Perturbation of Arabidopsis Amino Acid Metabolism Causes Incompatibility with the Adapted Biotrophic Pathogen Hyaloperonospora arabidopsidis

Abstract

Reliance of biotrophic pathogens on living plant tissues to propagate implies strong interdependence between host metabolism and nutrient uptake by the pathogen. However, factors determining host suitability and establishment of infection are largely unknown. We describe a loss-of-inhibition allele of ASPARTATE KINASE2 and a loss-of-function allele of DIHYDRODIPICOLINATE SYNTHASE2 identified in a screen for Arabidopsis thaliana mutants with increased resistance to the obligate biotrophic oomycete Hyaloperonospora arabidopsidis (Hpa). Through different molecular mechanisms, these mutations perturb amino acid homeostasis leading to overaccumulation of the Asp-derived amino acids Met, Thr, and Ile. Although detrimental for the plant, the mutations do not cause defense activation, and both mutants retain full susceptibility to the adapted obligate biotrophic fungus Golovinomyces orontii (Go). Chemical treatments mimicking the mutants' metabolic state identified Thr as the amino acid suppressing Hpa but not Go colonization. We conclude that perturbations in amino acid homeostasis render the mutant plants unsuitable as an infection substrate for Hpa. This may be explained by deployment of the same amino acid biosynthetic pathways by oomycetes and plants. Our data show that the plant host metabolic state can, in specific ways, influence the ability of adapted biotrophic strains to cause disease.

Pipecolic acid enhances resistance to bacterial infection and primes salicylic acid and nicotine accumulation in tobacco

“…However, besides participating in plant defense, free amino acids might also serve as nutrient sources for the invading pathogen, 55 and perturbations of a defined amino acid composition at infection sites can render compatible plant-microbe interactions incompatible. 15,16 In conclusion, the present work demonstrates that pipecolic acid induces resistance to bacterial pathogens, and mediates defense amplification and priming responses in tobacco. We have shown that Pip potentiates the pathogen-induced accumulation of SA and nicotine in tobacco leaves, and we naturally cannot rule out that further, non-examined defense responses are also positively affected.…”

“…15,16 However, the mechanisms by which homoserine and Thr provide plant resistance to oomycete pathogens are not yet defined.…”

The Conjugated Auxin Indole-3-Acetic Acid–Aspartic Acid Promotes Plant Disease Development

“…Recently, Stuttmann et al (2011) described two different mutants of Arabidopsis with increased resistance to the obligate biotrophic pathogen Hyaloperonospora arabidopsidis. The authors showed that this resistant phenotype results from an over accumulation of the Asp-derived amino acid Thr and does not appear to be linked to plant immunity (Stuttmann et al, 2011).…”

Host-related metabolic cues affect colonization strategies of a root endophyte

“…Whereas necrotrophs kill plant cells with subsequent saprotrophic nutrition, other fungi maintain biotrophic relationships with their hosts either transiently (hemibiotrophs) or as lifelong interactions. The degree of specialization to a particular host and the host's metabolic status may greatly influence plant colonization (1)(2)(3)(4). Broad-host range root endophytes undergo long-term interactions with a large variety of plants, thereby playing a significant role in natural and managed ecosystems and in the evolution of land plants.…”