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The prevalence, evolution and chromatin signatures of plant regulatory elements

Abstract

Chromatin accessibility and modification is a hallmark of regulatory DNA, the study of which led to the discovery of cis-regulatory elements (CREs). Here, we characterize chromatin accessibility, histone modifications and sequence conservation in 13 plant species. We identified thousands of putative CREs and revealed that distal CREs are prevalent in plants, especially in species with large and complex genomes. The majority of distal CREs have been moved away from their target genes by transposable-element (TE) proliferation, but a substantial number of distal CREs also seem to be created by TEs. Finally, plant distal CREs are associated with three major types of chromatin signatures that are distinct from metazoans. Taken together, these results suggest that CREs are prevalent in plants, highly dynamic during evolution and function through distinct chromatin pathways to regulate gene expression.

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Fig. 1: The prevalence of distal accessible regions is a consequence of genome size.
Fig. 2: dACRs are preserved between species.
Fig. 3: TEs play important roles in the distribution of ACRs across plant genomes.
Fig. 4: ACRs are characterized by distinct and conserved chromatin states depending on their distance to genes.
Fig. 5: The chromatin states of dACRs are conserved between species.

Data availability

The data generated in this study have been uploaded to the Gene Expression Omnibus (GEO) database and can be retrieved through accession number GSE128434. The data from this study can also be viewed interactively on the publicly accessible epigenome browser at http://epigenome.genetics.uga.edu/PlantEpigenome/.

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Acknowledgements

We thank R. Deal for providing the H2A.Z antibodies used in this study. This work was funded by the NSF IOS-1546867 and NSF IOS-1856627 to R.J.S. and X.Z., NSF IOS-1238142 to X.Z. and NSF IOS-1339194 to R.J.S. R.J.S. acknowledges support from the Technical University of Munich-Institute for Advanced Study funded by the German Excellent Initiative and the European Seventh Framework Programme under grant agreement no. 291763. R.J.S. is a Pew Scholar in the Biomedical Sciences, supported by The Pew Charitable Trusts.

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Contributions

X.Z. and R.J.S conceived and designed experiments. Z.L. performed experiments. Z.L., A.P.M., W.A.R. and C.L.E. analysed the data. Z.L., X.Z. and R.J.S. wrote the paper.

Corresponding authors

Correspondence to Xiaoyu Zhang or Robert J. Schmitz.

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Competing interests

R.J.S. and X.Z. are co-founders of REquest Genomics, LLC, a company that provides epigenomics services.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–10.

Reporting Summary

Supplementary Tables

Supplementary Table 1: ACRs identified in A. thaliana. Supplementary Table 2: ACRs identified in E. salsugineum. Supplementary Table 3: ACRs identified in P. trichocarpa. Supplementary Table 4: ACRs identified in P. vulgaris. Supplementary Table 5: ACRs identified in G. max. Supplementary Table 6: ACRs identified in S. polyrhiza. Supplementary Table 7: ACRs identified in A. officinalis. Supplementary Table 8: ACRs identified in B. distachyon. Supplementary Table 9: ACRs identified in H. vulgare. Supplementary Table 10: ACRs identified in O. Sativa. Supplementary Table 11: ACRs identified in S. viridis. Supplementary Table 12: ACRs identified in S. bicolor. Supplementary Table 13: ACRs identified in Z. mays. Supplementary Table 14: summary statistics for ATAC-seq. Supplementary Table 15: summary statistics for ChIP-seq. Supplementary Table 16: summary statistics for RNA-seq.

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Lu, Z., Marand, A.P., Ricci, W.A. et al. The prevalence, evolution and chromatin signatures of plant regulatory elements. Nat. Plants 5, 1250–1259 (2019). https://doi.org/10.1038/s41477-019-0548-z

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