Plant–Fungal Interactions in Mycorrhizas

Abstract

Mycorrhizas are widespread symbiotic associations established between the roots of the majority of land plants, and a heterogeneous group of beneficial fungi belonging to diverse fungal taxa. Their ubiquitous presence argues that they have been favoured during evolution thanks to the benefits gained by both the plant and fungal partners. Advances in deoxyribonucleic acid (DNA) technology coupled to high‐throughput sequencing have allowed the genomes of some symbionts to be studied, as well as the molecular basis of cross‐talk between plant and fungus. We are beginning to see the contributions of the partners to the functioning of mycorrhizal associations. Advanced microscopy of the living partner cells has unravelled some processes determining compatibility which are a peculiar feature of mycorrhizal interactions.

Key Concepts:

  • The term Mycorrhiza comes from two Greek words for ‘fungus’ and ‘root’ and describes root–fungus associations which may be morphologically and functionally diverse.

  • Molecular approaches have solved questions about the identity of mycorrhizal fungi both free in the soil and root associated in symbiotic structures.

  • Nutritional interactions among plants and fungi in the rhizosphere may be saprotrophic, pathogenic or symbiotic.

  • Recent advances in genome sequencing of ectomycorrhizal fungi identify some basic features which are characteristic of mycorrhizal fungi, that is the absence of effectors which may elicit plant defence.

  • Transcriptome profiles of ectomycorrhizal roots reveal differential regulation of both plant and fungus.

  • Glomeromycota possess peculiar features (i.e. an obligate biotrophic status and multinucleated hyphae) which at the moment limit a full understanding of their biology.

  • Many model plants are compatible hosts for arbuscular mycorrhizal fungi.

  • The transduction signalling pathways which control arbuscular mycorrhizal establishment and legume/rhizobium nodule formation are at least partly the same.

  • Plant cells undergo complex cellular and molecular reprogramming when they accommodate the AM fungus.

  • The core of a functioning arbuscular mycorrhiza lies at the interface between the two partners.

Keywords: arbuscular mycorrhizas; Glomeromycota; ectomycorrhizas; nutrient exchange; interface compartment; rhizosphere; genome sequencing; signalling molecules; GFP plants; cell compatibility

Figure 1.

The two major types of mycorrhiza are illustrated: an ectomycorrhiza (ECM) on the right and an arbuscular mycorrhiza (AM) on the left. The fungal mantle in ECMs surrounds the root from the tip, whereas the Hartig net is usually developed around the epidermal cells. AM fungal hyphae develop from the spore and produce a hyphopodium on the epidermis from which intraradical colonisation starts. Meristems are usually not colonised. Arbuscules, the little fungal trees, are produced in the inner cortical cells in the differentiated regions of the root. Arrows from the roots and mycorrhizal fungi indicate the release of diffusible factors (strigolactones, Myc factors, auxin‐like molecules) which are perceived by the reciprocal partners, eliciting the colonisation processes. Courtesy of A. Genre.

Figure 2.

(a) Confocal micrograph showing dual fluorescent staining of a section of hazelnut – Tuber melanosporum ectomycorrhizal root, showing a mantle of packed hyphae and a well‐developed Hartig net, which surrounds epidermal and outer cortical cells, as detailed in (b). (c) Ultrastructural features of the Hartig net of Tuber borchii in a fully 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 (inset). HW, host wall; FW, fungal wall. Bars: (a) 20 μm (micrometer); (b) 10 μm and (c) 2.5 μm. Courtesy of R. Balestrini.

Figure 3.

(a) Light micrograph showing arbuscules of Gigaspora margarita, an AM fungus in the roots of Lorus japonicus. The fungus determines a typical Arum morphology: that is an intercellular hypha moves from the spaces of the cortex towards the inner cortical cells creating terminal arbuscules. The fungal structures are stained by cotton blue. Courtesy of M. Novero. (b) An arbuscule from the same Lo. japonicus root is seen under electron microscope revealing the morphological reprogramming of the host cell. Plant nucleus (HN) is entangled by the arbuscule branches which are surrounded by the perifungal membrane, as well as by a labyrinthine vacuole. Bars correspond to 100 μm and 1,00 μm, respectively.

Figure 4.

AM fungal or Rhizobium‐derived signals are perceived by plant receptors and trigger a signal transduction pathway, mediated by at least seven shared components, which are illustrated using Lo. japonicus protein nomenclature. The symbiosis receptor kinase SYMRK acts upstream the Ca2+ spiking which is located around and inside the nucleus. The twin CASTOR and POLLUX are potassium‐permeable channels and are required for calcium oscillations together with the nucleoporins NUP133 and NUP85. A calcium calmodulin‐dependent protein kinase (CCaMK) acting downstream of Ca2+ spiking forms a complex with CYCLOPS and may be involved in decoding the calcium signature. Reproduced from Parniske , With permission from Nature Publishing Group.

Figure 5.

Electron micrograph illustrating the details of the plant–fungal interface in an AM root of Gingko biloba: arbuscular branches are surrounded by the membrane of host origin (large arrow), limiting the interface compartment (IM) where plant cell wall molecules are laid down in the interface. Here the golden granules (**) point to pectins revealed by a specific antibody. Plant cytoplasm – enriched in mitochondria (M) and membranes (m) is pinched between the perifungal membrane and the vacuolar tonoplast (thin arrow). Mycorrhiza‐specific phosphate transporters (P) have been detected on the perifungal membrane. Bar corresponds to 0,20 μm.

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Further Reading

Bucher M (2007) Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytologist 173: 11–26.

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Peterson RL, Massicotte HB and Melville LH (2004) Mycorrhizas: Anatomy and Cell Biology. Ottawa, ON: NRC Research Press. p. 173.

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Bonfante, P(Jun 2010) Plant–Fungal Interactions in Mycorrhizas. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0022339]