Establishing compatibility between plants and obligate biotrophic pathogens

Abstract

The apparent under-representation of the term ‘plant disease susceptibility’ as opposed to ‘plant disease resistance’ in the current scientific literature might indicate that ‘compatibility’ has not gained the same appreciation as ‘resistance’ in the past. However, these seemingly contrary phenomena are intimately linked, and progress in understanding one process inherently contributes to our comprehension of the other. Recent progress in analyzing plant–biotroph compatibility includes the molecular isolation and functional characterization of haustorium-specific cDNAs that encode presumptive hexose- and amino-acid-transporter proteins for proton-driven nutrient uptake. Accumulating evidence from cytological, pharmacological, phytopathological and molecular studies indicates that pathogens mediate the suppression of host defenses in a range of plant–biotroph interactions. Arabidopsis thaliana mutants that are resistant to powdery or downy mildew but that do not exhibit constitutively activated defense could be affected in host-compatibility factors.

Introduction

Obligate biotrophs, such as powdery mildews, downy mildews and rust fungi, constitute a phylogenetically unrelated group of phytopathogens that cannot be extensively cultured in vitro and that form specialized infection structures, haustoria, within infected host cells [1]. Convergent evolution of haustoria has apparently occurred in oomycetes (e.g. Peronospora parasitica), ascomycetes (e.g. powdery mildews, such as Blumeria and Erysiphe ssp.), and basidiomycetes (e.g. rusts, such as Puccinia ssp.). This suggests that the ability to form haustoria is either indispensable for obligate biotrophs or creates a selective advantage to these pathogens (e.g. facilitating access to intracellular pools of solutes that are not available in the apoplast [1]). In contrast to necrotrophic and hemibiotrophic fungal and oomycete pathogens, which have no or only a limited biotrophic phase, obligate biotrophs are entirely dependent on living plant tissue for their growth and propagation. The initial phases of pathogenesis do not differ fundamentally among obligate biotrophs, hemibiotrophs and necrotrophs, and commonly include spore adhesion, appressorium formation and penetration [2]. At later stages, differences become evident as biotrophs establish haustoria within living plant cells and redirect the host’s metabolism to meet their own needs without causing the death of host cells. By contrast, necrotrophic and hemibiotrophic fungi trigger host cell death either immediately (e.g. by secretion of toxins) or during the course of infection. Lack of host cell death in plant–biotroph interactions might be accomplished by the pathogen’s ability to avoid or durably suppress pre-formed and induced host defenses [2]. It is plausible that specific host genes and/or proteins are targeted by biotrophs to achieve these goals, and as such may be considered to be compatibility factors that are essential for successful pathogenesis.

In this review, I summarize recent findings on the potential role of haustoria in the biotrophic lifestyle, on defense suppression in various plant–biotroph interactions, and on host mutants in which potential compatibility factors are affected.