The false smut pathogen Ustilaginoidea virens requires rice stamens for false smut ball formation

Abstract

Rice false smut has emerged as a serious grain disease in rice production worldwide. The disease is characterized by the transformation of individual rice florets into false smut balls, which is caused by the fungal pathogen Ustilaginoidea virens. To date, little is known about the host factors required for false smut ball formation by U. virens. In this study, we identified histological determinants for the formation of false smut balls by inoculating U. virens into rice floral mutants defective with respect to individual floral parts. The results showed that U. virens could form mature false smut balls in rice floral mutants with defective pistils, but failed to develop false smut balls in the superwoman mutant lacking stamens, identifying that U. virens requires rice stamens to complete its infection cycle. Comparative transcriptome analysis indicated a list of candidate host genes that may facilitate nutrient acquisition by U. virens from the rice stamens, such as SWEET11, SWEET14 and SUT5, and genes involved in the biosynthesis of trehalose and raffinose family sugars. These data pinpoint rice stamens as the key target organ of U. virens infection and provide a valuable starting point for dissecting the molecular mechanism of false smut ball formation. Received

Comprehensive identification of lysine 2‐hydroxyisobutyrylated proteins in Ustilaginoidea virens reveals the involvement of lysine 2‐hydroxyisobutyrylation in fungal virulence

“…Rice false smut disease, caused by the pathogenic ascomycete fungus Ustilaginoidea virens (teleomorph: Villosiclava virens ), is a devastating grain disease in the majority of rice ( Oryza sativa )‐growing areas of the world (Zhang et al, 2014; Qiu et al, 2019; Sun et al, 2020). In floral organs, the pathogen first attacks the filaments, preventing pollen from maturing and blocking ovary fertilization, and then it invades the stigma and style to simulate fertilization, thereby hijacking nutrients to form rice false smut balls (Song et al, 2016; Fan et al, 2020). This disease not only causes yield loss, but also threatens human and animal health due to the production of cyclopeptide mycotoxins (Koiso et al, 1994; Miyazaki et al, 2009; Hu et al, 2019).…”

Mapping quantitative trait loci for disease resistance to false smut of rice

“…U. virens initially infects rice florets through stamen filaments and thus prevents the production of mature pollen grains and pollination. The pathogen subsequently invades the stigmas and styles, occasionally the ovaries (Tang et al 2013;Song et al 2016;Fan et al 2020). Interestingly, the pathogen might hijack rice nutrient supply system to benefit the formation of false smut balls by simulating ovule fertilization (Fan et al 2015;Song et al 2016).…”

Extraction and purification of ustiloxin A from rice false smut balls by a combination of macroporous resin and high-speed countercurrent chromatography

“…Rice false smut is a plant disease caused by the fungal pathogen Ustilaginoidea virens Takahashi, which is now rapidly emerging in rice cultivation worldwide (Qiu et al 2019). The most noticeable symptom of rice false smut is the false smut balls that form on rice florets as orange or green bulbs (Fan et al 2020). In addition to the yield loss caused by rice false smut, U. virens produces secondary metabolites called mycotoxins.…”