The LHT1 amino acid transporter limits Pseudomonas simiae growth in the rhizosphere, an essential function for bacteria-mediated plant growth promotion

Abstract

The root microbiome structure ensures optimal plant-host health and fitness, and it is, at least in part, defined by the plant genotype. It is well-documented that root-secreted amino acids promote microbial chemotaxis and growth in the rhizosphere. However, whether the plant-mediated re-uptake of amino acids contributes to maintaining optimal levels of amino acids in the root exudates, and in turn, microbial growth and metabolism, remains to be established. Here we show that LHT1, an amino acid inward transporter expressed in Arabidopsis thaliana roots, limits the growth of the plant-growth-promoting bacteria Pseudomonas simiae WCS417r (Ps WCS417r). Amino acid profiling of the lht1 mutant root exudates showed increased levels of glutamine, among other amino acids. Interestingly, lht1 exudates or Gln-supplemented wild-type exudates enhance Ps WCS417r growth. However, despite promoting bacterial growth and robust root colonization, lht1 exudates and Gln-supplemented wild-type exudates inhibited plant growth in a Ps WCS417r-dependent manner. Transcriptional analysis of defense and growth marker genes revealed that plant growth inhibition was not linked to the elicitation of plant defense, but likely to the impact of Ps WCS417r amino acids metabolism on auxin signaling. These data suggest that an excess of amino acids in the rhizosphere impacts Ps WCS417r metabolism which in turn inhibits plant growth. Together, these results unveil that LHT1 regulates the amino acid-mediated interaction between plants and Ps WCS417r and suggest a complex relationship between root-exuded amino acids, root colonization by beneficial bacteria, bacterial metabolism, and plant growth promotion.