Bacterial auxin catabolism as a driver of plant growth promotion and rhizosphere colonization fitness

Inter-kingdom communication between plants and their associated microbiota is central to plant development and environmental adaptation. Indole-3-acetic acid (IAA) is the primary auxin in plants and regulates plant growth and development, while also modulating bacterial physiology and behavior. The concentration at which IAA exerts its biological effects in plants is critical and maintaining auxin homeostasis is essential. Although IAA production by plant growth-promoting bacteria typically stimulates plant growth, excessive IAA levels can be detrimental to plant physiology. Here, we investigate the in planta functional role of bacterial IAA catabolism using Pseudomonas putida 1290, a model plant-associated bacterium that degrades IAA through the Iac aerobic pathway. By constructing a mutant strain defective in the iac gene cluster, we show that IAA catabolism is essential for reversing auxin-mediated growth inhibition in tomato and maize, both in vitro and in microcosms. In addition, bacterial IAA degradation also prevented the formation of IAA-induced tumor-like structures in maize roots. Moreover, competitive colonization assays revealed that IAA catabolism enhances bacterial fitness in the rhizosphere, particularly under high-auxin conditions. Our findings establish bacterial IAA catabolism as a mechanism of metabolic signal interference that maintains auxin homeostasis in planta and promotes successful rhizosphere colonization. This work highlights the significance of microbial auxin metabolism in shaping plant-microbe interactions and its potential for application in sustainable agriculture strategies.