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Low-affinity SPL binding sites contribute to subgenome expression divergence in allohexaploid wheat [ATAC-seq]

ABSTRACT: Expression divergence caused by genetic variation and crosstalks among subgenomes of the allohexaploid bread wheat (Triticum aestivum. L., BBAADD) is hypothesized to increase its adaptability and/or plasticity. However, the molecular basis of expression divergence remains unclear. Squamosa promoter-binding protein-like (SPL) transcription factors are critical for a wide array of biological processes. In this study, we constructed expression regulatory networks by combining DAP-seq for 40 SPLs, ATAC-seq, and RNA-seq. Our findings indicate that a group of low-affinity SPL binding regions (SBRs) were targeted by diverse SPLs and caused different sequence preferences around the core GTAC motif. The SBRs including the low-affinity ones are evolutionarily conserved, enriched GWAS signals related to important agricultural traits. However, those SBRs are highly diversified among the cis-regulatory regions (CREs) of syntenic genes, with less than 8% SBRs coexisting in triad genes, suggesting that CRE variations are critical for subgenome differentiations. Knocking out of TaSPL7A/B/D and TaSPL15A/B/D subfamily further proved that both high- and low-affinity SBRs played critical roles in the differential expression of genes regulating tiller number and spike sizes. Our results have provided baseline data for downstream networks of SPLs and wheat improvements and revealed that CRE variations are critical sources for subgenome divergence in the allohexaploid wheat.

ORGANISM(S): Triticum aestivum

PROVIDER: GSE188696 | GEO | 2022/11/28

REPOSITORIES: GEO

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Project description:The three subgenomes (B, A and D) of common wheat (2n=6x=42) are largely intact, which makes extraction of the BBAA subgenomes as organismally independent genomes possible. Availability of such novel extracted tetraploid wheat (Extracted-tetra) provides a unique opportunity to study whether and to what extent the BBAA subgenomes of common wheat have been irreversibly modified, as well as its attendant biological consequences, during their evolutionary trajectory as allohexaploidy. We report here that the extracted-tetra is stable in karyotype but with severely deteriorated phenotypes. Microarray-based transcriptome analysis revealed a substantial portion of differentially expressed genes (down- or up-regulation) between extracted and natural tetraploid wheat, Triticum turgidum, which exceeded the transcriptome divergence at tetraploid level, implying reinforced effects of allopolyploidization and domestication at the allohexaploid level. Great majority of the differentially expressed genes showed additive expression in a resynthesized allohexaploid wheat (parented by Extracted-tetra), indicating transcriptome modifications to the BBAA subgenomes are largely irreversible. Analysis of a newly synthesized allohexaploid wheat (parented by T. turgidum) suggests that whereas most of the modified genes are accrued evolutionary changes, some showed immediate regulation post-allohexaploidization and evolutionary perseverance. Homeologue-specific pyrosequencing of 44 genes revealed either concordant or independent expression changes to the B and A homeologues. The Extracted-tetra vs.T. turgidum down-regulated genes showed enrichment for distinct GO categories. Structurally, the three constituent subgenomes of common wheat, BB, AA and DD, are largely intact with only a few inter-subgenomic translocations. Because of these unique attributes, it is feasible to extract the BBAA subgenomes from the common wheat BBAADD genome by hybridization to a durum line and repeated back-crossing to the hexaploid parent, restituting a novel type of extracted tetraploid wheat, namely Extracted-tetr, with a genome constitution BBAA, virtually identical to the subgenomes BBAA of its common wheat donor. Availability of the extracted-tetra, the resynthesized allohexaploid wheat parented by the extracted-tetra, and newly synthesized allohexaploid wheat parented by natural tetraploid wheat, T. turgidum, provides an excellent system to address the issues of whether and to what extent transcriptome modifications to the BBAA subgenomes of common wheat have occurred since its formation ca. 10,000 years ago, timing of the modifications, and their biological consequences. Here, we have addressed these issues by microarray-based transcriptome analysis.

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Low-affinity SPL binding sites contribute to subgenome expression divergence in allohexaploid wheat [ATAC-seq]

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