez et al, 2022) would prove useful in improving the resolution of ELD and MLD analyses. Furthermore, multi-omics features have been employed in genomic selection in plants; hence, defining the role from each -omic feature per stage could be used to enhance expression and phenotype prediction modelling in B.napus (Seifert et al, 2018;Zrimec et al, 2020;Cheng et al, 2021;H.…”

“…The extent of these features in an allopolyploid model crop like B. napus also have potential implications in other polyploid crops where heterosis still remains to be exploited, such as wheat and potatoes (Steeg et al, 2022). Patterns of expression and methylation dominance levels could also contribute a new level of understand regarding allele-specific gene expression (Fan et al, 2020; Sands et al, 2021), isoform expression (Vitting-Seerup and Sandelin, 2019; Yao et al, 2020; Golicz et al, 2021), gene fusion and dosage (Mahmoud et al, 2019; Serin Harmanci et al, 2020; Bird et al, 2021b) as well as non-germline omics variations among F1 plants and populations (Higgins et al, 2018; Cortijo et al, 2019; Orantes-Bonilla et al, 2022; Quezada-Martinez et al, 2022). Their role in heterotic gene expression patterns is ultimately also of interest for transcriptome-based genomic selection or hybrid performance prediction (e.g.…”

“…Therefore, detailed assessment of transposable element densities and compositions between hybrids and their parents could be beneficial. Seerup and Sandelin, 2019;Yao et al, 2020;Golicz et al, 2021), gene fusion and dosage (Mahmoud et al, 2019;Serin Harmanci et al, 2020;Bird et al, 2021b) as well as non-germline omics variations among F1 plants and populations (Higgins et al, 2018;Cortijo et al, 2019;Orantes-Bonilla et al, 2022;Quezada-Martinez et al, 2022). Their role in heterotic gene expression patterns is ultimately also of interest for transcriptome-based genomic selection or hybrid performance prediction (e.g.…”

“…Additionally, plots showing DEGs and methylation levels for each chromosome and stage, centromere loci and repeat density were made using the circlize package (Gu et al, 2014). Repeat density for each 1 kbp bin within each chromosome was calculated using bedtools while predicted Express 617 centromere loci were added based on Orantes-Bonilla et al (2022).…”

Dosage-sensitivity shapes how genes transcriptionally respond to allopolyploidy and homoeologous exchange in resynthesized Brassica napus

“…Early studies in resynthesized polyploids showed extensive genetic changes in a short period of time (Song et al 1995). Subsequent investigations showed major genome structural changes from the first meiosis after polyploid formation, primarily in the form of homoeologous exchanges which can result in partial or complete deletion and duplication of chromosomal segments (Sharpe et al 2005;Osborn et al 2003;Jenczewski et al 2003;Pires et al 2004;Gaeta et al 2007;Nicolas et al 2007;Szadowski et al 2010;Xiong et al 2011;Chalhoub et al 2014;He et al 2017;Rousseau-Geutin et al 2017;Samans et al 2017;Stein et al 2017;Hurgobin et al 2018;Lloyd et al 2018;Pele et al 2018;Mason and Wendel 2020;Bayer et al 2021;Chawla et al 2021;Ferreira de Carvalho et al 2021;Higgins et al 2021;Xiong et al 2021;Orantes-Bonilla et al 2022). These rearrangements continue to accumulate over time, generating genomic diversity in early polyploids (Gaeta and Pires 2010;Xiong et al 2011;Mason and Wendel, 2020;Bird et al 2021).…”