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

Abstract

Allopolyploidy involves the hybridization of two evolutionary diverged species and the doubling of genomic material. Frequently, allopolyploids exhibit genomic rearrangements that recombine, duplicate, or delete homoeologous regions of the newly formed genome. While decades of investigation have focused on how genome duplication leads to systematic differences in the retention and expression of duplicate genes, the impact of genomic rearrangements on genome evolution has received less attention. We used genomic and transcriptomic data for six independently resynthesized, isogenic Brassica napus lines in the first, fifth, and tenth generation to identify genomic rearrangements and assess their impact on gene expression dynamics related to subgenome dominance and gene dosage constraint. We find that dosage constraints on the gene expression response to polyploidy begin to loosen within the first ten generations of evolution and systematically differ between dominant and non-dominant subgenomes. We also show that genomic rearrangements can bias estimation of homoeolog expression bias, but fail to fully obscure which subgenome is dominantly expressed. Finally, we demonstrate that dosage-sensitive genes exhibit the same kind of coordinated response to homoeologous exchange as they do for genome duplication, suggesting constraint on dosage balance also acts on these changes to gene dosage.

Transgressive and parental dominant gene expression and cytosine methylation during seed development in Brassica napus hybrids

“…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 F 1 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.…”

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.…”

“…Most frequently differentially methylated transposable elements corresponded to those more abundant in the Express 617 reference (Lee et al, 2020) like the Copia and Gypsy families. Transposable elements are considered not only as key factors in speciation and subgenome expression patterns (Bird et al, 2018; Bottani et al, 2018; Bird et al, 2021b) but also as genomic features with high variability across plant species (Novák et al, 2020; Mhiri et al, 2022). In addition, comparison of transposable element densities and compositions between Express 617 and G3D001 through genome assembly of the latter would provide more insights into how TEs diverge during seed development and between cultivars.…”

“…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.…”