Abstract

False smut is a destructive grain disease of rice worldwide, characterized by false smut balls formed in rice flowers. Here we identified a small secreted protein UV_1261 contributing to virulence of Ustilaginoidea virens, the causal agent of this disease. The sequence of UV_1261 was highly conserved among isolates of U. virens and absent in other fungi. UV_1261 encodes a protein targeted to plant chloroplasts. Its expression exhibited a bimodal pattern during pathogenesis. Ectopic expression of UV_1261 in Nicotiana benthamiana and Arabidopsis led to suppression of flg22-induced ROS burst, callose deposition, and expression of defense-related genes, as well as enhanced susceptibility to powdery mildew in Arabidopsis. Down-regulation of UV_1261 via exogenous siRNA treatment resulted in reduced number of false smut balls. Consistently, stably knocking-down UV_1261 caused less number of false smut balls associated with higher expression of defense-related genes in rice flower. Taken together, our data demonstrate that UV_1261 is a core effector of U. virens essential for virulence and suppressing defense in rice flower, and thus may serve as a potential molecular target for controlling rice false smut disease.

Highlights

  • Flower is a nutrient-rich sink organ, attracting habitation of a large number of microorganisms

  • We exploited a compatible U. virens-rice interaction established in our previous studies with the isolate PJ52 and the rice accession Pujiang 6 (Fan et al 2015; Huang et al 2016)

  • Compared to its expression in potato-sucrose broth (PSB) medium, UV_1261 was up-regulated at 1–3 days post inoculation, and slightly decreased from 5 to 9 dpi. It was up-regulated again at 11 dpi, and reached to the highest expression at 13 dpi, forming a bimodal pattern (Fig. 1). This bimodal pattern is coincident with the two infection stages of U. virens (Fan et al 2016), during which no obvious symptoms were detected from 1 to 7 dpi; whereas white fungal mass were seen in inner space of a spikelet at 9 dpi and the fungal mass increased to protrude out of the spikelet at 15 dpi (Fan et al 2015)

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Summary

Introduction

Flower is a nutrient-rich sink organ, attracting habitation of a large number of microorganisms. Flower-infecting fungi have caused diseases in many economically important crops. Claviceps purpurea causes ergot disease in rye and Gibberella zeae causes Fusarium head blight in wheat (Ngugi and Scherm 2006). Rice false smut (RFS) disease, caused by the flower-infecting pathogen Ustilaginoidea virens, has emerged as a serious grain disease worldwide (Fan et al 2016). Occurrence of RFS disease leads to yield loss, and contaminates grains and straws with mycotoxins that are poisonous to both human and animals (Koiso et al 1994; Nakamura et al 1994). Our understanding on the pathogenesis of this disease is very limited

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