Soybean Fine-Tunes Defense-Growth Trade-offs via Transcriptional Reprogramming During Beneficial P. chlororaphis Colonization

Rhizosphere-associated plant growth-promoting rhizobacteria (PGPR) critically enhance plant defense and growth. Our previous study identified Pseudomonas chlororaphis IRHB3 from the soybean rhizosphere and demonstrated its efficacy in suppressing soil-borne disease and promoting plant growth. However, the molecular mechanisms underlying IRHB3 colonization of soybean roots remain poorly characterized. In this study, spatio-temporal colonization dynamics revealed that IRHB3 rapidly adhered to the root surfaces and colonized into endosphere by the root tip, with cortical proliferation coinciding with lateral root formation. Transcriptional profiling indicated that early colonization activated pattern-triggered immunity (PTI) and differentially regulated genes associated with transmembrane signaling receptor kinase signaling, MAPK cascade, reactive oxygen species (ROS) burst, and phytohormone signaling. Following endosphere colonization, IRHB3 reprogrammed host transcriptional priorities toward developmental processes, upregulating photosynthesis-related genes and phytohormone pathways that facilitate root morphogenesis. Notably, multiple transcription factor (TF) families were dynamically induced during colonization. Crucially, transient overexpression of early adhesion-responsive GmWRKY22 or GmWRKY29 in soybean hairy roots suppressed IRHB3 colonization and dynamically modulated ROS biosynthesis-related RBOHs expression, whereas RNAi-mediated silencing of either gene enhanced bacterial colonization and attenuated ROS responses. Collectively, our findings demonstrate that soybean co-opts PTI machinery for the early detection of beneficial rhizobacteria while dynamically balancing defense-growth trade-offs. This work provides a mechanistic framework for optimizing PGPR applications in legume cultivation systems.