During arbuscular mycorrhizal (AM) symbiosis, cells within the root cortex develop a matrix-filled apoplastic compartment in which differentiated AM fungal hyphae called arbuscules reside. Development of the compartment occurs rapidly, coincident with intracellular penetration and rapid branching of the fungal hypha, and it requires much of the plant cell’s secretory machinery to generate the periarbuscular membrane that delimits the compartment. Despite recent advances, our understanding of the development of the periarbuscular membrane and the transfer of molecules across the symbiotic interface is limited. Here, using electron microscopy and tomography, we reveal that the periarbuscular matrix contains two types of membrane-bound compartments. We propose that one of these arises as a consequence of biogenesis of the periarbuscular membrane and may facilitate movement of molecules between symbiotic partners. Additionally, we show that the arbuscule contains massive arrays of membrane tubules located between the protoplast and the cell wall. We speculate that these tubules may provide the absorptive capacity needed for nutrient assimilation and possibly water absorption to enable rapid hyphal expansion.
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The data that support the findings of this study are available from the corresponding author upon request.
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Financial support for this project was provided by the U.S. National Science Foundation grant no. IOS-1353367 and by the TRIAD Foundation. Confocal microscopy was carried out in the BTI Plant Cell Imaging Center (NSF DBI-0618969). Electron microscopy was carried out in the Imaging and Microscopy Facility at the Danforth Plant Science Center and at the Cornell Center for Materials Research Shared Facilities (the latter is supported through the NSF MRSEC program (DMR-1719875)). Electron microscopy for 3D electron tomography was undertaken at the Advanced Electron Microscopy facility at The University of Chicago.
The authors declare no competing interests.
Journal peer review information: Nature Plants thanks Andrea Genre, Roger Innes, Erik Limpens and other anonymous reviewers for their contribution to the peer review of this work.
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Supplementary Figures 1–7, Supplementary Video Legends, Supplementary Methods and Supplementary Table 1.
Tomogram used for all modelling except in Fig. 2d,e. This slice movie through a 1-μm-thick section was made using 10-slice projections. The tomogram contains a total cellular volume of 10.14 μm3.
Tomogram used for modelling in Fig. 2d,e. The slice movie through a 1-μm-thick section was made using 10-slice projections and the part showing the features modelled in Fig. 2d,e is shown here.
Model of all components shown in Fig. 2 (except Fig. 2d,e) and Fig. 5.
IMC-I (with pores) and IMC-II (related to Fig. 2a).
ER remnants in the lumen of IMC-I (related to Fig. 2a).
Model of ER that has entered IMC-I (related to Fig. 2d,e).
Enclosure of fungal protoplast and tubules by the fungal cell wall (related to Fig. 5).
Top view of fungal tubules and protoplasts (related to Fig. 5).
Side view of fungal tubules and protoplasts (related to Fig. 5).
Proximity of the fungal tubules and plant intramatrix membrane systems (related to Fig. 2a and Fig. 5).
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Ivanov, S., Austin, J., Berg, R.H. et al. Extensive membrane systems at the host–arbuscular mycorrhizal fungus interface. Nature Plants 5, 194–203 (2019). https://doi.org/10.1038/s41477-019-0364-5
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