The rare sugar d-allose acts as a triggering molecule of rice defence via ROS generation

Akihito Kano,Akihide Yoshihara,Yoko Nishizawa,Kazuya Akimitsu,Toshiaki Ohara,Ken Izumori,Kazuya Ichimura,Keiji Tanaka,Kenji Gomi,Yasuomi Tada,Yutaka Ishida,Takeo Ohkouchi,Kouhei Ohtani,Takeshi Fukumoto,Shigeyuki Tajima

doi:10.1093/jxb/ert282

Abstract

Only d-allose, among various rare monosaccharides tested, induced resistance to Xanthomonas oryzae pv. oryzae in susceptible rice leaves with defence responses: reactive oxygen species, lesion mimic formation, and PR-protein gene expression. These responses were suppressed by ascorbic acid or diphenylene iodonium. Transgenic rice plants overexpressing OsrbohC, encoding NADPH oxidase, were enhanced in sensitivity to d-allose. d-Allose-mediated defence responses were suppressed by the presence of a hexokinase inhibitor. 6-Deoxy-d-allose, a structural derivative of d-allose unable to be phosphorylated, did not confer resistance. Transgenic rice plants expressing Escherichia coli AlsK encoding d-allose kinase to increase d-allose 6-phosphate synthesis were more sensitive to d-allose, but E. coli AlsI encoding d-allose 6-phosphate isomerase expression to decrease d-allose 6-phosphate reduced sensitivity. A d-glucose 6-phosphate dehydrogenase-defective mutant was also less sensitive, and OsG6PDH1 complementation restored full sensitivity. These results reveal that a monosaccharide, d-allose, induces rice resistance to X. oryzae pv. oryzae by activating NADPH oxidase through the activity of d-glucose 6-phosphate dehydrogenase, initiated by hexokinase-mediated conversion of d-allose to d-allose 6-phosphate, and treatment with d-allose might prove to be useful for reducing disease development in rice.

Highlights

Rare sugars are a group of ~50 monosaccharides that are present in very low amounts in the natural world (Izumori, 2002, 2006)
A d-glucose 6-phosphate dehydrogenase-defective mutant was less sensitive, and OsG6PDH1 complementation restored full sensitivity. These results reveal that a monosaccharide, d-allose, induces rice resistance to X. oryzae pv. oryzae by activating NADPH oxidase through the activity of d-glucose 6-phosphate dehydrogenase, initiated by hexokinase-mediated conversion of d-allose to d-allose 6-phosphate, and treatment with d-allose might prove to be useful for reducing disease development in rice
Since the lesion mimic after a hypersensitive response is often induced by production of ROS and is associated with induction of disease resistance to Xanthomonas oryzae pv. oryzae (Xoo) in rice (Yin et al, 2000; Ono et al, 2001; Torres et al, 2005), hydrogen peroxide (H2O2) production was monitored as an indicator of ROS generation by staining leaf tissues with DAB after the d-allose treatment (Fig. 1E)

Summary

Introduction

Rare sugars are a group of ~50 monosaccharides that are present in very low amounts in the natural world (Izumori, 2002, 2006). Biological functions and metabolic pathways of one of these rare sugars, d-allose, for several organisms have been reported. D-allose can have an immunosuppressive effect (Hossain et al, 2000). A protective effect against liver damage (Hossain et al, 2003). It can inhibit cancer cell proliferation and production of reactive oxygen species (ROS) in neutrophils (Murata et al, 2003; Sui et al, 2005).

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