Daniele Nicotra ^1,2 Farideh Ghadamgahi ³ Samrat Ghosh ³ Alice Anzalone ¹ Giulio Dimaria ¹ Alexandros Mosca ¹ Maria E. Massimino ¹ Ramesh R. Vetukuri ^3* Vittoria Catara ^1*

• ¹ Department of Agriculture Food and Environment, University of Catania, Catania, Sicily, Italy
• ² Department of Biomedical and BIotechnology Science, University of Catania, Catania, Sicily, Italy
• ³ Department of Plant Breeding, Faculty of Landscape Architecture, Horticulture and Crop Production Science, Swedish University of Agricultural Sciences, Alnarp, Sweden

Despite their adverse environmental effects, modern agriculture relies heavily on agrochemicals to manage diseases and pests and enhance plant growth and productivity. Some of these functions could instead be fulfilled by endophytes from the plant microbiota, which have diverse activities beneficial for plant growth and health. We therefore used a microbiome-guided top-down approach to select ten bacterial strains from different taxa in the core microbiome of tomato plants in the production chain for evaluation as potential bioinoculants. These taxa included some that are commonly used as biofertilizers and biocontrol agents (Pseudomonas and Bacillus) as well as the less studied genera Leclercia, Chryseobacterium, Glutamicibacter, and Paenarthorbacter. When inoculated in the tomato rhizosphere, these strains promoted plant growth and reduced the severity of Fusarium Crown and Root Rot and Bacterial Spot infections. High-quality genomes for each strain were obtained using Oxford Nanopore long-read and Illumina short-read sequencing, enabling the dissection of their genetic makeup to identify phyto-beneficial traits. This yielded a comprehensive inventory of genes from each strain related to processes including colonization, biofertilization, phytohormones, and plant signaling. Traits directly relevant to fertilization including phosphate solubilization and acquisition of nitrogen and iron were also identified. Moreover, the strains carried several functional genes putatively involved in abiotic stress alleviation and biotic stress management, traits that indirectly foster plant health and growth. This study employs a top-down approach to identify new plant growth-promoting rhizobacteria (PGPRs), offering an alternative to the conventional bottom-up strategy. This method goes beyond the traditional screening of the strains and thus can expand the range of potential bioinoculants available for market application, paving the way to the use of new still underexplored genera.