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Organelle DNA degradation contributes to the efficient use of phosphate in seed plants

Nature Plantsvolume 4pages10441055 (2018) | Download Citation

Abstract

Mitochondria and chloroplasts (plastids) both harbour extranuclear DNA that originates from the ancestral endosymbiotic bacteria. These organelle DNAs (orgDNAs) encode limited genetic information but are highly abundant, with multiple copies in vegetative tissues, such as mature leaves. Abundant orgDNA constitutes a substantial pool of organic phosphate along with RNA in chloroplasts, which could potentially contribute to phosphate recycling when it is degraded and relocated. However, whether orgDNA is degraded nucleolytically in leaves remains unclear. In this study, we revealed the prevailing mechanism in which organelle exonuclease DPD1 degrades abundant orgDNA during leaf senescence. The DPD1 degradation system is conserved in seed plants and, more remarkably, we found that it was correlated with the efficient use of phosphate when plants were exposed to nutrient-deficient conditions. The loss of DPD1 compromised both the relocation of phosphorus to upper tissues and the response to phosphate starvation, resulting in reduced plant fitness. Our findings highlighted that DNA is also an internal phosphate-rich reservoir retained in organelles since their endosymbiotic origin.

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Data availability

Accession numbers of the genes used in this study are listed in Supplementary Table 9. Precise P values calculated by statistical tests in this study are listed in Supplementary Table 10. The raw data used to construct graphs in this study are presented as Supplementary Dataset. The raw transcriptomic data are deposited in the DDBJ with the accession number DRA007138, under the BioProject with the accession number PRJDB7233. All transcriptomic data used in Fig. 5 and Supplementary Figs. 10 and 11 are available in Supplementary Tables 18.

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Acknowledgements

We thank R. Hijiya (Institute of Plant Science and Resources, Okayama University, Kurashiki, Japan) for technical support, H. Kanegae (Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, Japan) for assisting mtDNA sequence alignment in Populus species and K. Baba (Research Institute for Sustainable Humanosphere, Kyoto University, Kyoto, Japan) for supporting poplar leaf sampling. This work was supported by KAKENHI grants from JSPS (16H06554 and 17H03699 to W.S.) and from the Oohara Foundation (to W.S.).

Author information

Author notes

    • Yuko Kurita

    Present address: Faculty of Agriculture, Ryukoku University, Otsu, Japan

Affiliations

  1. Institute of Plant Science and Resources, Okayama University, Kurashiki, Japan

    • Tsuneaki Takami
    • , Norikazu Ohnishi
    •  & Wataru Sakamoto
  2. Department of Biology, Graduate School of Science, Kobe University, Kobe, Japan

    • Yuko Kurita
    • , Shoko Iwamura
    • , Miwa Ohnishi
    •  & Tetsuro Mimura
  3. Graduate School of Science, Hiroshima University, Higashi-Hiroshima, Japan

    • Makoto Kusaba

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Contributions

W.S. designed the project. T.T. performed all qPCR and qRT–PCR measurements for various environments, in addition to photosynthetic activity measurements and RNA-seq analysis. N.O. performed the nuclease assays. Y.K., S.I., M.O. and T.M. prepared the poplar samples and conducted primary work related to poplar. T.T., M.K. and W.S. analysed the data. W.S. wrote the manuscript with consultation among all co-authors.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Wataru Sakamoto.

Supplementary information

  1. Supplementary Information

    Supplementary Figures 1–15 and Supplementary Table 9.

  2. Reporting Summary

  3. Supplementary Tables 1–8

    Supplementary Table 1: Differential expression analysis of Col under P deprivation by edgeR. Supplementary Table 2: Differential expression analysis of dpd1-1 under P deprivation by edgeR. Supplementary Table 3: Expression profile of literature-curated phosphate starvation marker genes. Supplementary Table 4: Expression profile of PHR1 regulon genes. Supplementary Table 5: Differential expression analysis of Col under N deprivation by edgeR. Supplementary Table 6: Differential expression analysis of dpd1-1 under N deprivation by edgeR. Supplementary Table 7: Comparative analysis between Krapp et al. (ref. 32) and this study on upregulated gene profile under long term nitrogen starvation. Supplementary Table 8: Comparative analysis between Peng et al. (ref. 34) and this study on upregulated gene profile under long term nitrogen starvation.

  4. Supplementary Supplementary Table 10

    Precise P values in this study.

  5. Supplementary Dataset

    Raw data used to construct bar graphs.

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https://doi.org/10.1038/s41477-018-0291-x