Friends or foes? Emerging insights from fungal interactions with plants

Abstract

Fungi interact with plants in various ways, with each interaction giving rise to different alterations in both partners. While fungal pathogens have detrimental effects on plant physiology, mutualistic fungi augment host defence responses to pathogens and/or improve plant nutrient uptake. Tropic growth towards plant roots or stomata, mediated by chemical and topographical signals, has been described for several fungi, with evidence of species-specific signals and sensing mechanisms. Fungal partners secrete bioactive molecules such as small peptide effectors, enzymes and secondary metabolites which facilitate colonization and contribute to both symbiotic and pathogenic relationships. There has been tremendous advancement in fungal molecular biology, omics sciences and microscopy in recent years, opening up new possibilities for the identification of key molecular mechanisms in plant-fungal interactions, the power of which is often borne out in their combination. Our fragmentary knowledge on the interactions between plants and fungi must be made whole to understand the potential of fungi in preventing plant diseases, improving plant productivity and understanding ecosystem stability. Here, we review innovative methods and the associated new insights into plant-fungal interactions.

Keywords: advanced microscopy; crop productivity; phytopathogenic and symbiotic fungi; plant defence response; plant receptors; plant–fungal interactions.

Figure 1.

Comparison of different plant–fungus interactions. Mutualistic associations occupy the mutual benefit (+ +) quadrant in diagrams contrasting the relative benefits (+) or harm (–) to two interacting organisms. The figure was redrafted with permission from Adjunct Associate Professor Mark Brundrett, Plant Biology, University of Western Australia; (http://mycorrhizas.info/download/pdf/symb-assoc.pdf).

Figure 2.

Mycoparasitic attack of T. atroviride induces tip growth arrest, tip swelling and cell lysis in B. cinerea. (A) Before B. cinerea (expressing cytoplasmic GFP; Schumacher et al.2012) is attacked by T. atroviride, the apical cell wall extends quickly and hence shows only weak staining with the chitin-specific fluorescent dye Congo Red (arrowheads). (B) As soon as there is an attack, hyphal tip growth arrests, leading to tip swelling and increased deposition of chitin in the apical cell wall (arrowheads). (C) Tip lysis of the prey hypha results in the release of cytoplasm into the surroundings (asterisks and inset), which can be used as nutrient substrate by T. atroviride. Scale bars, 20 μm.

Figure 3.

Disease cycle. For details see text.

Figure 4.

Schematic representation of induced immune responses in plants. SAR is a long-lasting and broad-spectrum induced disease resistance and evidence accumulated that the SA-induced pathway is primarily triggered by fungal biotrophic pathogens while the pathway induced by necrotrophic and symbiotic fungi relies on JA and ET as signalling molecules and is designated as ISR (Induced Systemic Resistance) (adopted from Pieterse et al. ; redrafted with permission).

Figure 5.

Signalling in plant–fungal pathogen interaction. The first defence line of plants is based on receptor proteins located in the plasma membrane. PRRs recognize conserved microbial structures (MAMPs/PAMPs) which lead to activation of PTI via calcium signalling and MAPK cascades. Pathogens interfere with PTI through effectors, inducing susceptibility known as effector-triggered susceptibility (ETS) by blocking the PTI response. On the other hand, effector recognition by plant R proteins triggers an immune reaction designated as effector-triggered immunity (ETI) (adopted from Kazan and Lyons ; redrafted with permission).

Figure 6.

(a) Disease triangle illustrating the interactions among pathogen, host and the environment. The triangle serves as a conceptual model describing the environmental factors that may affect the host–pathogen interaction and favour disease in the development of an epidemic. Climate directly and indirectly affects plant health by altering abiotic conditions. It also has an influence on forest health by directly acting on various pathogens (insect pests and fungal symbionts). (b) The interactions among G. clavigera, its vector mountain pine beetle (MPB) and their host trees (P. contorta) under climate change. (I) Climate change causing e.g. drought may stress the trees. (II) Mountain pine beetle builds galleries in the infected conifer during range expansion and mass attack. A culture of Grosmannia clavigera is isolated from infected conifer. (III). Many lodgepole pines are killed during the epidemics in BC, Canada.