MAT1-1-3, a Mating Type Gene in the Villosiclava virens, Is Required for Fruiting Bodies and Sclerotia Formation, Asexual Development and Pathogenicity.

Wende Liu,Yongfeng Liu,Zhongqiang Qi,Rongsheng Zhang,Zhiyi Chen,Xiayan Pan,Mina Yu,Yan Du,Mingli Yong,Huijuan Cao,Tianqiao Song,Junjie Yu,Xiaole Yin

doi:10.3389/fmicb.2020.01337

Abstract

Villosiclava virens is the prevalent causative pathogen of rice false smut, a destructive rice disease. Mating-type genes play a vital role in the evolution of mating systems in fungi. Some fungi have lost MAT1-1-3, one of the mating-type genes, during evolution, whereas others still retain MAT1-1-3. However, how MAT1-1-3 regulates the sexual development of heterothallic V. virens remains unknown. Here, we generated the MAT1-1-3 mutants, which exhibited defects in vegetative growth, stress response, pathogenicity, sclerotia formation and fruiting body maturation. An artificial outcrossing inoculation assay showed that the Δmat1-1-3 mutant was unable to produce sclerotia. Unexpectedly, the Δmat1-1-3 mutant could form immature fruiting bodies without mating on potato sucrose agar medium (PSA) compared with the wild-type strain, most likely by activating the truncated MAT1-2-1 transcription to regulate the sexual development. Moreover, RNA-seq data showed that knockout of MAT1-1-3 results in misregulation of a subset of genes involved in sexual development, MAPK signaling, cell wall integrity, autophagy, epigenetic modification, and transcriptional regulation. Collectively, this study reveals that MAT1-1-3 is required for asexual and sexual development, and pathogenicity of V. virens, thereby provides new insights into the function of mating-type genes in the fungi life cycle and infection process.

Highlights

Villosiclava virens (Anamorph, Ustilaginoidea virens) is a plant pathogen that causes rice false smut (RFS), which results in substantial rice yield losses worldwide (Brooks et al, 2010; Ladhalakshmi et al, 2012; Jecmen and Tebeest, 2015; Fan et al, 2016)
Genetic recombination occurs during sexual reproduction when two compatible strains mate, thereby playing a vital role in expanding V. virens genetic diversity (Sun et al, 2013; Wang et al, 2014)
Our results demonstrated that the growth inhibition rate of mycelial growth of mutant displays significant difference, the mat1-1-3 mutant exhibited increases in the tolerance to NaCl, Sorbitol, H2O2, congo red (CR) and calcofluor white (CFW), but more sensitive to sodium dodecyl sulfate (SDS) compared with WT and complemented strain C mat1-1-3#16 (Figure 3)

Summary

Introduction

Villosiclava virens (Anamorph, Ustilaginoidea virens) is a plant pathogen that causes rice false smut (RFS), which results in substantial rice yield losses worldwide (Brooks et al, 2010; Ladhalakshmi et al, 2012; Jecmen and Tebeest, 2015; Fan et al, 2016). During the pathogen’s sexual life cycle, V. virens can produce ascospores by sexual reproduction (Zhang et al, 2014; Yong et al, 2018), which, through invasion of rice spikelets, are considered to be one of the primary infection sources of rice false smut (RFS) (Ikegami, 1960; Wang, 1995). Genetic recombination occurs during sexual reproduction when two compatible strains mate, thereby playing a vital role in expanding V. virens genetic diversity (Sun et al, 2013; Wang et al, 2014). The sexual reproduction plays an important role in the prevalence of RFS and genetic diversity in V. virens

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Results

Conclusion