The Arabidopsis LHT1 amino acid transporter contributes toPseudomonas simiae-mediated plant-growth promotion by modulating bacterial metabolism in the rhizosphere

Abstract

Belowground microbiome structure ensures optimal plant-host health and fitness, and it is, at least in part, defined by the plant genotype. Root-secreted amino acids (AAs) promote microbial chemotaxis and growth in the rhizosphere. However, whether the plant-mediated reuptake of AAs contributes to maintaining optimal levels of AAs in the rhizosphere, and in turn, microbial growth, remains to be established. The Arabidopsis thaliana LHT1 is a high-affinity transporter expressed in the rhizodermis that can take up AAs from the soil. Here we show that a loss-of-function mutant for LHT1 leads to increased accumulation of plant-derived amino acids in the root exudates and that lht1 root exudates enable more growth of the plant-growth-promoting bacteria (PGPB) Pseudomonas simiae WCS417r (Ps WCS417r). Amino acid profiling of the lht1 exudates showed increased levels of glutamine (Gln) and other amino acids. Excitingly, supplementing wild-type root exudates with Gln was sufficient to promote Ps WCS417r growth. However, intriguingly, despite promoting Ps WCS417r growth, lht1 exudates and wild-type exudates supplemented with Gln inhibit plant growth in a Ps WCS417r-dependent manner. These data suggest that an excess of AAs in the rhizosphere impacts Ps WCS417r metabolism which in turn inhibits plant growth. Together, the results unveil that LHT1 regulates the amino acid-mediated interaction between plants and Ps WCS417r and suggest a complex relationship between root-exuded metabolites, PGPB, and plant growth.