Article

The evening complex coordinates environmental and endogenous signals in Arabidopsis

  • Nature Plants 3, Article number: 17087 (2017)
  • doi:10.1038/nplants.2017.87
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Abstract

Plants maximize their fitness by adjusting their growth and development in response to signals such as light and temperature. The circadian clock provides a mechanism for plants to anticipate events such as sunrise and adjust their transcriptional programmes. However, the underlying mechanisms by which plants coordinate environmental signals with endogenous pathways are not fully understood. Using RNA-sequencing and chromatin immunoprecipitation sequencing experiments, we show that the evening complex (EC) of the circadian clock plays a major role in directly coordinating the expression of hundreds of key regulators of photosynthesis, the circadian clock, phytohormone signalling, growth and response to the environment. We find that the ability of the EC to bind targets genome-wide depends on temperature. In addition, co-occurrence of phytochrome B (phyB) at multiple sites where the EC is bound provides a mechanism for integrating environmental information. Hence, our results show that the EC plays a central role in coordinating endogenous and environmental signals in Arabidopsis.

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Acknowledgements

We thank members of the Wigge laboratory for feedback and discussions. This work was supported by the Biotechnology and Biology Research Council (RG80054 to P.A.W.); P.A.W.'s laboratory is supported by a Fellowship from the Gatsby Foundation (GAT3273/GLB). Funding for open access charge: (Gatsby Foundation/GAT3273/GLB). We thank S. Kay for providing us with the gLUX-GFP lux-4 and gELF4-HA elf4-2 transgenic plants.

Author information

Author notes

    • Surojit Biswas

    Present address: Division of Medical Sciences, Harvard Medical School, Boston, Massachusetts 02115, USA.

Affiliations

  1. Sainsbury Laboratory, University of Cambridge, 47 Bateman Street, Cambridge CB2 1LR, UK

    • Daphne Ezer
    • , Jae-Hoon Jung
    • , Hui Lan
    • , Surojit Biswas
    • , Mathew S. Box
    • , Varodom Charoensawan
    • , Sandra Cortijo
    • , Xuelei Lai
    • , Dorothee Stöckle
    • , Katja E. Jaeger
    •  & Philip A. Wigge
  2. LPCV, CNRS, CEA, INRA, Univ. Grenoble Alpes, BIG, 38000 Grenoble, France

    • Laura Gregoire
    • , Xuelei Lai
    •  & Chloe Zubieta
  3. Department of Biochemistry, Faculty of Science, and Integrative Computational BioScience (ICBS) Center, Mahidol University, Bangkok 10400, Thailand

    • Varodom Charoensawan

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Contributions

D.E.: wrote a large proportion of the manuscript, lead researcher on all analysis. Involved in experimental design, prepared Figs 14. J.-H.J.: experimental design, generated Fig. 5, created lines used in the study. H.L.: extensive bioinformatics analysis. Mapped and analysed most of the datasets for the ChIP experiments. Performed motif searching and so on. S.B.: performed the initial mapping of the first ELF3 ChIP and made insights into rhythmical gene expression using clustering that were instrumental in the development of the project. L.G.: collaborating group. Performed the first analysis of EC binding and motif analysis. M.S.B.: generated the RNA-seq time course datasets. V.C.: generated the RNA-seq time course datasets. S.C.: generated the RNA-seq time course datasets. D.S.: helped perform ChIP-seq experiments. C.Z.: PI. Collaborator, supervisor of L.G., made key structural biology and experimental design contributions. Helped write the paper. K.E.J.: PI. Performed all the ChIP-seq experiments the paper is based on. Writing the paper and experimental design. P.A.W.: PI. Experimental design and discussions, helped write the paper.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Philip A. Wigge.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    Supplementary Figures 1–7.

Excel files

  1. 1.

    Supplementary Table 1

    A table containing information about the sequencing quality, such as the number of reads and the number of mapped reads, for each ChIP-seq experiment.

  2. 2.

    Supplementary Table 2

    A table containing ChIP-seq peaks predicted by MACS2 for ELF3, ELF4, and LUX at 22 °C and LUX at 17 °C.

  3. 3.

    Supplementary Table 3

    A table containing the details of all the statistical analysis (that is, the contingency tables used in the Fisher exact tests).

  4. 4.

    Supplementary Table 4

    A table containing information about both the de novo predicted motifs from HOMER2 and the occurrence of the G-box, LBS, and 'motif 2' motifs in the peaks that are within 3000 bp of differentially expressed genes.

  5. 5.

    Supplementary Table 5

    A table containing TPM values for the Col-0, elf3-1 and lux-4 time courses at 22 °C and 27 °C.

  6. 6.

    Supplementary Table 6

    A table containing the list of genes that are within the top 5% most differentially expressed in elf3-1 versus Col-0 or lux-4 versus Col-0 in at least one time point.

  7. 7.

    Supplementary Table 7

    A table containing lists the GO annotations of each of the predicted target genes from Supplementary Table 4.

  8. 8.

    Supplementary Table 8

    A table containing the raw data used in the production of Fig. 5a.