Accessible chromatin regions and DNA methylation regulate gene expression leading to changes in agronomic traits in Brassica allotriploid hybrids

IntroductionInterspecific hybridization is a common method in plant breeding to combine traits from different species, resulting in allopolyploidization and significant genetic and epigenetic changes. However, our understanding of genome-wide chromatin and gene expression dynamics during allopolyploidization remains limited. ObjectivesWe aimed to explore the relationship and underlying mechanisms between accessible chromatin regions and DNA methylation and gene transcription in genome-wide reorganization after interspecific hybridization. MethodsThis study generated two Brassica allotriploid hybrids via interspecific hybridization, combining transcriptomics, whole-genome bisulfite sequencing (WGBS) and assay for transposase-accessible chromatin with high throughput sequencing (ATAC-seq), revealing that accessible chromatin regions (ACRs) and DNA methylation regulate gene expression after interspecific hybridization, ultimately influencing the agronomic traits of the hybrids. ResultsA total of 234,649 ACRs were identified in the parental lines and hybrids, the hybridization process induces changes in the distribution and abundance of there accessible chromatin regions, particularly in gene regions and their proximity. On average, genes associated with Proximal ACRs were more highly expressed than the genes associated with Distal and Genic ACRs. More than half of novel ACRs drove transgressive gene expression in the hybrids, and the transgressive up-regulated genes showed significant enrichment in metal ion binding, especially magnesium ion, calcium ion, and potassium ion binding. We also identified the Bna.bZIP11 in the single-parent activation ACR (SPA-ACR), which binds to BnaA06.UF3GT to promote anthocyanin accumulation in F1 hybrids. Additionally, in F1 hybrids, the level of DNA methylation in ACRs was higher compared to gene bodies, and the A-subgenome ACRs were associated with genome dosage rather than DNA methylation. ConclusionsThe interplay among DNA methylation, TEs, and sRNA contributes to the dynamic landscape of ACRs during interspecific hybridization, resulting in distinct gene expression patterns on the genome. HIGHLIGHTSO_LIThe study utilized the accessible chromatin regions (ACR) and DNA methylation to elucidate the mechanism behind gene expression changes following interspecific hybridization. C_LIO_LIWhole-genome recombination after interspecific hybridization leads to the rearrangement of ACR, and novel ACR and single-parent activation ACR regulate the expression of genes. C_LIO_LIDNA methylation plays a role in repressing gene expression within ACRs, and unmethylated ACRs have more transcriptionally active. C_LIO_LIA-subgenome ACRs were associated with genome dosage rather than DNA methylation. C_LI GRAPHICAL ABSTRACT O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=125 SRC="FIGDIR/small/613586v1_ufig1.gif" ALT="Figure 1"> View larger version (32K): org.highwire.dtl.DTLVardef@1504e51org.highwire.dtl.DTLVardef@145b0b8org.highwire.dtl.DTLVardef@551847org.highwire.dtl.DTLVardef@ace197_HPS_FORMAT_FIGEXP M_FIG C_FIG