Publication

Blurred boundaries: lifestyle lessons from ectomycorrhizal fungal genomes. Public

Jonathan M. Plett and Francis Martin 2011 January 01 Trends Genet. 2011 Jan;27(1):14-22. doi: 10.1016/j.tig.2010.10.005. Epub 2010 Nov 27.

Abstract

Soils contain a multitude of fungi with vastly divergent lifestyles ranging from saprotrophic to mutualistic and pathogenic. The recent release of many fungal genomes has led to comparative studies that consider the extent to which these lifestyles are encoded in the genome. The genomes of the symbiotic fungi Laccaria bicolor and Tuber melanosporum are proving especially useful in characterizing the genetic foundation of mutualistic symbiosis. New insights gleaned from these genomes, as compared to their saprotrophic and pathogenic cousins, have helped to redefine and shape our understanding of the nature of the symbiotic lifestyle. Here we detail the current state of research into this complex relationship and discuss avenues for future exploration.

Highlights

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Phylogenetic distribution of basidiomycete and ascomycete saprotophic and ectomycorrhizal fungal orders with genomes sequenced or scheduled for sequencing. Because the ECM lifestyle has arisen independently several times from saprotrophic ancestors within the ascomycota (blue box) and the basidiomycota (purple box) [6], the genomes of ECM and saprotrophic fungi from many diverse orders are currently being sequenced within the JGI MycoCosm project to understand better the genetic basis of mutualistic symbiosis. The number of genomes currently available (with upcoming genomes in parentheses) are found in the brown column for sapotrophic and wood decay species and in the green column for ECM species. Orders with sequenced ECM fungi discussed in the text are highlighted in bold and underlined. Additional orders with no sequenced species have been included for completness. Oidiodendron maius, an ascomycete of the Leotiomycete class, has not been included because it does not have a defined order at the time of publication. *, Piriformospora indica, of the Sebacinales order, is a growth-promoting endophyte of Arabidopsis thaliana and is not a true mycorrhizal fungus. Figure adapted from 0380 and 0385.

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Schematic representation of a transverse cross-section of a root undergoing colonization by an ECM fungus. (a) Representation of a transverse cross-section of a plant lateral root before ECM fungal colonization. (b) During the initial contact between the root (green cells) and ECM fungal hyphae (brown cells) the fungus begins by attaching to the root surface. The attachment process causes the fungus to secrete proteins, phytohormones and metabolites that cause restructuring of the root that allows fungal hyphae to penetrate into the root apoplastic space. (c) Representation of a transverse cross-section of a mature mycorrhizal root tip. At this stage of colonization the fungus has completely wrapped around the entire root surface forming a thick, multi-layered ‘mantle’ constructed from individual hyphae (cells outlined in black). A number of fungal hyphae have also invaded between the plant cells of the root, forming a structure called the Hartig net. It is in the Hartig net that nutrient exchange between the fungus and the plant takes place.


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Summary of three key levels of control in the symbiotic interaction between ECM fungi and plant cells. High magnification schematic representation of a hyphal cell (brown) and a plant cell (green) from a transverse cross-section of the Hartig net (see inset for orientation, red box). (a) The main common feature of all plant–ECM fungus mutualistic symbiotic interactions is reciprocal nutrient exchange. Photosynthetically-derived sucrose from the plant is cleaved by invertases (INV) into glucose and fructose in the symbiotic interface. Hexose transporters in the hyphae uptake this glucose which is used by the fungus as its primary carbon source. In return, the fungus releases nutrients (e.g. nitrogen, phosphorus) into the apoplastic space of the root, after which high-affinity plant nutrient importers take these nutrients into the root cell where they are used to support plant growth and metabolism. (b) To establish symbiosis, ECM fungi must have novel signaling pathways, as compared to their saprotrophic cousins, to negotiate a mutualistic relationship with the plant root. Suggested novel signaling pathways are those controlled by tyrosine and tyrosine-like kinases (TKs) that activate signaling cascades within the fungal cells. The signaling pathways controlled by these kinases are unknown. Diffusible elements such as ethylene and auxin have also been implicated in the development of symbiosis between the two partners. (c) A second set of novel control pathways in ECM fungi are those governed by MiSSPs. These secreted proteins are thought to act as effectors to control the fate of plant cells and disrupt plant cell defenses in both the apoplastic space of the root as well as in root cells, although this has yet to be proven. The plant partner is unlikely to be silent in the symbiotic relationship. As has been demonstrated in bacterial symbiosis with plant roots, ECM host plants probably release a fleet of SSPs which, like MiSSPs, are destined to control fungal development within the root. Solid arrows represent known pathways active in ECM root tips; dashed arrows represent hypothesized signaling relays at work during symbiosis. N, nucleus.

Citation

Plett JM, Martin F. Blurred boundaries: lifestyle lessons from ectomycorrhizal fungal genomes. Trends Genet. 2011 Jan;27(1):14-22. doi: 10.1016/j.tig.2010.10.005. Epub 2010 Nov 27. Review. PubMed PMID: 21112661.