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.
IntroductionPenetration 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.Linking cell wall structure to biotic stress signalling Callose, a (1!3)-b-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 barrie...