Current understanding on Villosiclava virens, a unique flower‐infecting fungus causing rice false smut disease

Abstract

Villosiclava virens (Vv) is an ascomycete fungal pathogen that causes false smut disease in rice. Recent reports have revealed some interesting aspects of the enigmatic pathogen to address the question of why it specifically infects rice flowers and converts a grain into a false smut ball. Comparative and functional genomics have suggested specific adaptation of Vv in the colonization of rice flowers. Anatomical studies have disclosed that Vv specifically infects rice stamen filaments before heading and intercepts seed formation. In addition, Vv can occupy the whole inner space of a spikelet embracing all floral organs and activate the rice grain-filling network, presumably for nutrient acquisition to support the development of the false smut ball. This profile provides a general overview of the rice false smut pathogen, and summarizes advances in the Vv life cycle, genomics and genetics, and the molecular Vv-rice interaction. Current understandings of the Vv-rice pathosystem indicate that it is a unique and interesting system which can enrich the study of plant-pathogen interactions. Taxonomy: Ustilaginoidea virens is the anamorph form of the pathogen (Kingdom Fungi; Phylum Ascomycota; Class Ascomycetes; Subclass Incertae sedis; Order Incertae sedis; Family Incertae sedis; Genus Ustilaginoidea). The teleomorph form is Villosiclava virens (Kingdom Fungi; Phylum Ascomycota; Class Ascomycetes; Subclass Sordariomycetes; Order Hypocreales; Family Clavicipitaceae; Genus Villosiclava). Disease symptoms: The only visible symptom is the replacement of rice grains by ball-shaped fungal mycelia, namely false smut balls. When maturing, the false smut ball is covered with powdery chlamydospores, and the colour changes to yellowish, yellowish orange, green, olive green and, finally, to greenish black. Sclerotia are often formed on the false smut balls in autumn. Identification and detection: Vv conidia are round to elliptical, measuring 3-5 μm in diameter. Chlamydospores are ornamented with prominent irregularly curved spines, which are 200-500 nm in length. The sclerotia are black, horseshoe-shaped and irregular oblong or flat, ranging from 2 to 20 mm. Nested polymerase chain reaction (PCR) and quantitative PCR have been developed to specifically detect Vv presence in rice tissues and other biotic and abiotic samples in fields. Host range: Rice is the primary host for Vv. Natural infection by Vv has been found on several paddy field weeds, including Digitaria marginata, Panicum trypheron, Echinochloa crusgalli and Imperata cylindrica. However, the occurrence of infection in these potential alternative hosts is very rare. Life cycle: Vv infects rice spikelets at the late rice booting stage, and produces false smut balls covered with dark-green chlamydospores. Occasionally, sclerotia form on the surface of false smut balls in late autumn when the temperature fluctuates greatly between day and night. Both chlamydospores and sclerotia may serve as primary infection sources. Rainfall at the rice booting stage is a major environme...

The Contents of Ustiloxins A and B along with Their Distribution in Rice False Smut Balls

“…Rice false smut has been one of the most destructive rice ( Oryza sativa L.) fungal diseases in many rice cultivation areas worldwide over the past few years [ 1 ]. It is caused by the ascomycetous pathogen Villosiclava virens (Nakata) Tanaka & Tanaka (anamorph: Ustilaginoidea virens Takahashi) [ 2 ].…”

A core effector UV_1261 promotes Ustilaginoidea virens infection via spatiotemporally suppressing plant defense

“…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). Therefore, the expression pattern of UV_1261 suggested its role in both infection stages.…”

“…For example, Claviceps purpurea causes ergot disease in rye and Gibberella zeae causes Fusarium head blight in wheat (Ngugi and Scherm 2006). In recent years, 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 not only leads to yield loss, but also contaminates grains and straws with mycotoxins that are poisonous to both human and animals (Koiso et al 1994;Nakamura et al 1994).…”

Ustiloxin G, a New Cyclopeptide Mycotoxin from Rice False Smut Balls

“…The importance of this disease has risen recently, with the change of its status from “minor” to “major” causing concern in almost all rice cultivation regions across the globe [ 3 ]. In particular, this disease has been estimated to occur in one-third of the rice cultivation areas in China [ 4 ].…”