Phyllosphere microbes are associated with variety-specific accumulation of di-n-butyl phthalate in choysum ().

Plant-microbe interactions in the phyllosphere have been demonstrated to facilitate plant growth and enhance resistance to diverse stresses, but the resulting effect on bioaccumulation of contaminants in plants is rarely considered. Here, by comparing differences in the phyllosphere morphology, bacterial community assembly, and metabolites between two choysum () varieties differing in di-n-butyl phthalate (DBP) accumulation, we revealed associations between the key phyllosphere exudate (fumarate) and the recruited specific microbes that may contribute to the variety-specific DBP accumulation in choysum. Compared with the DBP-high accumulation variety (HAV), the DBP-low accumulation variety (LAV) could not only enhance the recruitment of phyllosphere microbes capable of degrading DBP by increasing fumarate secretion, but also facilitate the colonization of DBP-degrading bacteria via induction of biofilm formation, ultimately resulting in lower DBP accumulation in leaves. These findings offer novel insights into the LAV formation from the phyllosphere microbial perspective and highlight the role of phyllosphere microbes in mediating pollutant accumulation within crops, which is instrumental in minimizing pollutant accumulation through regulating the phyllosphere microbial community.IMPORTANCEThe bioaccumulation of phthalic acid esters (PAEs) in crops poses significant concerns for food safety, attracting considerable attention. Although existing studies have primarily elucidated the formation mechanisms of crop varieties with low PAE accumulation at both physiological and molecular levels, the role of phyllosphere microbiota remains uninvestigated. Specifically, the mechanisms through which these microbiotas mitigate PAE accumulation, along with the key exudate components involved, are still poorly comprehended. This study revealed the role of fumarate-a key phyllosphere exudate-and its recruited microbes in determining variety-specific PAE accumulation in choysum, based on the "cry for help" theory and supported by integrated microbiome and metabolome analysis. Furthermore, we provided direct evidence of how fumarate promoted the phyllosphere colonization of PAE-degrading bacteria and resulting reduction of PAE accumulation in plants. The novel findings highlight the crucial role of phyllosphere microbes in mediating pollutant accumulation within crops.