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Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots

Nature volume 433, pages 527–531 (2005)Cite this article

Abstract

The roots of most higher plants form arbuscular mycorrhiza, an ancient, phosphate-acquiring symbiosis with fungi, whereas only four related plant orders are able to engage in the evolutionary younger nitrogen-fixing root-nodule symbiosis with bacteria1. Plant symbioses with bacteria and fungi require a set of common signal transduction components that redirect root cell development2,3. Here we present two highly homologous genes from Lotus japonicus, CASTOR and POLLUX, that are indispensable for microbial admission into plant cells and act upstream of intracellular calcium spiking4, one of the earliest plant responses to symbiotic stimulation. Surprisingly, both twin proteins are localized in the plastids of root cells, indicating a previously unrecognized role of this ancient endosymbiont in controlling intracellular symbioses that evolved more recently.

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Figure 1: Phenotypes of castor and pollux mutants.
Figure 2: Southern blot and RT–PCR expression analyses of CASTOR and POLLUX.
Figure 3: Structure, domains and homologues of CASTOR and POLLUX.
Figure 4: Intracellular localization of CASTOR and POLLUX.

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Acknowledgements

We thank K. Szczyglowski, J. Webb and J. Stougaard for providing mutant seeds; M. Hayashi for help with mapping; T. Kojima and R. Ohtomo for mycorrhiza analysis; Y. Niwa for providing pUC18-CaMV35S-sGFP (S65T)-nos vector; G. Oldroyd and J. Sun for help with Ca-spiking assays; J. Krüger and B. B. H. Wulff for critical reading of the manuscript; J. Soll for providing the pea root transformation protocol before publication; and M. Durrant for help with modelling the CASTOR pore structure. Part of this work was supported by the fund of Promotion of Basic Research Activities for Innovative Biosciences (BRAIN), and Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency. Research at the Sainsbury Laboratory is funded by the Gatsby Charitable Foundation.

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Author notes

  1. Myriam Charpentier & Martin Parniske

    Present address: Genetics Institute, Ludwig Maximilians Universität (LMU), Maria-Ward-Str. 1a, D-80638, München, Germany

  2. Haruko Imaizumi-Anraku and Naoya Takeda: These authors contributed equally to this work

Authors and Affiliations

  1. National Institute of Agrobiological Sciences, 2-1-2 Kannondai, 305-8602, Tsukuba, Ibaraki, Japan

    Haruko Imaizumi-Anraku, Yosuke Umehara, Hiroshi Kouchi, Yasuhiro Murakami & Shinji Kawasaki

  2. Bio-oriented Technology Research Advancement Institution (BRAIN), Tokyo Office, 3-18-19 Toranomon Minato-ku, 105-0001, Tokyo, Japan

    Haruko Imaizumi-Anraku, Yasuhiro Murakami & Shinji Kawasaki

  3. Department of Biotechnology, Graduate School of Engineering, Osaka University, 2-1 Yamadaoka, 565-0871, Suita, Osaka, Japan

    Naoya Takeda, Makoto Yoshikawa, Yoshikatsu Murooka & Makoto Hayashi

  4. The Sainsbury Laboratory, John Innes Centre, Colney Lane, NR4 7UH, Norwich, UK

    Myriam Charpentier, Jillian Perry, Lonneke Mulder, Kate Vickers, Jodie Pike & Martin Parniske

  5. John Innes Centre, Colney Lane, NR4 7UH, Norwich, UK

    Hiroki Miwa, J. Allan Downie & Trevor Wang

  6. Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency, 4-1-8 Honcho, 332-0112, Kawaguchi, Saitama, Japan

    Yosuke Umehara, Hiroshi Kouchi, Masayoshi Kawaguchi & Makoto Hayashi

  7. Kazusa DNA Research Institute, 2-6-7 Kazusa-kamatari, 292-0818, Kisarazu, Chiba, Japan

    Shusei Sato, Erika Asamizu & Satoshi Tabata

  8. Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, 113-0033, Bunkyo, Tokyo, Japan

    Guo-Jiang Wu & Masayoshi Kawaguchi

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  1. Haruko Imaizumi-Anraku
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Corresponding author

Correspondence to Shinji Kawasaki.

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Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Figure S1

Positional cloning of CASTOR and POLLUX genes, and legend. (PPT 86 kb)

Supplementary Figure 1 legend

Additional copy of the legend for Supplementary Figure S1. (DOC 21 kb)

Supplementary Table 1

Castor and pollux mutant alleles. (DOC 41 kb)

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Imaizumi-Anraku, H., Takeda, N., Charpentier, M. et al. Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 433, 527–531 (2005). https://doi.org/10.1038/nature03237

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