Antibacterial Effect and Mechanism of Chelerythrine on Xanthomonas oryzae pv. oryzae

<i>Xanthomonas oryzae</i> pv. <i>oryzae</i> (<i>Xoo</i>) is a biotrophic bacterial pathogen, which causes devastating bacterial blight disease worldwide. In this study, we thoroughly investigated the antimicrobial effect of the plant-derived extract chelerythrine against <i>Xanthomonas oryzae</i> pv. <i>oryzae</i> (<i>Xoo</i>) and elucidated its mechanism. Chelerythrine is a quaternary ammonium alkaloid with a 2,3,7,8-tetrasubstituted phenanthridine structure, extracted from plants, such as the whole plant of Chelidonium majus, and the roots, stems, and leaves of Macleaya cordata. We found that chelerythrine significantly inhibited the growth of <i>Xoo</i> at a concentration of 1.25 μg/mL. Further experiments revealed that chelerythrine interfered with the division and reproduction of the bacterium, leading to its filamentous growth. Additionally, it increased the permeability of <i>Xoo</i> cell membranes and effectively decreased the pathogenicity of <i>Xoo</i>, including the inhibition of extracellular polysaccharide production, cellulase secretion, and biofilm formation. Chelerythrine induced the accumulation of reactive oxygen species in the bacterium, triggering oxidative stress. The result showed that chelerythrine inhibited the formation of the Z-ring of <i>Xoo</i>, interfered with the synthesis of pyrimidine and purine nucleotides, inhibited DNA damage repair, and inhibited the formation of peptidoglycan and lipid-like A, thus interfering with cell membrane permeability, inhibiting carbohydrate metabolism and phosphorylation of sugars, reducing pathogenicity, and ultimately inhibiting bacterial growth and leading to the destruction or lysis of bacterial cells. Altogether, our results suggest that the antimicrobial effect of chelerythrine on <i>Xoo</i> exhibits multi-target properties. Additionally, its effective inhibitory concentration is low. These findings provide a crucial theoretical basis and guidance for the development of novel and efficient plant-derived antimicrobial compounds.