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Arbuscular cell invasion coincides with extracellular vesicles and membrane tubules

Nature Plants volume 5, pages 204–211 (2019)Cite this article

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Abstract

During establishment of arbuscular mycorrhizal symbioses, fungal hyphae invade root cells producing transient tree-like structures, the arbuscules, where exchange of photosynthates for soil minerals occurs. Arbuscule formation and collapse lead to rapid production and degradation of plant and fungal membranes, their spatiotemporal dynamics directly influencing nutrient exchange. We determined the ultra-structural details of both membrane surfaces and the interstitial apoplastic matrix by transmission electron microscopy tomography during growth and senescence of Rhizophagus irregularis arbuscules in rice. Invasive growth of arbuscular hyphae was associated with abundant fungal membrane tubules (memtubs) and plant peri-arbuscular membrane evaginations. Similarly, the phylogenetically distant arbuscular mycorrhizal fungus, Gigaspora rosea, and the fungal maize pathogen, Ustilago maydis, developed memtubs while invading host cells, revealing structural commonalities independent of the mutualistic or parasitic outcome of the interaction. Additionally, extracellular vesicles formed continuously in the peri-arbuscular interface from arbuscule biogenesis to senescence, suggesting an involvement in inter-organismic signal and nutrient exchange throughout the arbuscule lifespan.

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Fig. 1: Transmission electron micrographs of Rhizophagus irregularis-colonized rice cortex cells showing paramural fungal memtubs.
Fig. 2: Tomography and 3D reconstruction of fungal memtubs.
Fig. 3: Transmission electron micrographs documenting PAM evaginations and membrane-bound vesicles within the PAS.
Fig. 4: Tomography and 3D reconstruction of PAS-localized apoplastic vesicular structures.

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All data that support the findings of this study are available from the corresponding author on request.

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  • 06 January 2021

    In the version of this Article originally published, Supplementary Videos 1 and 2 were missing. These videos are now available.

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Acknowledgements

We thank A. Bates and S. Gold for technical assistance, and Y. Kobae for kindly providing PT11-GFP transgenic rice lines. R. Roth was supported by Marie Curie FP7-PEOPLE-2013-IEF grant No. 629887 and by the Isaac Newton Trust RG74108; and U. Paszkowski by the BBSRC grant No. BB/N008723/1.

Author information

Authors and Affiliations

  1. Department of Plant Sciences, University of Cambridge, Cambridge, UK

    Ronelle Roth & Uta Paszkowski

  2. Electron Microscopy Core Facility, University of Heidelberg, Heidelberg, Germany

    Stefan Hillmer & Charlotta Funaya

  3. Department of Chemistry, University of Cambridge, Cambridge, UK

    Marco Chiapello

  4. Centre for Organismal Studies, University of Heidelberg, Heidelberg, Germany

    Karin Schumacher

  5. Max-Planck Institute for Terrestrial Microbiology, Marburg, Germany

    Libera Lo Presti & Regine Kahmann

  6. Springer Nature Heidelberg, Berlin, Germany

    Libera Lo Presti

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Contributions

R.R. and U.P. conceptualized the project. R.R., S.H. and C.F. carried out the experiments. R.R. and S.H. conducted the TEM and IGL analysis. C.F. and S.H. carried out the tomography and R.R. performed the IMOD 3D reconstruction. R.R. and M.C. did the quantitative analysis. R.R. and U.P. wrote the manuscript.

Corresponding author

Correspondence to Uta Paszkowski.

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Journal Peer Review Information Nature Plants thanks Rogers Innes, Erik Limpens and other anonymous reviewers for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Figures 1–7 and Supplementary Table 1.

Reporting Summary

Video 1

TEM tilt tomography and IMOD 3-D modeling shows memtubs, which remain connected with the fungal plasma membrane. Scale bar, 100 nm.

Video 2

TEM tilt tomography and IMOD 3-D modeling shows extracellular vesicles in the peri-arbuscular space and membrane evaginations continuous with the PAM. Scale bar, 100 nm.

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Roth, R., Hillmer, S., Funaya, C. et al. Arbuscular cell invasion coincides with extracellular vesicles and membrane tubules. Nature Plants 5, 204–211 (2019). https://doi.org/10.1038/s41477-019-0365-4

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