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The evening complex coordinates environmental and endogenous signals in Arabidopsis

Nature Plants volume 3, Article number: 17087 (2017) Cite this article

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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.

Plants are sensitive to their environment, and the distribution and phenology of plants has already altered in response to climate change1,2. Such growth and developmental changes require the integration of multiple environmental signals, such as light and temperature, into endogenous gene expression programmes. The circadian clock plays a key role in this process by enabling plants to anticipate future events such as sunrise and darkness as well as gating responses to environmental information according to time of day3–5. The expression levels of many circadian clock genes vary in response to changes in the environment6, but the underlying mechanisms by which these signals are integrated are not known. The circadian clock in Arabidopsis contains multiple interlocking loops with transcriptional and post-translational regulation. Three circadian clock genes, EARLY FLOWERING3, 4 (ELF3 and 4) and the MYB transcription factor LUX ARRYTHMO (LUX) together comprise the evening complex (EC)5,7, and are expressed at the end of the day. The EC coordinates elongation growth in Arabidopsis seedlings, as it directly represses the expression of the bHLH transcription factor PHYTOCHROME INTERACTING FACTOR 4 (PIF4) (refs 7–9). PIF4 is necessary for warm temperature-mediated elongation growth10, and pif4 and pif4,5 mutants also display a reduced induction of flowering in response to warm temperature11–14. Natural variation in the activity of the EC is responsible for differences in thermal responsiveness and warmer temperatures reduce the binding of the EC to target promoters, resulting in increased PIF4 expression15,16.

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Figure 1: There is a high degree of overlap of binding sites for ELF3, ELF4 and LUX genome-wide.
Figure 2: The EC regulates a wide set of target genes controlling major biological processes in the plant, particularly the circadian clock, photosynthesis, temperature signalling, growth and phytohormone signalling.
Figure 3: The EC directly regulates many genes that are rhythmically expressed.
Figure 4: The EC affects temperature response genome-wide.
Figure 5: EC target genes are temperature responsive.
Figure 6: The EC and phytochrome temperature response is additive in seedlings.

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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.

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  1. Surojit Biswas

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

Authors and Affiliations

  1. Sainsbury Laboratory, University of Cambridge, 47 Bateman Street, CB2 1LR, Cambridge, 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, 10400, Bangkok, 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 1–4. 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.

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Correspondence to Philip A. Wigge.

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Supplementary information

Supplementary Information

Supplementary Figures 1–7. (PDF 43186 kb)

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. (XLSX 38 kb)

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. (XLSX 180 kb)

Supplementary Table 3

A table containing the details of all the statistical analysis (that is, the contingency tables used in the Fisher exact tests). (XLSX 22 kb)

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. (XLSX 197 kb)

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. (XLSX 33808 kb)

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. (XLSX 178 kb)

Supplementary Table 7

A table containing lists the GO annotations of each of the predicted target genes from Supplementary Table 4. (XLSX 84 kb)

Supplementary Table 8

A table containing the raw data used in the production of Fig. 5a. (XLSX 40 kb)

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Ezer, D., Jung, JH., Lan, H. et al. The evening complex coordinates environmental and endogenous signals in Arabidopsis. Nature Plants 3, 17087 (2017). https://doi.org/10.1038/nplants.2017.87

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