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Integrative analysis of chloroplast DNA methylation in a marine alga—Saccharina japonica

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Abstract

Key message

We applied an integrative approach using multiple methods to verify cytosine methylation in the chloroplast DNA of the multicellular brown alga Saccharina japonica.

Abstract

Cytosine DNA methylation is a heritable process which plays important roles in regulating development throughout the life cycle of an organism. Although methylation of nuclear DNA has been studied extensively, little is known about the state and role of DNA methylation in chloroplast genomes, especially in marine algae. Here, we have applied an integrated approach encompassing whole-genome bisulfite sequencing, methylated DNA immunoprecipitation, gene co-expression networks and photophysiological analyses to provide evidence for the role of chloroplast DNA methylation in a marine alga, the multicellular brown alga Saccharina japonica. Although the overall methylation level was relatively low in the chloroplast genome of S. japonica, gametophytes exhibited higher methylation levels than sporophytes. Gene-specific bisulfite-cloning sequencing provided additional evidence for the methylation of key photosynthetic genes. Many of them were highly expressed in sporophytes whereas genes involved in transcription, translation and biosynthesis were strongly expressed in gametophytes. Nucleus-encoded photosynthesis genes were co-expressed with their chloroplast-encoded counterparts potentially contributing to the higher photosynthetic performance in sporophytes compared to gametophytes where these co-expression networks were less pronounced. A nucleus-encoded DNA methyltransferase of the DNMT2 family is assumed to be responsible for the methylation of the chloroplast genome because it is predicted to possess a plastid transit peptide.

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Data availability

The Illumina data for whole genome bisulfite sequencing were deposited at NCBI with the GEO accession number GSE117191 (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSM3273187). The Illumina data of the MeDIP experiments were deposited at CNGB Nucleotide Sequence Archive with the accession number CNP0000364 (https://db.cngb.org/search/project/CNP0000364/). The Illumina raw data for transcriptomes were deposited at NCBI database with the SRA accession numbers SRR5860560–SRR5860568.

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Acknowledgements

TM acknowledges partial support from the School of Environmental Sciences, University of East Anglia, Norwich Research Park, UK

Funding

This work was supported by National Key Research and Development Program of China (2018YFD0900703); National Natural Science Foundation of China (32000402, 41976110); Fund for Doctor Research of Dezhou University, China (2019xgrc26); Marine S&T Fund of Shandong Province for Pilot National Laboratory for Marine Science and Technology (Qingdao) (2018SDKJ0406-3); Major Scientific and Technological Innovation Project of Shandong Provincial Key Research and Development Program (2019JZZY020706); Central Public-interest Scientific Institution Basal Research Fund, CAFS (2020TD27); China Agriculture Research System (CARS-50); Financial Fund of the Ministry of Agriculture and Rural Affairs, P.R. China (NFZX2018); Taishan Scholars Funding and Talent Projects of Distinguished Scientific Scholars in Agriculture; A Project of Shandong Province Higher Educational Science and Technology (J16LC59).

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Author notes

  1. Linhong Teng and Wentao Han have contributed equally to this work.

Authors and Affiliations

  1. Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, 266071, China

    Linhong Teng, Wentao Han, Xiao Fan, Xiaowen Zhang, Dong Xu, Yitao Wang & Naihao Ye

  2. Function Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266071, China

    Linhong Teng & Naihao Ye

  3. College of Life Science, Dezhou University, Dezhou, 253023, China

    Linhong Teng

  4. Tropical Medicine and Biology Platform and School of Science, Monash University Malaysia, Jalan Lagoon Selatan, 47500, Bandar Sunway, Selangor Darul Ehsan, Malaysia

    Sadequr Rahman

  5. Department of Molecular, Cell and Developmental Biology, Institute for Genomics and Proteomics, University of California, Los Angeles, CA, 90095, USA

    Matteo Pellegrini

  6. School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich, NR4 7TJ, UK

    Thomas Mock

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  1. Linhong Teng
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Contributions

NY designed the experiment. LT, TM and NY co-wrote the manuscript. WH, XF, TM and NY analyzed and interpreted the sequencing data. WH and YW cultured the algae and performed biochemistry experiments. SR, MP and TM revised the manuscript.

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Correspondence to Naihao Ye.

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Teng, L., Han, W., Fan, X. et al. Integrative analysis of chloroplast DNA methylation in a marine alga—Saccharina japonica. Plant Mol Biol 105, 611–623 (2021). https://doi.org/10.1007/s11103-020-01113-9

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