Interconnected Metabolism of Host Plants and Obligate Biotrophic Pathogens

Abstract

Downy mildew disease, caused by obligate biotrophic oomycetes in the family Peronsporaceae, affects a wide range of flowering plants, including numerous monocot and dicot crops. Species from the Hyaloperonospora genus are causal agents of downy mildew in Arabidopsis thaliana and many other Cruciferae species, including crops such as broccoli, cabbage, and canola, and the Arabidopsis/ Hyaloperonospora arabidopsidis pathosystem is an established model for downy mildews (Coates and Beynon, 2010). Obligate biotrophic parasites depend on living host cells for their growth and reproduction (reviewed in O’Connell and Panstruga, 2006). This means that, following successful infection, the parasite must establish connections within plant cells (e.g., haustoria) and obtain nourishment from the host without causing immediate host cell death. Therefore, changes in the metabolic state of the host might be expected to influence the growth of obligate biotrophic pathogens and the development of disease. In new work, Stuttmann et al. (pages 2788–2803) describe two distinct mutants of Arabidopsis ,b oth of which show increased resistance to H. arabidopsidis (Hpa) resulting from a disruption in amino acid metabolism causing overaccumulation of the amino acid Thr. Although the mutant plants overaccumulated all three Asp-derived amino acids, Thr, Ile, and Met, enhanced resistance was found to be related specifically to Thr accumulation. Mutant plants that overaccumulate only Met were not hyperresistant to Hpa, and pretreatment of plants with Thr, but not Ile, led to reduced Hpa sporulation (see figure). In addition, the mutations did not cause constitutive plant defense activation, and enhanced resistance did not appear to be linked to plant immunity. Rather, the effect appeared to be due to a loss of susceptibility (i.e., Thr overaccumulation somehow rendered the plant unsuitable for Hpa infection). Interestingly, this effect was specific for Hpa susceptibility, since pretreatment of plants with Thr did not affect sporulation of another obligate biotroph, the powdery mildew ascomycete Golovinomyces orontii (Go). The authors addressed the question of how overaccumulation of Thr might affect Hpa but not Go. Excess Thr is known to be toxic to Arabidopsis, and, indeed, the mutants described in this study were smaller than wild-type plants. An assessment of genes and biochemical pathway components present in the different phyla provided support for the notion that oomycetes and plants might use similar pathways of amino acid biosynthesis and metabolism in a distinct manner from the more distantly related ascomycete. Thus, the toxic effect of high Thr accumulation might be shared among plants and oomycetes, but not by the fungal ascomycete Go. These data provide solid examples of how plant host metabolic state can influence growth and pathogenicity of adapted biotrophic pathogens.