Microbial metabolic configuration modulates plant growth–defense transcriptional responses in Nicotiana benthamiana
TL;DR
It is suggested that metabolically altered bacterial states may be associated with quantitative differences in plant growth- and defense-associated transcriptional responses without altering their directional polarity, and support incorporating bacterial metabolic profiling alongside strain identity as a rational selection criterion for next-generation bioinoculant development in sustainable agriculture.
Abstract
Plant growth-promoting rhizobacteria (PGPR) enhance host fitness through phytohormone modulation, induced systemic resistance, and pathogen suppression, yet whether variation in bacterial metabolic state independently shapes plant transcriptional response pattern remains unresolved. Here, we compare genome-wide transcriptional responses of Nicotiana benthamiana to a characterized PGPR strain (JS) and a UV-induced mutant (MT) harboring mutations including frameshift disruptions affecting nadB and sacX, genes encoding enzymes involved in NAD⁺ biosynthesis and carbon catabolite regulation. MT-treated plants retained the directional framework of JS-induced transcriptional responses but exhibited attenuated amplitude and redistributed relative transcriptional contribution, consistent with preservation of transcriptional response directionality accompanied by reduced expression amplitude rather than qualitative regulatory replacement. JS exposure coordinated pathways associated with energy metabolism, terpenoid and phenylpropanoid biosynthesis, and plant-pathogen interaction, whereas MT redistributed metabolic emphasis toward carbon and lipid metabolism categories. Hormone-associated analyses revealed that JS promoted coordinated auxin-, gibberellin-, and jasmonate/ethylene-centered signaling, while MT exhibited differential salicylic acid- versus jasmonate-associated weighting, suggesting that bacterial metabolic configuration may contribute to variation in growth-defense hormonal balance. Transcription factor profiling identified reconfigured AP2/ERF, GRAS, Dof, and MADS-box family representation under MT, suggesting that metabolic perturbation is associated with altered representation of upstream regulatory components. Phenotypically, MT reduced shoot growth promotion while preserving root architecture and antifungal efficacy, revealing a functional decoupling between metabolically tunable growth-promoting outputs and resilient biocontrol traits. These findings suggest that metabolically altered bacterial states may be associated with quantitative differences in plant growth- and defense-associated transcriptional responses without altering their directional polarity, and support incorporating bacterial metabolic profiling alongside strain identity as a rational selection criterion for next-generation bioinoculant development in sustainable agriculture.