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Genome-wide high-resolution mapping of DNA methylation reveals epigenetic variation in the offspring of sexual and asexual propagation in Robinia pseudoacacia

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Abstract

Key Message

We detected the genome-wide pattern of DNA methylation and its association with gene expression in sexual and asexual progenies of mature Robinia pseudoacacia trees.

Abstract

DNA methylation plays an important role in plant reproduction and development. Although some studies on sexual reproduction have been carried out in model plants, little is known about the dynamic changes in DNA methylation and their effect on gene expression in sexual and asexual progeny of woody plants. Here, through whole-genome bisulfite sequencing, we revealed DNA methylation patterns in the sexual and asexual progenies of mature Robinia pseudoacacia to understand the regulation of gene expression by DNA methylation in juvenile seedlings. An average of 53% CG, 34% CHG and 5% CHH contexts was methylated in the leaves of mature and juvenile individuals. The CHH methylation level of asexually propagated seedlings was significantly lower than that of seed-derived seedlings and mature trees. The intergenic regions had the highest methylation level. Analysis of differentially methylated regions (DMRs) showed that most of them were hypermethylated and located in the gene upstream and introns. A total of 24, 108 and 162 differentially expressed genes containing DMRs were identified in root sprouts (RSs), root cuttings (RCs) and seed-derived seedlings (SSs), respectively, and a large proportion of them showed hypermethylation. In addition, DMRs were enriched within GO subcategories including catalytic activity, metabolic process and cellular process. The results reveal widespread DNA methylation changes between mature plants and their progenies through sexual/asexual reproduction, which provides novel insights into DNA methylation reprogramming and the regulation of gene expression in woody plants.

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Availability of data and material

The datasets generated and/or analyzed during the current study have been deposited in the NCBI Sequence Read Archive repository under accession numbers PRJNA743019 and PRJNA742908 (https://www.ncbi.nlm.nih.gov/bioproject). Any reasonable requests are available from the corresponding author.

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Acknowledgements

We thank the staff and other members of the forest farm in Lvcun, Luoning county, He’nan province for their help in samples identification and collection. We also thank other students in our lab for their help in the daily work.

Funding

This work was funded by the Long-Term Research Program for Young Teachers of Beijing Forestry University (2015ZCQ-SW-03), the National Nature Science Foundation of China (31971675) and National Key R&D Program of China (2017YFD0600503).

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Authors and Affiliations

  1. National Engineering Laboratory for Tree Breeding, College of Biological Science and Technology, Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Engineering Technology Research Center of Black Locust of National Forestry and Grassland Administration, Beijing Forestry University, Beijing, 100083, People’s Republic of China

    Zijie Zhang, Jie Liu, Yuhan Sun & Yun Li

  2. State-Owned Quanbaoshan Forestry Station in Luoning County of He’nan Province, Luoyang, 471717, People’s Republic of China

    Shaoming Wang

  3. Agricultural Service Center of Wangfan Hui Town in Luoning County of He’nan Province, Luoyang, 471700, People’s Republic of China

    Xiuxia Xing

  4. State-Owned Lvcun Forestry Station in Luoning County of He’nan Province, Luoyang, 471700, People’s Republic of China

    Xiaojing Feng

  5. Instituto de Bioingeniería, Universidad Miguel Hernández de Elche, Alicante, Spain

    José Manuel Pérez-Pérez

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  1. Zijie Zhang
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  2. Jie Liu
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  3. Yuhan Sun
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  4. Shaoming Wang
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  5. Xiuxia Xing
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  6. Xiaojing Feng
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  7. José Manuel Pérez-Pérez
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  8. Yun Li
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Contributions

YL and JP conceived the research; ZZ and JL designed and performed the experiments, analyzed the data and drafted the manuscript; YS and SW participated in the coordination of the study; XX analyzed a portion of the WGBS data; XF analyzed a portion of the RNA-seq data. All authors read and approved the final manuscript.

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Correspondence to Yun Li.

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Communicated by Tarek Hewezi.

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Supplementary Information

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299_2021_2787_MOESM1_ESM.tif

Supplementary Fig. S1 Total number of differentially expressed genes in different seedlings. RS represents root sprouting seedlings; RC represents root cutting seedlings; SS represents seed-derived seedlings (TIF 138 kb)

299_2021_2787_MOESM2_ESM.tif

Supplementary Fig. S2 Number of DMR-associated genes in various seedlings. RS represents root sprouting seedlings; RC represents root cutting seedlings; SS represents seed-derived seedlings (TIF 132 kb)

299_2021_2787_MOESM3_ESM.xlsx

Supplementary Table S1 List of DMR-associated genes with differential expression in different seedlings. RS represents root sprouting seedlings; RC represents root cutting seedlings; SS represents seed-derived seedlings (XLSX 16 kb)

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Zhang, Z., Liu, J., Sun, Y. et al. Genome-wide high-resolution mapping of DNA methylation reveals epigenetic variation in the offspring of sexual and asexual propagation in Robinia pseudoacacia. Plant Cell Rep 40, 2435–2447 (2021). https://doi.org/10.1007/s00299-021-02787-1

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