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.
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Data availability
All the raw sequencing data generated during the current study are available in the Gene Expression Omnibus (GEO) database (https://www.ncbi.nlm.nih.gov/geo) under accession number GSE188724 and Genome Sequence Archive (https://bigd.big.ac.cn/gsa) under accession number PRJCA007017. Tracks for all sequencing data can be visualized through our local genome browser (http://49.233.173.230/JBrower/?data=triticum_aestivum).
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This work was supported by the Central Public-interest Scientific Institution Basic Research Found (S2022ZD02), the Excellent Young Scientists Fund (Overseas) of National Natural Science Foundation of China, the Fundamental Research Funds from the Institute of Crop Sciences, Chinese Academy of Agricultural Sciences (S2020YC07, S2021YC03), the Major Basic Research Program of Shandong Natural Science Foundation (ZR2019ZD15) and the Top Talents Program “One Case One Discussion (Yishiyiyi)” of Shandong Province, China. We would like to acknowledge Prof. Robert J. Schmitz from the University of Georgia for revising the manuscript and Ting Li from the Flow Cytometry Core of the Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, for the help with the nuclear sorting.
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Pei, H., Teng, W., Gao, L. et al. Low-affinity SPL binding sites contribute to subgenome expression divergence in allohexaploid wheat. Sci. China Life Sci. 66, 819–834 (2023). https://doi.org/10.1007/s11427-022-2202-3
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DOI: https://doi.org/10.1007/s11427-022-2202-3