Chloroplast-associated metabolic functions influence the susceptibility of maize to Ustilago maydis

Biotrophic fungal pathogens must evade or suppress plant defence responses to establish a compatible interaction in living host tissue. In addition, metabolic changes during disease reflect both the impact of nutrient acquisition by the fungus to support proliferation and the integration of metabolism with the plant defence response. In this study, we used transcriptome analyses to predict that the chloroplast and associated functions are important for symptom formation by the biotrophic fungus Ustilago maydis on maize. We tested our prediction by examining the impact on disease of a genetic defect (whirly1) in chloroplast function. In addition, we examined whether disease was influenced by inhibition of glutamine synthetase by glufosinate (impacting amino acid biosynthesis) or inhibition of 3-phosphoshikimate 1-carboxyvinyltransferase by glyphosate (influencing secondary metabolism). All of these perturbations increased the severity of disease, thus suggesting a contribution to resistance. Overall, these findings provide a framework for understanding the components of host metabolism that benefit the plant versus the pathogen during a biotrophic interaction. They also reinforce the emerging importance of the chloroplast as a mediator of plant defence.