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MED25 connects enhancer–promoter looping and MYC2-dependent activation of jasmonate signalling

Abstract

The lipid-derived hormone jasmonate (JA) regulates plant immunity and adaptive growth by triggering a genome-wide transcriptional programme. In Arabidopsis thaliana, JA-triggered transcriptional programming is largely orchestrated by the master transcription factor MYC2. The function of MYC2 is dependent on its physical interaction with the MED25 subunit of the Mediator transcriptional co-activator complex. Here we report the identification of JA enhancers (JAEs) through profiling the occupancy pattern of MYC2 and MED25. JA regulates the dynamic chromatin looping between JAEs and their promoters in a MED25-dependent manner, while MYC2 auto-regulates itself through JAEs. Interestingly, the JAE of the MYC2 locus (named ME2) positively regulates MYC2 expression during short-term JA responses but negatively regulates it during constant JA responses. We demonstrate that new gene editing tools open up new avenues to elucidate the in vivo function of enhancers. Our work provides a paradigm for functional study of plant enhancers in the regulation of specific physiological processes.

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Fig. 1: Prediction of JA enhancers co-occupied by MYC2 and MED25.
Fig. 2: Hormone treatment enhances the binding enrichment of MYC2 and MED25 to the predicted JA enhancers.
Fig. 3: Hormone treatment promotes chromatin loop formation between predicted JAEs and the corresponding promoters.
Fig. 4: Disruption of MYC2 and MED25 impairs MeJA-induced chromatin loop formation between predicted JA enhancers and their target promoters.
Fig. 5: JA responses of me2 mutants in response to short-term MeJA treatment.
Fig. 6: JA responses of me2 mutants in response to long-term MeJA treatment.

Data availability

All sequencing data have been deposited under accession number CRA001078 (Bioproject Accession: PRJCA001012, Experiment Accessions: CRR032459, CRR032460, CRR032461, CRR032462, CRR032463) and are available from the website of the Genome Sequence Archive (GSA) (http://bigd.big.ac.cn/bioproject/browse/PRJCA001012) of the Beijing Institute of Genomics Data Center.

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Acknowledgements

We thank Q. Xie for providing the Yao promoter-driven CRISPR–Cas9 system. This work was supported by the National Key Research and Development Programme of China (No. 2016YFD0100600), the Strategic Priority Research Programme of the Chinese Academy of Sciences (No. XDB11030200), the National Natural Science Foundation of China (No. 31730010), and the Tai-Shan Scholar Programme from Shandong Province.

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Contributions

J.Z. and C.L. designed the project. H.W., S.L., Y.L., R.Z., W.S. and Q.C. performed the experiments. Y.X., Y.W. and X.-J.W. performed the bioinformatics analysis. C.L. and J.Z. wrote the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Chuanyou Li or Jiuhai Zhao.

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The authors declare no competing interests.

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Journal Peer Review Information: Nature Plants thanks Kemal Kezan, Roberto Solano and other anonymous reviewers for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–6, Supplementary Tables 1 and 2

Reporting Summary

Supplementary datasets 1–6

Supplementary dataset 1, Occupancy profile of MYC2. Supplementary dataset 2, Occupancy profile of MED25. Supplementary dataset 3, MMOSs (co-occupancy sites of MYC2 and MED25). Supplementary dataset 4, MMOSs with G-box. Supplementary dataset 5, Putative JAEs. Supplementary dataset 6, Representatice JAEs.

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Wang, H., Li, S., Li, Y. et al. MED25 connects enhancer–promoter looping and MYC2-dependent activation of jasmonate signalling. Nat. Plants 5, 616–625 (2019). https://doi.org/10.1038/s41477-019-0441-9

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