Dynamics of cis -regulatory sequences and transcriptional divergence of duplicated genes in soybean

Abstract

Transcriptional divergence of duplicated genes after whole genome duplication (WGD) has been described in many plant lineages and is often associated with subgenome dominance, a genome-wide mechanism. However, it is unknown what underlies the transcriptional divergence of duplicated genes in polyploid species that lack subgenome dominance. Soybean is a paleotetraploid with a WGD that occurred 5 to 13 Mya. Approximately 50% of the duplicated genes retained from this WGD exhibit transcriptional divergence. We developed accessible chromatin region (ACR) datasets from leaf, flower, and seed tissues using MNase-hypersensitivity sequencing. We validated enhancer function of several ACRs associated with known genes using CRISPR/Cas9-mediated genome editing. The ACR datasets were used to examine and correlate the transcriptional patterns of 17,111 pairs of duplicated genes in different tissues. We demonstrate that ACR dynamics are correlated with divergence of both expression level and tissue specificity of individual gene pairs. Gain or loss of flanking ACRs and mutation of cis -regulatory elements (CREs) within the ACRs can change the balance of the expression level and/or tissue specificity of the duplicated genes. Analysis of DNA sequences associated with ACRs revealed that the extensive sequence rearrangement after the WGD reshaped the CRE landscape, which appears to play a key role in the transcriptional divergence of duplicated genes in soybean. This may represent a general mechanism for transcriptional divergence of duplicated genes in polyploids that lack subgenome dominance.

A spatially resolved multiomic single-cell atlas of soybean development

“…Activating ACRs were more likely to act proximally compared to repressing ACRs (Figure 3K). Notably, we identified three known activating CREs expressed in different tissues and involved diverse developmental pathways (Figure 3N-P), such as in seed tissues, 35 ASYMMETRIC LEAVES2-LIKE 18 (ASL18) , a known root nodule symbiosis marker, 36 and a pod shattering-resistance related gene 37 .…”

Dynamics of accessible chromatin regions and subgenome dominance in octoploid strawberry

“…Chromatin accessibility levels of the 5′ ACRs of active genes are positively correlated with the expression levels of the genes 77 . In addition, enhancer functions of ACRs located outside of promoter regions, including those located in the introns, have been demonstrated in several plant species 25 , 71 , 78 . Therefore, the number of ACRs and the chromatin accessibility level of each ACR can be used to measure and compare the activity and divergence of duplicated genes or homoeologous genes.…”

“…Therefore, the number of ACRs and the chromatin accessibility level of each ACR can be used to measure and compare the activity and divergence of duplicated genes or homoeologous genes. We recently demonstrated that gain or loss of DNA sequences and mutation of cis -regulatory elements located within flanking ACRs can change the balance of the expression level and/or tissue specificity of duplicated genes in soybean 25 . In the current study, we found that the dominant subgenome A contains a greater number of total MHSs and MHS per gene than the submissive B/C/D subgenomes.…”

“…Although subgenome dominance has been documented in a number of plant species, not all polyploids exhibit subgenome dominance 22 – 25 . The lack of subgenome dominance was thought to be skewed toward autopolyploids or polyploids with highly similar subgenomes 26 – 28 .…”

Identification of the New GmJAG1 Transcription Factor Binding Motifs Using DAP-Seq

“…In contrast to human or model plants (e.g., Arabidopsis), there are many databases with abundant sequencing data for understanding the function of noncoding regions, such as the human ENCODE (https://www.encodeproject.org accessed on 1 May 2024) and the Arabidopsis Cistrome database [20]. Although soybean also has abundant DNA resequencing data characterizing the single nucleotide polymorph (SNP) or structural variation (SV) at the genomic level, for example, the recently published soybean PAN-genome data [21], few high-throughput sequencing data (e.g., ATAC-seq) [22][23][24] have been aimed at finding these functional non-coding elements (e.g., motifs) in the soybean genome. Compared to the ChIP-seq method [14], a traditional strategy for discovering new motifs, DAP-seq [15] is able to select the DNA fragments directly bound by the recombinant TF in vitro, which showed some advantage over the ChIP-seq in finding motifs.…”