Comparative genomics-based insights into <i>Pantoea ananatis</i> strains, isolated from white spot diseased leaves of maize with plant growth-promoting attributes

<i>Pantoea ananatis</i> is a member of the Enterobacteriaceae family known for its broad host adaptability. This study isolated 10 <i>P</i>. <i>ananatis</i> strains from white spot (MWS)-diseased leaves of maize (<i>Zea mays</i>) grown in Yunnan Province, China, and analyzed their putative functions, genomic diversity, and variation. The inoculation tests revealed that none of the 10 isolates caused MWS symptoms in maize. Nine maize isolates, except for S47, induced a hypersensitive response (HR) in tobacco and caused rot symptoms in onion. Most isolates exhibited plant growth-promoting characteristics, with strains JCC14, JCY1, and S47 significantly enhancing maize seedling growth parameters. Genomic sequencing of 10 maize isolates and two rice isolates revealed that 12 isolates clustered into three groups, with an open pan-genome identified. Ancestral reconstruction indicated that the genome size increased in Group A and then decreased in Group B, with significant gains in orthologous groups at Node 14, the most recent common ancestor (MRCA) of Group A and Group B, and at Node 19, the MRCA of seven maize-isolated strains and other Group B strains. Additionally, 11 single-copy orthologous groups were under positive selection. Furthermore, the HIVir (high virulence, also known as PASVIL, <i>P. ananatis</i>-specific virulence locus) cluster and type VI secretion system-related genes were conserved in certain <i>P. ananatis</i> strains but were not related to their group divergences. This study not only reveals the diverse functions of MWS-diseased maize <i>P. ananatis</i> isolates, but also enhances our understanding of divergent genome evolution and environmental adaptation across <i>P. ananatis</i> species.IMPORTANCE<i>Pantoea ananatis</i> is a bacterium commonly found in various agronomic crops. Maize white spot (MWS) has been one of the most destructive diseases affecting maize, leading to significant economic losses. This study clarified that <i>P. ananatis</i> strains colonized maize leaves but were not the causal agents of MWS in Yunnan Province, China. Moreover, most of these <i>P. ananatis</i> strains exhibited plant growth-promoting (PGP) activities, induced hypersensitive response (HR) activity on tobacco, and caused rot symptoms in onion. Notably, the analysis of divergence throughout the evolutionary process revealed significant genomic evolution and environmental adaptation in these <i>P. ananatis</i> strains. This highlights the genetic exchange that has shaped the genome of <i>P. ananatis</i>. These findings improve our understanding of the functional diversity of <i>P. ananatis</i> strains across different hosts and their positions within the evolutionary lineages of <i>P. ananatis</i> species.