Plant–Fungal Interactions in Mycorrhizas

P Bonfante, University of Torino, Torino, Italy

Published online: June 2010

DOI: 10.1002/9780470015902.a0022339

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 m (micrometer); (b) 10 m and (c) 2.5 m. 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 m and 1,00 m, 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 (2008), 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 m.
close
 References
    Akiyama K, Matsuzaki K and Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435: 824–827.
    Besserer A, Puech-Pagès V, Kiefer P et al. (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biology 4: 1239–1247.
    book Bonfante P (1984) "Anatomy and morphology of VA Mycorrhizae". In: Powell CL and Joseph Bagyaraj D (eds) VA Mycorrhiza, pp. 5–33. Conway: CRC Press.
    book Bonfante P (2001) "At the interface between mycorrhizal fungi and plants: the structural organization of cell wall, plasma membrane and cytoskeleton". In: Hock B (ed.) Mycota, IX Fungal Associations, pp. 45–91. Berlin: Springer.
    Bonfante P and Anca I (2009) Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annual Review of Microbiology 63: 363–383.
    Bonfante P and Genre A (2008) Plants and arbuscular mycorrhizal fungi: an evolutionary-developmental perspective. Trends in Plant Science 13: 492–498.
    Bucher M, Wegmüller S and Drissner D (2009) Chasing the structures of small molecules in arbuscular mycorrhizal signaling. Current Opinion in Plant Biology 12: 500–507.
    Buée M, Reich M, Murat C et al. (2009) 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversità. New Phytologist 184: 449–456.
    Couturier J, Montanini B, Martin F et al. (2007) The expanded family of ammonium transporters in the perennial poplar plant. New Phytologist 174: 137–150.
    Croll D, Giovannetti M, Koch AM et al. (2009) Nonself vegetative fusion and genetic exchange in the arbuscular mycorrhizal fungus Glomus intraradices. New Phytologist 181: 924–937.
    Felten J, Kohler A, Morin E et al. (2009) The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in poplar and Arabidopsis through auxin transport and signaling. Plant Physiology 151: 1991–2005.
    Genre A, Chabaud M, Faccio A, Barker DG and Bonfante P (2008) Prepenetration apparatus assembly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungi within the root cortex of both Medicago truncatula and Daucus carota. Plant Cell 20: 1407–1420.
    Genre A, Chabaud M, Timmers T, Bonfante P and Barker DG (2005) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17: 3489–3499.
    Gomez-Roldan V, Fermas S, Brewer PB et al. (2008) Strigolactone inhibition of shoot branching. Nature 455: 189–194.
    Guether M, Balestrini R, Hannah M et al. (2009a) Genome-wide reprogramming of regulatory networks transport cell wall synthesis and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. New Phytologist 182: 200–212.
    Guether M, Neuhäuser B, Balestrini R et al. (2009b) A mycorrhizal specific ammonium transporter from Lotus japonicus acquires nitrogen. Plant Physiology 150: 73–83.
    Guimil S, Chang H, Zhu T et al. (2005) Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proceedings of the National Academy of Sciences of the USA 102: 8066–8070.
    Gutjahr C, Banba M, Croset V et al. (2008) Arbuscular mycorrhiza-specific signaling in rice transcends the common symbiosis signaling pathway. Plant Cell 20: 2989–3005.
    Javot H, Penmetsa RV, Terzaghi N, Cook DR and Harrison MJ (2007) A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences of the USA 104: 1720–1725.
    Kosuta S, Chabaud M, Lougnon G et al. (2003) A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiology 131: 952–962.
    Kosuta S, Hazledine S, Sun J et al. (2008) Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes. Proceedings of the National Academy of Sciences of the USA 105: 9823–9828.
    Liu J, Maldonado-Mendoza I, Lopez-Meyer M et al. (2007) Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant Journal 50: 529–544.
    Martin F, Aerts A, Ahr¢en D et al. (2008) The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452: 88–92.
    Martin F, Kohler A, Murat C et al. (2010) Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature (in press).
    Martin F and Nehls U (2009) Harnessing ectomycorrhizal genomics for ecological insights. Current Opinion in Plant Biology 12: 508–515.
    book Martin FM, Perotto S and Bonfante P (2007) "Mycorrhizal fungi: a fungal community at the interface between soil and roots". In: Pinton R, Varanini Z and Nannipieri P (eds) The Rhizosphere: Biochemistry and Organic Substances at the Soil-Plant Interface, 2nd edn, pp. 201–236. Boca Raton, FL: CRC Press.
    Navazio L, Moscatiello R, Genre A et al. (2007) A diffusible signal from arbuscular mycorrhizal fungi elicits a transient cytosolic calcium elevation in host plant cells. Plant Physiology 144: 673–681.
    Oldroyd GE and Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annual Review of Plant Biology 59: 519–546.
    Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature Reviews. Microbiology 6: 763–775.
    Paszkowski U (2006) A journey through signaling in arbuscular mycorrhizal symbioses. Tansley review. New Phytologist 172: 35–46.
    Pumplin N and Harrison MJ (2009) Live-cell imaging reveals periarbuscular membrane domains and organelle location in Medicago truncatula roots during arbuscular mycorrhizal symbiosis. Plant Physiology 151: 809–819.
    book Read DJ (2001) Mycorrhiza. Encyclopedia of Life Sciences. Sheffield, UK: Nature Publishing Group. pp. 1–7.
    book Smith SE and Read DJ (2008) Mycorrhizal Symbiosis. New York: Academic Press.
    Tuskan G, Di Fazio S, Jansson S et al. (2006) The genome of black cottonwood, Populus trichocarpa. Science 313: 1596–1604.
 Further Reading
    Bucher M (2007) Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytologist 173: 11–26.
    Chalot M, Blaudez D and Brun A (2006) Ammonia: a candidate for nitrogen transfer at the mycorrhizal interface. Trends in Plant Science 11: 263–266.
    Gianinazzi-Pearson V, Séjalon-Delmas N, Genre A, Jeandroz S and Bonfante P (2007) Plants and arbuscular mycorrhizal fungi: cues and communication in the early steps of symbiotic interactions. Advances in Botanical Research 46: 181–219.
    Gomez SK, Javot H, Deewatthanawong P et al. (2009) Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis. BMC Plant Biology 9: 10.
    Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annual Review of Microbiology 59: 19–42.
    Küster H, Vieweg MF, Manthey K et al. (2007) Identification and expression regulation of symbiotically activated legume genes. Phytochemistry 68: 8–18.
    Markmann K and Parniske M (2009) Evolution of root endosymbiosis with bacteria: how novel are nodules? Trends in Plant Science 14: 77–86.
    Martin F and Selosse MA (2008) The Laccaria genome: a symbiont blueprint decoded. New Phytologist 180: 296–310.
    Oldroyd GED, Harrison MJ and Paszkowski U (2009) Reprogramming plant cells for endosymbiosis. Science 324: 753–754.
    book Peterson RL, Massicotte HB and Melville LH (2004) Mycorrhizas: Anatomy and Cell Biology. Ottawa, ON: NRC Research Press. p. 173.

Related Sub-Topics:

Evolutionary Ecology | Mutualism and Symbiosis | Fungi | Plant Evolution | Plant Nutrition | Roots and Root Systems
Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Plant–Fungal Interactions in Mycorrhizas
 
How to Cite close
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]