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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Data availability
All data that support the findings of this study are available from the corresponding author on request.
Change history
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.
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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.
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Supplementary Figures 1–7 and Supplementary Table 1.
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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DOI: https://doi.org/10.1038/s41477-019-0365-4
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