The peanut root exudate increases the transport and metabolism of nutrients and enhances the plant growth-promoting effects of burkholderia pyrrocinia strain P10

BACKGROUND: Burkholderia pyrrocinia strain P10 is a plant growth-promoting rhizobacterium (PGPR) that can substantially increase peanut growth. However, the mechanisms and pathways involved in the interaction between B. pyrrocinia P10 and peanut remain unclear. To clarify complex plant–PGPR interactions and the growth-promoting effects of PGPR strains, the B. pyrrocinia P10 transcriptome changes in response to the peanut root exudate (RE) were elucidated and the effects of RE components on biofilm formation and indole-3-acetic acid (IAA) secretion were analyzed. RESULTS: During the early interaction phase, the peanut RE enhanced the transport and metabolism of nutrients, including carbohydrates, amino acids, nitrogen, and sulfur. Although the expression of flagellar assembly-related genes was down-regulated, the expression levels of other genes involved in biofilm formation, quorum sensing, and Type II, III, and VI secretion systems were up-regulated, thereby enabling strain P10 to outcompete other microbes to colonize the peanut rhizosphere. The peanut RE also improved the plant growth-promoting effects of strain P10 by activating the expression of genes associated with siderophore biosynthesis, IAA production, and phosphorus solubilization. Additionally, organic acids and amino acids were identified as the dominant components in the peanut RE. Furthermore, strain P10 biofilm formation was induced by malic acid, oxalic acid, and citric acid, whereas IAA secretion was promoted by the alanine, glycine, and proline in the peanut RE. CONCLUSION: The peanut RE positively affects B. pyrrocinia P10 growth, while also enhancing colonization and growth-promoting effects during the early interaction period. These findings may help to elucidate the mechanisms underlying complex plant–PGPR interactions, with potential implications for improving the applicability of PGPR strains. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-023-02818-9.