Knocking on the heaven’s wall: pathogenesis of and resistance to biotrophic fungi at the cell wall

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Abstract

New findings challenge the traditional view of the plant cell wall as passive structural barrier to invasion by fungal microorganisms. A surveillance system for cell wall integrity appears to sense perturbation of the cell wall structure upon fungal attack and is interconnected with known plant defence signalling pathways. Biotrophic fungi might manipulate this surveillance system for the establishment of biotrophy. The attempts of fungi to invade also induce a sub-cellular polarisation in attacked cells, which activates an ancient vesicle-associated resistance response that possibly enables the focal transport of regulatory cargo and the secretion of toxic cargo. The underlying resistance machinery might have been subverted by biotrophic fungi for pathogenesis.

Introduction

Penetration through the plant cell wall represents an Achilles heel in the pathogenesis of most biotrophic fungi and marks a lifestyle transition from extra-cellular to invasive growth. Modification of the plant cell wall was recognised for the first time as potential resistance mechanism almost 80 years ago following work in which 78 plant species and varieties were challenged with Alternaria spp. and other leaf-spotting fungi [1]. The termination of fungal pathogenesis at the cell wall was commonly associated with wall ‘thickenings’ and the formation of local additions or ‘callosities’ in the paramural space (i.e. the space between the cell wall and the plasma membrane). Formation of these cell wall appositions (CWAs) or papillae is usually accompanied by a co-localised accumulation of phenolics and reactive oxygen species 2., 3., 4., 5., 6.. The complex process of sub-cellular cell wall remodelling is tightly linked to the rapid disassembly and subsequent focal reassembly of the plant cytoskeleton at fungal entry sites, which is indicative of a pathogen-triggered cell polarisation 6., 7., 8., 9.. There has been a long-standing controversy, however, over whether CWAs function in disease resistance or facilitate the entry of fungal pathogens into host cells by providing a structural collar for the intruder. New molecular genetic data from Arabidopsis and barley have indeed revealed that molecular processes at and in CWAs have Janus-faced functions, that is, functions for fungal pathogenesis and in resistance responses. Focal vesicle transport and vesicle fusion events that are dependent on SNAP (soluble N-ethylmaleimide-sensitive-factor-association protein) receptor (SNARE) proteins at the plasma membrane emerge as potential common underlying mechanisms that might be interconnected with a poorly understood cell wall integrity surveillance system. In this review, I discuss the seemingly paradoxical functions of these processes in establishing the biotrophic lifestyle and in disease resistance at the cell periphery.

Section snippets

Linking cell wall structure to biotic stress signalling

Callose, a (1→3)-β-d-glucan, has long been known to be synthesised and deposited rapidly at CWAs upon microbial attack. This polymer was thought to contribute to a physical barrier that slowed the invading microorganism and enabled the plant to focus anti-microbial compounds, such as wall-degrading enzymes, phytoalexins and active oxygen species, upon them [10]. Recently, it has been shown that a single glucan synthase-like isoform in Arabidopsis, GLUCAN SYNTHASE-LIKE5 (GSL5)/POWDERY MILDEW

SNARE proteins and the first line of defence against fungal intruders

The other half of the Janus-faced biological functions at CWAs was revealed by the isolation of a novel class of Arabidopsis mutants and a previously described barley mutant 21.•, 22.. This work links processes at the cell wall with nonhost resistance to powdery mildew fungi. In wildtype Arabidopsis, nonhost resistance to the grass powdery mildew fungus Blumeria graminis f. sp. hordei (Bgh) is tightly associated with CWA formation and the failure of fungal sporelings to enter attacked leaf

Suppression of disease resistance at the cell wall

The detection of an ancient SNARE-dependent and vesicle-associated process that mediates effective nonhost resistance to Bgh in Arabidopsis and inefficient basal penetration resistance to this pathogen in the host barley raises the question of how biotrophic fungi bypass this ‘first line of defence’ in compatible interactions. Recent data suggest that the fungus might suppress the SNARE-dependent resistance layer by misuse of another host protein, MLO. Homozygous loss-of-function alleles of MLO

Intracellular accommodation of fungal infection structures

The invasive growth of biotrophs after cell wall penetration leads to the invagination of the plasma membrane and creates an interface between host and fungus that consists of the haustorial membrane, an extra-haustorial matrix, and the extra-haustorial membrane, which follows the contours of the haustorial membrane (Figure 1b; [52]). The presumed role of the haustorium in nutrient absorption has been supported experimentally by the identification and functional characterisation of

Conclusions

There is an intriguing possibility that pathogenic and symbiotic biotrophic fungi have evolved similar strategies to manipulate normally coupled exo- and endocytosis pathways such that exocytosis prevails. It remains to be shown whether the same or different vesicle-trafficking pathways become activated in response to attempted cellular invasion by both classes of fungal microorganisms. In this context, it might be relevant that the expression of the MtPT4 gene occurs exclusively in cells

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • of special interest

  • ••

    of outstanding interest

Acknowledgements

This work was supported by funds from the Max Planck Society granted to P S-L.

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