Host legume-exuded antimetabolites optimize the symbiotic rhizosphere

Abstract

Rhizobia form symbiotic nodules on host legumes and fix nitrogen for their hosts in exchange for nutrients. In order to establish this mutually beneficial relationship, rhizobia must compete with other soil bacteria in the host legume rhizosphere to colonize plant roots efficiently. A promoter-trap transposon screen in Mesorhizobium tianshanense, a Rhizobium that forms nodules on licorice (Glycyrrhiza uralensis) plants revealed that the expression of msiA, which encodes a putative exporter protein belonging to the LysE family of translocators, is activated by both legume exudates and MsiR, a LysR family transcriptional regulator. Chemical analysis suggests that the msiA-inducing signal in exudates is canavanine, an anti-metabolite present in the seeds and exudates of a variety of legume plants. We show that MsiA serves as a canavanine exporter that is indispensable for canavanine resistance in M. tianshanense. We also show that the expression of MsiA homologues in other rhizobial species is induced by canavanine and is critical for canavanine resistance. Furthermore, rhizobial canavanine resistance is important for root hair adherence as well as for survival in a canavanine-producing legume rhizosphere. Together, these data suggest that host legumes may exude specific antimetabolites into their surroundings to optimize the bacterial population in order to have successful symbiotic events with rhizobia.