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Epigenetic modifications and miRNAs determine the transition of somatic cells into somatic embryos

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Abstract

Key message

This review discusses the epigenetic changes during somatic embryo (SE) development, highlights the genes and miRNAs involved in the transition of somatic cells into SEs as a result of epigenetic changes, and draws insights on biotechnological opportunities to study SE development.

Abstract

Somatic embryogenesis from somatic cells occurs in a series of steps. The transition of somatic cells into somatic embryos (SEs) is the most critical step under genetic and epigenetic regulations. Major regulatory genes such as SERK, WUS, BBM, FUS3/FUSA3, AGL15, and PKL, control SE steps and development by turning on and off other regulatory genes. Gene transcription profiles of somatic cells during SE development is the result of epigenetic changes, such as DNA and histone protein modifications, that control and decide the fate of SE formation. Depending on the type of somatic cells and the treatment with plant growth regulators, epigenetic changes take place dynamically. Either hypermethylation or hypomethylation of SE-related genes promotes the transition of somatic cells. For example, the reduced levels of DNA methylation of SERK and WUS promotes SE initiation. Histone modifications also promote SE induction by regulating SE-related genes in somatic cells. In addition, miRNAs contribute to the various stages of SE by regulating the expression of auxin signaling pathway genes (TIR1, AFB2, ARF6, and ARF8), transcription factors (CUC1 and CUC2), and growth-regulating factors (GRFs) involved in SE formation. These epigenetic and miRNA functions are unique and have the potential to regenerate bipolar structures from somatic cells when a pluripotent state is induced. However, an integrated overview of the key regulators involved in SE development and downstream processes is lacking. Therefore, this review discusses epigenetic modifications involved in SE development, SE-related genes and miRNAs associated with epigenetics, and common cis-regulatory elements in the promoters of SE-related genes. Finally, we highlight future biotechnological opportunities to alter epigenetic pathways using the genome editing tool and to study the transition mechanism of somatic cells.

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All data generated or analysed during this study are included in this published article and its supplementary information files.

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Acknowledgements

The authors wish to thank the anonymous reviewers for their valuable time and insightful comments, which greatly improved the quality of the manuscript. We apologize to those whose original work(s) could not be included in this review owing to space limitations.

Funding

Preparation of this review was supported by a grant from the Jiangxi “Shuangqian” Program (Grant No. S2019DQKJ2030), the Qing Lan Project of Jiangsu Higher Education Institutions, the Natural Science Foundation for Distinguished Young Scholars of Nanjing Forestry University (Grant No. JC2019004), the Project for Groundbreaking Achievements of Nanjing Forestry University (Grant No. 202211), and also a project funded by the Priority Academic Programme Development of Jiangsu Higher Education Institutions. The authors are also grateful for the Young Foreign Talent Program (Grant No. QN2022014012L) and the support of Metasequoia Faculty Research Start-up Funding (Grant No. 163100028) at the Bamboo Research Institute, Nanjing Forestry University, for the first author MR.

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Authors and Affiliations

  1. State Key Laboratory of Tree Genetics and Breeding, Co-Innovation Center for Sustainable Forestry in Southern China, Bamboo Research Institute, Key Laboratory of National Forestry and Grassland Administration On Subtropical Forest Biodiversity Conservation, School of Life Sciences, Nanjing Forestry University, Nanjing, 210037, Jiangsu, China

    Muthusamy Ramakrishnan, Zishan Ahmad & Qiang Wei

  2. State Key Laboratory of Subtropical Silviculture, Bamboo Industry Institute, Zhejiang A&F University, Lin’an, Hangzhou, 311300, Zhejiang, China

    Mingbing Zhou & Anket Sharma

  3. Zhejiang Provincial Collaborative Innovation Center for Bamboo Resources and High-Efficiency Utilization, Zhejiang A&F University, Lin’an, Hangzhou, 311300, Zhejiang, China

    Mingbing Zhou

  4. Department of Biosciences, Rajagiri College of Social Sciences (Autonomous), Kalamassery, Kochi, 683104, Kerala, India

    Stanislaus Antony Ceasar & Theivanayagam Maharajan

  5. State Key Laboratory of Bioelectronics, School of Biological Science and Medical Engineering, Southeast University, Nanjing, 210096, Jiangsu, China

    Doulathunnisa Jaffar Ali

  6. Division of Genetics, ICAR—Indian Agricultural Research Institute, New Delhi, 110012, India

    Kunnummal Kurungara Vinod

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  1. Muthusamy Ramakrishnan
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MR planned, designed and wrote the review together with MZ, KKV, and QW. MR, KKV, and QW outlined the review. MR drew the images with QW, DJA, and KKV. MR, KKV, and TM analyzed the cis-acting elements of major regulatory genes involved in SE. AC and MR wrote the alteration of SE-epigenetic modification using the genome editing tool. MR, KKV, AC, AS, MZ, ZA, and QW edited and revised the review. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Qiang Wei.

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Communicated by Wusheng Liu.

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Ramakrishnan, M., Zhou, M., Ceasar, S.A. et al. Epigenetic modifications and miRNAs determine the transition of somatic cells into somatic embryos. Plant Cell Rep 42, 1845–1873 (2023). https://doi.org/10.1007/s00299-023-03071-0

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