Glucose 6-phosphate isomerase (Pgi) is required for extracellular polysaccharide biosynthesis, DSF signals production and full virulence of Xanthomonas oryzae pv. oryzicola in rice

Abstract

Xanthomonas oryzae pv. oryzicola (Xoc), the causal agent of bacterial leaf streak (BLS), recruits five carbohydrate catabolic pathways (glycolysis, ED, PPP, gluconeogenesis and TCA cycle) to acquire nutrients from host rice for parasitism and pathopoiesis. Glucose 6-phosphate isomerase (Pgi), which reversibly converts glucose 6-phosphate to fructose 6-phosphate, plays an important role in glycolysis and gluconeogenesis. In this study, we found that Pgi was essential for the pathogenicity of Xoc in rice. The mutagenesis in pgi caused the pathogen unable to effectively utilize fructose, sucrose, mannose and pyruvate for growth, but did not affect bacterial growth when glucose or galactose used as the sole carbon source. The expression of hrpX and hrpG was repressed and the transcription of hrpE, hpa3 and hrcU were enhanced when pgi or clp (encoding cAMP-regulatory protein) was mutated. Intriguingly, the mutation in pgi resulted in the transcription alteration of key genes, rpfF, rpfC, rpfG and clp, in the quorum-sensing (QS) signaling pathway mediated by diffusible signal factor (DSF) signals and significantly reduced DSF signals production compared with the wild-type. Additionally, the pgi deletion not only impaired bacterial growth and virulence in rice, but also reduced bacterial extracellular polysaccharide (EPS) biosynthesis and cell motility. The lost properties mentioned above in RΔpgi were completely restored to the wild-type levels by the presence of pgi in trans. Taken together, these findings exhibited functional roles of Pgi coordinating with the hrp system and the QS system mediated by DSF signals in carbon metabolic pathways.