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Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening

Nature Biotechnology volume 31, pages 154–159 (2013)Cite this article

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Abstract

Ripening of tomato fruits is triggered by the plant hormone ethylene, but its effect is restricted by an unknown developmental cue to mature fruits containing viable seeds. To determine whether this cue involves epigenetic remodeling, we expose tomatoes to the methyltransferase inhibitor 5-azacytidine and find that they ripen prematurely. We performed whole-genome bisulfite sequencing on fruit in four stages of development, from immature to ripe. We identified 52,095 differentially methylated regions (representing 1% of the genome) in the 90% of the genome covered by our analysis. Furthermore, binding sites for RIN, one of the main ripening transcription factors, are frequently localized in the demethylated regions of the promoters of numerous ripening genes, and binding occurs in concert with demethylation. Our data show that the epigenome is not static during development and may have been selected to ensure the fidelity of developmental processes such as ripening. Crop-improvement strategies could benefit by taking into account not only DNA sequence variation among plant lines, but also the information encoded in the epigenome.

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Figure 1: Application of a methylation inhibitor uncouples seed maturation and fruit ripening.
Figure 2: The tomato epigenome.
Figure 3: Tissue and developmental specific epigenetic variation in tomato.
Figure 4: Demethylation of RIN binding sites during ripening.
Figure 5: Model of fruit ripening regulation.

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Acknowledgements

We thank E. Richards, R. Schmitz and J. Ecker for discussion and thoughtful advice in preparing this manuscript, and R. White, Y. Xu and Z. Li for technical assistance. This project was supported by the United States Department of Agriculture – Agricultural Research Service, National Science Foundation IOS-0606595 and IOS-0923312 to J.J.G. and Z.F., DBI-0820612 to J.J.G., National Natural Science Foundation of China 30900783 and 3090243 to S.Z. and B.L. and the Human Frontier Science Program LTF000076/2009 to S.Z.

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  1. Silin Zhong and Zhangjun Fei: These authors contributed equally to this work.

Authors and Affiliations

  1. Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, New York, USA

    Silin Zhong, Zhangjun Fei, Yun-Ru Chen, Yi Zheng, Mingyun Huang, Julia Vrebalov, Ryan McQuinn, Nigel Gapper & James J Giovannoni

  2. Key Laboratories of Molecular Epigenetics of Ministry of Education, Northeast Normal University, Changchun, China

    Silin Zhong & Bao Liu

  3. US Department of Agriculture/Agriculture Research Service, Robert W. Holley Centre for Agriculture and Health, Ithaca, New York, USA

    Zhangjun Fei & James J Giovannoni

  4. Weill Medical College, Genomics Resource Core Facility, Cornell University, New York, New York, USA

    Jenny Xiang & Ying Shao

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  1. Silin Zhong
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Contributions

J.J.G., Z.F. and S.Z. devised the project and wrote the manuscript. Z.F. and S.Z. led the bioinformatic and experimental teams, respectively. Y.-R.C., J.V., R.M. and N.G. performed the experiments. Y.Z., Z.F., M.H., B.L., Y.S., J.X. and J.J.G. analyzed and interpreted the data.

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Correspondence to Silin Zhong, Zhangjun Fei or James J Giovannoni.

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Zhong, S., Fei, Z., Chen, YR. et al. Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat Biotechnol 31, 154–159 (2013). https://doi.org/10.1038/nbt.2462

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