Dynamic control of enhancer activity drives stage-specific gene expression during flower morphogenesis

Wenhao Yan,Julia Schumacher,Cristel C Carles,Diego Durantini,Kerstin Kaufmann,Ming Chen,Dijun Chen,Julia Engelhorn

doi:10.1038/s41467-019-09513-2

Abstract

Enhancers are critical for developmental stage-specific gene expression, but their dynamic regulation in plants remains poorly understood. Here we compare genome-wide localization of H3K27ac, chromatin accessibility and transcriptomic changes during flower development in Arabidopsis. H3K27ac prevalently marks promoter-proximal regions, suggesting that H3K27ac is not a hallmark for enhancers in Arabidopsis. We provide computational and experimental evidence to confirm that distal DNase І hypersensitive sites are predictive of enhancers. The predicted enhancers are highly stage-specific across flower development, significantly associated with SNPs for flowering-related phenotypes, and conserved across crucifer species. Through the integration of genome-wide transcription factor (TF) binding datasets, we find that floral master regulators and stage-specific TFs are largely enriched at developmentally dynamic enhancers. Finally, we show that enhancer clusters and intronic enhancers significantly associate with stage-specific gene regulation by floral master TFs. Our study provides insights into the functional flexibility of enhancers during plant development, as well as hints to annotate plant enhancers.

Highlights

Enhancers are critical for developmental stage-specific gene expression, but their dynamic regulation in plants remains poorly understood
We found that H3K27ac prevalently marks promoters but rarely localizes in distal regulatory regions, suggesting that H3K27ac is not a hallmark for active enhancers in Arabidopsis thaliana as it is in metazoans[22], and as data from rice and maize indicate[23,24]
To further investigate whether other histone modifications are hallmarks of enhancers annotated by distal DNase I hypersensitivity sites (DHSs), we extended our analyses by using a large catalog of histone modifications, including H3K27ac, H3K4me[1], H3K4me[2], H3K4me[3], H3K9ac, H3K9me[2], H3K27me[3], and H3K36me[3], for which datasets were generated from Arabidopsis thaliana seedlings[20,30] (Fig. 2d)

Summary

Introduction

Enhancers are critical for developmental stage-specific gene expression, but their dynamic regulation in plants remains poorly understood. Through the integration of genome-wide transcription factor (TF) binding datasets, we find that floral master regulators and stage-specific TFs are largely enriched at developmentally dynamic enhancers. Correspondence and requests for materials should be addressed to Multicellular development is controlled by precise spatiotemporal regulation of gene expression, which is largely accomplished through the activation and repression via cis-regulatory elements within the promoterproximal or distal regulatory regions, such as enhancers. Promoters and enhancers are noncoding DNA sequences that can be bound by multiple regulatory proteins, especially transcription factors (TFs) to activate the expression of target genes[1]. Contrary to the fast growing knowledge of the regulatory function of enhancers in metazoans, knowledge of genome-wide landscapes of plant enhancers and their dynamic activities remains limited in the context of developmental stage-specific gene regulation[15]. In 2012, Zhang et al reported the mapping of open chromatin in rice seedlings and callus using

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