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Trithorax-group protein ATX5 mediates the glucose response via impacting the HY1-ABI4 signaling module

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Trithorax-group Protein ARABIDOPSIS TRITHORAX5 modulates the glucose response.

Abstract

Glucose is an evolutionarily conserved modulator from unicellular microorganisms to multicellular animals and plants. Extensive studies have shown that the Trithorax-group proteins (TrxGs) play essential roles in different biological processes by affecting histone modifications and chromatin structures. However, whether TrxGs function in the glucose response and how they achieve the control of target genes in response to glucose signaling in plants remain unknown. Here, we show that the Trithorax-group Protein ARABIDOPSIS TRITHORAX5 (ATX5) affects the glucose response and signaling. atx5 loss-of-function mutants display glucose-oversensitive phenotypes compared to the wild-type (WT). Genome-wide RNA-sequencing analyses have revealed that ATX5 impacts the expression of a subset of glucose signaling responsive genes. Intriguingly, we have established that ATX5 directly controls the expression of HY1 by trimethylating H3 lysine 4 of the Arabidopsis Heme Oxygenase1 (HY1) locus. Glucose signaling causes the suppression of ATX5 activity and subsequently reduces the H3K4me3 levels at the HY1 locus, thereby leading to the increased expression of ABSCISIC ACID-INSENSITIVE4 (ABI4). This result suggests that an important ATX5-HY1-ABI4 regulatory module governs the glucose response. This idea is further supported by genetic evidence showing that an atx5 hy1-100 abi4 triple mutant showed a similar glucose-insensitive phenotype as compared to that of the abi4 single mutant. Our findings show that a novel ATX5-HY1-ABI4 module controls the glucose response in Arabidopsis thaliana.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (31601311 and 31771352), the National Key Research and Development Program of China (2016YFD0102003), the Natural Science Foundation of Jilin Province of China (20180101233JC) and the Fundamental Research Funds for the Central Universities (#2412018BJ002) to Z.-Y.X. We thank Dr. Wenbiao Shen (College of Life Sciences, Laboratory Center of Life Sciences, Nanjing Agricultural University, Nanjing 20095, China) for generously providing the hy1-100, abi4 and hy1-100 abi4 double mutants. We appreciate Dr. Lei Li and Dr. Lin Shi (Department of Genetics, Harvard Medical School and Department of Molecular Biology; Center for Computational and Integrative Biology, Massachusetts General Hospital, MA 02114, USA) for suggestions about the project.

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  1. Yutong Liu and Jie Wang have contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Molecular Epigenetics of the Ministry of Education (MOE), Northeast Normal University, Changchun, 130024, People’s Republic of China

    Yutong Liu, Jie Wang, Hao Yin, Ai Zhang, Shuangzhan Huang, Tian-Jing Wang, Qingxiang Meng, Nan Nan, Yifan Wu, Peng Guo, Rafiq Ahmad, Bao Liu & Zheng-Yi Xu

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  1. Yutong Liu
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Contributions

Z-YX and BL devised the project. Z-YX and BL supervised the project. YL performed the most of physiological analyses in response to glucose. JW performed RNA-sequencing experiment and analyzed data. HY performed the ChIP-qPCR analysis. AZ, SH, T-JW, performed biochemical analyses. QM, NN, YW, PG and RA took part in performing molecular cloning and some physiological analyses. Z-YX, and BL wrote the manuscript. All authors reviewed, revised, and approved the manuscript.

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Correspondence to Bao Liu or Zheng-Yi Xu.

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The authors declare that they have no competing interests.

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Data generated in this study are deposited in the National Center for Biotechnology Information Sequence Read Archive (Accession No. SUB3959287).

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Liu, Y., Wang, J., Yin, H. et al. Trithorax-group protein ATX5 mediates the glucose response via impacting the HY1-ABI4 signaling module. Plant Mol Biol 98, 495–506 (2018). https://doi.org/10.1007/s11103-018-0791-0

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