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Cytosolic acetyl-CoA promotes histone acetylation predominantly at H3K27 in Arabidopsis

Nature Plants volume 3, pages 814–824 (2017)Cite this article

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Abstract

Acetyl-coenzyme A (acetyl-CoA) is a central metabolite and the acetyl source for protein acetylation, particularly histone acetylation that promotes gene expression. However, the effect of acetyl-CoA levels on histone acetylation status in plants remains unknown. Here, we show that malfunctioned cytosolic acetyl-CoA carboxylase1 (ACC1) in Arabidopsis leads to elevated levels of acetyl-CoA and promotes histone hyperacetylation predominantly at lysine 27 of histone H3 (H3K27). The increase of H3K27 acetylation (H3K27ac) is dependent on adenosine triphosphate (ATP)-citrate lyase which cleaves citrate to acetyl-CoA in the cytoplasm, and requires histone acetyltransferase GCN5. A comprehensive analysis of the transcriptome and metabolome in combination with the genome-wide H3K27ac profiles of acc1 mutants demonstrate the dynamic changes in H3K27ac, gene transcripts and metabolites occurring in the cell by the increased levels of acetyl-CoA. This study suggests that H3K27ac is an important link between cytosolic acetyl-CoA level and gene expression in response to the dynamic metabolic environments in plants.

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Fig. 1: Identification and characterization of a new mutant of ACC1.
Fig. 2: Hyperacetylation of H3K27 is associated with the accumulation of acetyl-CoA in acc1 mutants.
Fig. 3: Genome-wide analysis of H3K27ac in acc1.
Fig. 4: Increased H3K27ac in acc1-5 depends on the activity of ACL.
Fig. 5: Histone acetyltransferase GCN5/HAG1 is required for the increased H3K27ac in acc1-5.
Fig. 6: Transcriptome and metabolome analysis of acc1-5 seedlings.

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Acknowledgements

We thank R. Menassa and N. Hüner for helpful discussions, M. Tasaka for the seeds of gk101 (acc1-4), J.L. Micol for the seeds of elo3 (elp3), ABRC for the seeds of T-DNA insertion lines, and A. Molnar for help with preparing the figures. This work was supported by grants from the Natural Science and Engineering Research Council of Canada (R4019A01, to Y.C.), Agriculture and Agri-Food Canada (to Y.C.) and National Natural Science Foundation of China (31371715, to J.L.). C.C. was supported by a graduate fellowship from the Chinese Scholarship Council.

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  1. Chen Chen and Chenlong Li contributed equally to this work

Authors and Affiliations

  1. Agriculture and Agri-Food Canada, London Research and Development Centre, London, Ontario, N5V 4T3, Canada

    Chen Chen, Chenlong Li, Ying Wang, Justin Renaud, Gang Tian, Shrikaar Kambhampati, Behnaz Saatian, Vi Nguyen, Abdelali Hannoufa, Frédéric Marsolais, Ze-Chun Yuan, Ryan S. Austin, Jun Liu & Yuhai Cui

  2. Department of Biology, Western University, London, Ontario, N6A 5B7, Canada

    Chen Chen, Shrikaar Kambhampati, Behnaz Saatian, Abdelali Hannoufa, Frédéric Marsolais, Ryan S. Austin, Susanne E. Kohalmi & Yuhai Cui

  3. State Key Laboratory of Biocontrol and Guangdong Key Laboratory of Plant Resource, School of Life Sciences, Sun Yat-sen University, Guangzhou, China

    Chenlong Li & Shangzhi Huang

  4. Agriculture and Agri-Food Canada, Harrow Research and Development Centre, Harrow, Ontario, N0R 1G0, Canada

    Kangfu Yu

  5. Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, China

    Jun Liu

  6. Institute of Plant Biology, College of Life Science, National Taiwan University, Taipei, 106, Taiwan

    Keqiang Wu

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Contributions

C.C. and Y.C. conceived and designed the experiments; C.C., Y.W. and A.H. quantified the level of acetyl-CoA; J.R and C.C performed metabolome profiling; J.R., F. M. and S.K. analysed the metablomic data; G.T., B.S. and R.S.A. conducted mapping of p1045. V.N. and Z.C.Y. performed all the Sanger DNA sequencing; C.C. performed all the rest of the experiments; C.C., C.L., Z.C.Y., J.L., K.Y., S.E.K., S.H. and K.W. analysed ChIP-seq and RNA-seq data; C.C., C.L. and Y.C. wrote the paper.

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Correspondence to Yuhai Cui.

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Supplementary Information

Supplementary Figures 1-18, Supplementary Tables 1-3

Life Sciences Reporting Summary

Supplementary Dataset 1 H3K27ac targets identified by ChIP-seq in WT and acc1-5

Supplementary Dataset 2 List of genes with increased and decreased H3K27ac in acc1-5

41477_2017_23_MOESM5_ESM.xlsx

Supplementary Dataset 3 List of genes with increased and decreased acetylations (at lysine residues other than H3K27) in acc1-5

41477_2017_23_MOESM6_ESM.xlsx

Supplementary Dataset 4 Transcripts significantly changed in acc1-5 identified from RNA-seq and lists of genes in 7 functional categories

Supplementary Dataset 5 List of detected and identified metabolite features from both +ve and –ve mode

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Chen, C., Li, C., Wang, Y. et al. Cytosolic acetyl-CoA promotes histone acetylation predominantly at H3K27 in Arabidopsis . Nature Plants 3, 814–824 (2017). https://doi.org/10.1038/s41477-017-0023-7

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