Pseudomonas fluorescens P34 colonization impacts expression changes in wheat roots, reshapes rhizosphere microbial communities and promotes wheat plant growth.

Plant growth-promoting rhizobacteria (PGPR) can stimulate crop growth and performance through multiple mechanisms, making them promising bioinoculants for sustainable agriculture. Among known PGPR species, Pseudomonas fluorescens has attracted considerable attention because of its superior growth-promoting mechanisms and broad adaptability. Although P. fluorescens P34 has excellent colonization and growth-promoting abilities, the molecular and ecological mechanisms underlying its growth-promoting effects remain poorly understood. Here, we conducted a 25-day pot experiment utilizing an integrated approach combining transcriptomics and microbial amplicon sequencing to investigate how P. fluorescens P34 influences wheat gene expression profiles and the response of the indigenous rhizosphere microbial community to P34 colonization. P34 application increased the seedling fresh weight, seedling dry weight, root fresh weight, root dry weight, phosphorus content, nitrogen content in wheat leaves and available phosphorus content in rhizosphere soil by 39.61 %, 29.67 %, 84.07 %, 64.71 %, 43.05 %, 17.79 % and 14.45 %, respectively, while it increased the length, projected area and number of forks of the wheat root system by 17.35 %, 35.87 % and 23.57 %, respectively. RNA sequencing revealed 3166 differentially expressed genes that were predominantly involved in nitrogen and phosphorus transport, carbohydrate metabolism, phytohormone biosynthesis and transport, and plantmicrobe signaling recognition. Moreover, microbial community dynamic modulation demonstrated that strain P34 induced shifts in the indigenous rhizosphere microbiome by enriching beneficial microorganisms (e.g., Massilia and Pseudomonas) while reducing potential pathogens. These findings revealed the molecular and ecological mechanisms underlying PGPR-mediated plant growth promotion, providing new insights for optimizing PGPR applications in sustainable agriculture ‌and demonstrating its potential to reduce chemical fertilizer dependency while enhancing soil health in agroecosystems‌.