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Extensive membrane systems at the host–arbuscular mycorrhizal fungus interface

Nature Plants volume 5, pages 194–203 (2019)Cite this article

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Abstract

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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Fig. 1: Extensions of the PAM form vesicular–tubular compartments in the PAS.
Fig. 2: Electron tomography of an IMC.
Fig. 3: Integral membrane proteins outline the PAM but also accumulate in distinct regions.
Fig. 4: An extensive mass of membrane tubules extend beyond the protoplast of the arbuscule but remain within the fungal cell wall.
Fig. 5: Electron tomography of fungal tubules.
Fig. 6: IMCs and fungal membrane tubules in M. truncatula exo70i mutant.

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Data Availability

The data that support the findings of this study are available from the corresponding author upon request.

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Acknowledgements

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.

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Authors and Affiliations

  1. Boyce Thompson Institute, Ithaca, NY, USA

    Sergey Ivanov & Maria J. Harrison

  2. Advanced Electron Microscopy Facility, University of Chicago, Chicago, IL, USA

    Jotham Austin II

  3. Integrated Microscopy Facility, Donald Danforth Plant Science Center, St Louis, MS, USA

    R. Howard Berg

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Contributions

All authors conceived the experiments and analysed data; S.I., R.H.B. and J.A. carried out experiments; all authors wrote the manuscript.

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Correspondence to Maria J. Harrison.

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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 information

Supplementary Information

Supplementary Figures 1–7, Supplementary Video Legends, Supplementary Methods and Supplementary Table 1.

Reporting Summary

Supplementary Video 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.

Supplementary Video 2

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.

Supplementary Video 3

Model of all components shown in Fig. 2 (except Fig. 2d,e) and Fig. 5.

Supplementary Video 4

IMC-I (with pores) and IMC-II (related to Fig. 2a).

Supplementary Video 5

ER remnants in the lumen of IMC-I (related to Fig. 2a).

Supplementary Video 6

Model of ER that has entered IMC-I (related to Fig. 2d,e).

Supplementary Video 7

Enclosure of fungal protoplast and tubules by the fungal cell wall (related to Fig. 5).

Supplementary Video 8

Top view of fungal tubules and protoplasts (related to Fig. 5).

Supplementary Video 9

Side view of fungal tubules and protoplasts (related to Fig. 5).

Supplementary Video 10

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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