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Review
. 2014 Jun 4:5:237.
doi: 10.3389/fpls.2014.00237. eCollection 2014.

Cell wall remodeling in mycorrhizal symbiosis: a way towards biotrophism

Raffaella Balestrini  1 , Paola Bonfante  2
Affiliations
Review

Cell wall remodeling in mycorrhizal symbiosis: a way towards biotrophism

Raffaella Balestrini et al. Front Plant Sci. .

Abstract

Cell walls are deeply involved in the molecular talk between partners during plant and microbe interactions, and their role in mycorrhizae, i.e., the widespread symbiotic associations established between plant roots and soil fungi, has been investigated extensively. All mycorrhizal interactions achieve full symbiotic functionality through the development of an extensive contact surface between the plant and fungal cells, where signals and nutrients are exchanged. The exchange of molecules between the fungal and the plant cytoplasm takes place both through their plasma membranes and their cell walls; a functional compartment, known as the symbiotic interface, is thus defined. Among all the symbiotic interfaces, the complex intracellular interface of arbuscular mycorrhizal (AM) symbiosis has received a great deal of attention since its first description. Here, in fact, the host plasma membrane invaginates and proliferates around all the developing intracellular fungal structures, and cell wall material is laid down between this membrane and the fungal cell surface. By contrast, in ectomycorrhizae (ECM), where the fungus grows outside and between the root cells, plant and fungal cell walls are always in direct contact and form the interface between the two partners. The organization and composition of cell walls within the interface compartment is a topic that has attracted widespread attention, both in ecto- and endomycorrhizae. The aim of this review is to provide a general overview of the current knowledge on this topic by integrating morphological observations, which have illustrated cell wall features during mycorrhizal interactions, with the current data produced by genomic and transcriptomic approaches.

Keywords: cell wall; fungal genomes; gene expression; interface; mycorrhizal interactions.

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Figures

FIGURE 1
FIGURE 1
In AM symbiosis, once the fungus overcomes the epidermal layer, it grows inter- and intracellularly all along the root in order to spread fungal structures. Only when the fungus reaches the cortical layers, does a peculiar branching process that leads to the highly branched structures, called arbuscules, which are the main site for nutrient exchanges. (A) R. irregularis arbuscule (a) after staining with wheat germ agglutinin-FITC, on paraffin section of M. truncatula root, to detect chitin in the fungal cell wall. Arrow points to an intercellular hypha. Bar, 7 μm. (B) At the electron microscope level, a new apoplastic space, based on membrane proliferation (arrow), is evident around the intracellular hyphae (F). The picture shows the morphology of the interface material (asterisk), with respect to the plant cell walls (W), where neatly arranged fibers are evident. w, fungal cell wall. Bar, 0.17 μm. (C) The host membrane surrounding the fungus (F) is smooth (arrows) in a clover root prepared through high pressure/freeze substitution. The interface material is electron-dense after PATAg treatment, and the fungal wall (arrowheads) is very thin. Bar, 0.3 μm. Inset: High magnification of the interface compartment. F, fungus; H, host cell. Bar, 0.25 μm.
FIGURE 2
FIGURE 2
During the symbiotic phase, ECM fungi form a fungal sheath (the mantle), which consists of aggregated hyphae that surround the root surface. This mycelium is linked to extramatrical hyphae that explore the substrate and are responsible for the mineral nutrition and water uptake of the symbiotic tissues. Some hyphae from the inner zone of the mantle penetrate between the root cells to form the Hartig net, an intercellular hyphal network inside the root tissues where metabolites are exchanged between the symbiotic partners. The hyphae always remain apoplastic and can colonize epidermal and cortical cell layers. (A) Confocal micrograph showing a section of hazelnut – Tuber melanosporum ectomycorrhizal root. The mantle (m), formed by packed hyphae, and the Hartig net (arrows), which surrounds the epidermal and outer cortical cells, show a green signal after treatment with WGA-FITC. Bar, 15 μm. (B) Hartig net (Hn) in a fully truffle developed mycorrhiza. Hyphae develop among plant cells, and their cell walls are in direct contact with the plant cell walls, showing a simple interface structure. H, host cell; Hn, Hartig net. Bar, 0.6 μm. (C) Magnification of the contact zone between plant (asterisk) and fungal cell wall (arrows). F, fungus; H, host cell. Bar, 0.4 μm.
FIGURE 3
FIGURE 3
Schematic view of the interface zone in AM (A) and ECM (B) symbiosis, in which several of the molecules so far determined through in situ labeling experiments (Balestrini et al., 1996a,b; Laurent et al., 1999; Tagu et al., 2001; Balestrini and Bonfante, 2005) are listed. HRGPs, hydroxyproline-rich glycoprotein; SRAPs, symbiosis-regulated acidic polypeptides.
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