Abstract
Fructose-bisphophate aldolase (FbaB), is an enzyme in glycolysis and gluconeogenesis in living organisms. The mutagenesis in a unique fbaB gene of Xanthomonas oryzae pv. oryzicola, the causal agent of rice bacterial leaf streak, led the pathogen not only unable to use pyruvate and malate for growth and delayed its growth when fructose was used as the sole carbon source, but also reduced extracellular polysaccharide (EPS) production and impaired bacterial virulence and growth in rice. Intriguingly, the fbaB promoter contains an imperfect PIP-box (plant-inducible promoter) (TTCGT-N9-TTCGT). The expression of fbaB was negatively regulated by a key hrp regulatory HrpG and HrpX cascade. Base substitution in the PIP-box altered the regulation of fbaB with the cascade. Furthermore, the expression of fbaB in X. oryzae pv. oryzicola RS105 strain was inducible in planta rather than in a nutrient-rich medium. Except other hrp-hrc-hpa genes, the expression of hrpG and hrpX was repressed and the transcripts of hrcC, hrpE and hpa3 were enhanced when fbaB was deleted. The mutation in hrcC, hrpE or hpa3 reduced the ability of the pathogen to acquire pyruvate and malate. In addition, bacterial virulence and growth in planta and EPS production in RΔfbaB mutant were completely restored to the wild-type level by the presence of fbaB in trans. This is the first report to demonstrate that carbohydrates, assimilated by X. oryzae pv. oryzicola, play critical roles in coordinating hrp gene expression through a yet unknown regulator.
Highlights
Carbohydrate nutrient acquisition is essential for bacterial pathogen growth to establish successful infections in host plants [1,2,3]
In Xanthomonas, ED, in conjunction with tricarboxylic acid (TCA), has been confirmed to be the predominant pathway for glucose catabolism, and a small portion (8 to 16%) of substrate glucose is routed into phosphate pathway (PPP) [5], whereas the EMP pathway of glycolysis does not play a significant role in glucose catabolism, since Xanthomonas species, including rice bacterial leaf streak X. oryzae pv. oryzicola, lack an essential phosphofructokinase activity which converts fructose 6-phosphate to fructose-1,6-bisphosphate [5,6,7]
Results fbaB is required for full virulence and growth of X. oryzae pv. oryzicola in planta The discovery of the fbaB gene as a virulence factor came from work aimed at the identification of genes involved in virulence alteration of X. oryzae pv. oryzicola RS105 strain in rice
Summary
Carbohydrate nutrient acquisition is essential for bacterial pathogen growth to establish successful infections in host plants [1,2,3]. As in other living organisms, plant pathogenic bacteria carry out the catabolic process via the Emden-Meyerhof-Parnas (EMP) pathway of glycolysis, Entner–Doudoroff (ED), pentose phosphate pathway (PPP) and terminal oxidation mediated by the tricarboxylic acid (TCA) cycle to break down hexoses, like glucose, outside of their cells for energy and carbon molecules. Vesicatoria [12] show that xanthomonads possess essential genes for the EMP pathway of glycolysis, ED, PPP, gluconeogenesis and TCA cycle. Great interests have been focused on whether or not and how the carbon metabolic pathways are involved in the virulence of plant pathogenic bacteria. The phosphoenolpyruvate synthase gene (ppsA), converting pyruvate to phosphoenolpyruvate, is essential for gluconeogenesis, in planta growth, and full virulence of X. campestris pv.
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