Altered Arabidopsis thaliana sugar metabolism affects exudation, immune responses, and plant-microbe interactions

Abstract

Sugars are critical for plant growth, development, and environmental interactions. They have multiple roles as nutrients for plants, associated beneficial and pathogenic microbes, and as signaling compounds for immunity. We characterize the interconnectedness of these functions by analyzing sugar metabolism and transporter mutant lines. We find that in these lines, root-derived compounds, exudates, are significantly altered in comparison with wild-type not only for carbohydrates, but also for lipids, organic acids, and defense compounds. Quantification of sugar exudation reveals more carbon release during the day than at night, altered sugar exudation in mutant lines, and an opposite exudation pattern with elevated exudation at night for pgm1, a line deficient in starch synthesis. Sugar levels in exudates and tissues did not correlate, suggesting a controlled mode of exudation for sugars. Altered sugar levels have functional consequences: mutant lines exhibit increased resistance against the pathogen Pseudomonas syringae and harbor altered numbers of microbes on roots. Day- and nighttime exudates of mutant lines impact the growth of single microbes such as an inability to grow for Bacillus subtilis. Exogenous sugar alters the production of reactive oxygen species in a plant development-dependent manner with opposite effects at 9 days and 14 days. An RNAseq experiment reveals candidate genes potentially involved in this regulation. Our data highlight that sugar metabolism is intricately linked with other metabolite pathways. Alteration of single genes in central carbon metabolism profoundly alters plant immune responses and plant-microbe interactions.