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Abstract

Plants tightly associate with an array of diverse bacteria, with which they share complex and fascinating interactions, including parasitism, mutualism, and commensalism. These plant-associated (PA) bacteria have evolved a large set of genes that enable them to adapt to the plant environment. The functions of these genes are in many cases poorly studied and lack sufficient mechanistic understanding to facilitate microbiome engineering. Here, we sequenced 485 genomes of bacterial isolates and single cells isolated from the root environments of Arabidopsis, poplar, and maize. We then employed a large-scale comparative genomics study to characterize PA genes, and in particular root-associated (RA) genes. This was done by comparing 20 million genes from 3900 high quality and phylogenetically diverse bacterial genomes that were classified based on their isolation site. Several genomic features are common to most PA bacteria, such as the expansion of carbohydrate metabolism regulons. Many of the PA genes are encoded within putative gene operons. Novel PA genes include a rapidly evolving virulence factor in the Acidovorax genus, a phage-like secretion system, and bacterial proteins with plant-like domains. The large PA and RA gene repository and the novel sequenced RA bacterial genomes will not deepen our basic understanding of plant-microbe interactions, but will enable engineering of beneficial interactions for improved crop productivity and agricultural sustainability.