Abstract

Ustilaginoidea virens is a biotrophic fungal pathogen specifically colonizing rice floral organ and causes false smut disease of rice. This disease has emerged as a serious problem that hinders the application of high-yield rice cultivars, by reducing grain yield and quality as well as introducing mycotoxins. However, the pathogenic mechanisms of U. virens are still enigmatic. Here we demonstrate that U. virens employs a secreted protein UvCBP1 to manipulate plant immunity. In planta expression of UvCBP1 led to compromised chitin-induced defense responses in Arabidopsis and rice, including burst of reactive oxygen species (ROS), callose deposition, and expression of defense-related genes. In vitro-purified UvCBP1 protein competes with rice chitin receptor OsCEBiP to bind to free chitin, thus impairing chitin-triggered rice immunity. Moreover, UvCBP1 could significantly promote infection of U. virens in rice flowers. Our results uncover a mechanism of a floral fungus suppressing plant immunity and pinpoint a universal role of chitin-battlefield during plant–fungi interactions.

Highlights

  • As a staple food, rice feeds over half of the population of the world

  • The wild-type YTK12 cannot utilize raffinose due to its deficiency in invertase secretion, whereas the YTK12 strain transformed with the UvCBP1SP-SUC2 could grow well on YPRAA medium supplemented with raffinose as the sole carbon source

  • Future work to knockout or knockdown UvCBP1 in U. virens may reveal whether it is required for pathogenicity, we demonstrate that its in planta expression in rice spikelets enhances U. virens colonization (Figures 7A,B), supporting its role as a potential virulence factor

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Summary

Introduction

Rice feeds over half of the population of the world. Rice diseases have caused significant yield losses every year, being urgent problems to ensure food security (Liu et al, 2014). U. virens infects rice flowers and develops into large mycelial colonies covered with massive chlamydospores, called false smut balls (Tang et al, 2013; Fan et al, 2016). Formation of false smut balls leads to considerable yield losses and generates a diversity of mycotoxins poisonous to humans and animals (Zhou et al, 2012; Dhua et al, 2015). Resistance genes against U. virens have not been cloned in rice or its relatives, except

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