Unraveling the Mechanism of the Endophytic Bacterial Strain Pseudomonas oryzihabitans GDW1 in Enhancing Tomato Plant Growth Through Modulation of the Host Transcriptome and Bacteriome

Endophytic <i>Pseudomonas</i> species from agricultural crops have been extensively studied for their plant-growth-promoting (PGP) potential, but little is known about their PGP potential when isolated from perennial trees. This study investigated the plant-growth-promoting (PGP) potential of an endophyte, <i>Pseudomonas oryzihabitans</i> GDW1, isolated from a healthy pine tree by taking tomato as a host plant. We employed multiomics approaches (transcriptome and bacteriome analyses) to elucidate the underlying PGP mechanisms of GDW1. The results of greenhouse experiments revealed that the application of GDW1 significantly improved tomato plant growth, increasing shoot length, root length, fresh weight, and biomass accumulation by up to 44%, 38%, 54%, and 59%, respectively, compared with control. Transcriptomic analysis revealed 1158 differentially expressed genes significantly enriched in the plant hormone signaling (auxin, gibberellin, and cytokinin) and stress response (plant-pathogen interaction, MAPK signaling pathway-plant, and phenylpropanoid biosynthesis) pathways. Protein-protein interaction network analysis revealed nine hub genes (<i>MAPK10</i>, <i>ARF19-1</i>, <i>SlCKX1</i>, <i>GA2ox2</i>, <i>PAL5</i>, <i>SlWRKY37</i>, <i>GH3.6</i>, <i>XTH3</i>, and <i>NML1</i>) related to stress tolerance, hormone control, and plant defense. Analysis of the tomato root bacteriome through 16S rRNA gene amplicon sequencing revealed that GDW1 inoculation dramatically altered the root bacterial community structure, enhancing the diversity and abundance of beneficial taxa (Proteobacteria and Bacteroidota). Co-occurrence network analysis showed a complex bacterial network in treated plants, suggesting increasingly intricate microbial relationships and improved nutrient absorption. Additionally, FAPROTAX and PICRUSt2 functional prediction analyses suggested the role of GDW1 in nitrogen cycling, organic matter degradation, plant growth promotion, and stress resistance. In conclusion, this study provides novel insights into the symbiotic relationship between <i>P. oryzihabitans</i> GDW1 and tomato plants, highlighting its potential as a biofertilizer for sustainable agriculture and a means of reducing the reliance on agrochemicals.