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Coupling of histone methylation and RNA processing by the nuclear mRNA cap-binding complex

Nature Plants volume 2, Article number: 16015 (2016) | Download Citation

Abstract

In eukaryotes, genes are transcribed into pre-mRNAs that are subsequently processed into mature mRNAs by adding a 5′-cap and a 3′-polyA tail and splicing introns. Pre-mRNA processing involves their binding proteins and processing factors, whereas gene transcription often involves chromatin modifiers. It has been unclear how the factors involved in chromatin modifications and RNA processing function in concert to control mRNA production. Here, we show that in Arabidopsis thaliana, the evolutionarily conserved nuclear mRNA cap-binding complex (CBC) forms multi-protein complexes with a conserved histone 3 lysine 4 (H3K4) methyltransferase complex called COMPASS-like and a histone 3 lysine 36 (H3K36) methyltransferase to integrate active histone methylations with co-transcriptional mRNA processing and cap preservation, leading to a high level of mature mRNA production. We further show that CBC is required for H3K4 and H3K36 trimethylation, and the histone methyltransferases are required for CBC-mediated mRNA cap preservation and efficient pre-mRNA splicing at their target loci, suggesting that these factors are functionally interdependent. Our study reveals novel roles for histone methyltransferases in RNA-processing-related events and provides mechanistic insights into how the ‘downstream’ RNA CBC controls eukaryotic gene transcription.

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Acknowledgements

We thank A. Jarmolowski for kindly providing the cbp20 seeds, Stanton B. Gelvin for BiFC vectors, and Heng Zhang for high-throughput sequencing of ChIP samples. This work was supported by funding from the Chinese Academy of Sciences and by a grant from the Singapore Ministry of Education (AcRF Tier 2; MOE2013-T2-1-025) to Y.H.

Author information

Author notes

    • Danhua Jiang

    Present address: Gregor Mendel Institute of Molecular Plant Biology, 1030 Vienna, Austria

    • Zicong Li
    •  & Danhua Jiang

    These authors contributed equally to this work.

Affiliations

  1. Shanghai Center for Plant Stress Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 201602, China

    • Zicong Li
    • , Xing Fu
    • , Xiao Luo
    • , Renyi Liu
    •  & Yuehui He
  2. Department of Biological Sciences and Temasek Life Sciences Laboratory, National University of Singapore, 117543 Singapore, Singapore

    • Zicong Li
    • , Danhua Jiang
    •  & Yuehui He

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Contributions

Y.H. conceived the research. Z.L., D.J. and X.L. conducted the experiments, Z.L., D.J., Y.H., X.F., X.L. and R.L. carried out data analyses. Y.H. and Z.L. wrote the paper.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Yuehui He.

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DOI

https://doi.org/10.1038/nplants.2016.15

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