The MAT Locus Genes Play Different Roles in Sexual Reproduction and Pathogenesis in Fusarium graminearum

Qian Zheng,Zhongshou Wu,Rui Hou,Juanyu Juanyu,Jiwen Ma,Guanghui Wang,Chenfang Wang,Jin-Rong Xu,Zhang Zhang,Jae-Hyuk Yu

doi:10.1371/journal.pone.0066980

Qian Zheng, Zhongshou Wu + Show 8 more

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https://doi.org/10.1371/journal.pone.0066980

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Abstract

Sexual reproduction plays a critical role in the infection cycle of Fusarium graminearum because ascospores are the primary inoculum. As a homothallic ascomycete, F. graminearum contains both the MAT1-1 and MAT1-2-1 loci in the genome. To better understand their functions and regulations in sexual reproduction and pathogenesis, in this study we assayed the expression, interactions, and mutant phenotypes of individual MAT locus genes. Whereas the expression of MAT1-1-1 and MAT12-1 rapidly increased after perithecial induction and began to decline after 1 day post-perithecial induction (dpi), the expression of MAT1-1-2 and MAT1-1-3 peaked at 4 dpi. MAT1-1-2 and MAT1-1-3 had a similar expression profile and likely are controlled by a bidirectional promoter. Although none of the MAT locus genes were essential for perithecium formation, all of them were required for ascosporogenesis in self-crosses. In outcrosses, the mat11-1-2 and mat11-1-3 mutants were fertile but the mat1-1-1 and mat1-2-1 mutants displayed male- and female-specific defects, respectively. The mat1-2-1 mutant was reduced in FgSO expression and hyphal fusion. Mat1-1-2 interacted with all other MAT locus transcription factors, suggesting that they may form a protein complex during sexual reproduction. Mat1-1-1 also interacted with FgMcm1, which may play a role in controlling cell identity and sexual development. Interestingly, the mat1-1-1 and mat1-2-1 mutants were reduced in virulence in corn stalk rot assays although none of the MAT locus genes was important for wheat infection. The MAT1-1-1 and MAT1-2-1 genes may play a host-specific role in colonization of corn stalks.

Highlights

Fusarium graminearum is a causal agent of Fusarium head blight (FHB) or scab of wheat, barley, and other small grains worldwide [1,2]
In addition to the male- and femalespecific defects observed in the mat1-1-1 and mat1-2-1 deletion mutants, respectively, we found that MAT1-1-1 and MAT1-2-1 are important for colonization of corn stalks, suggesting that they play a host-specific role in pathogenesis
In aerial hyphae harvested before perithecial induction, the expression of MAT locus genes was not detectable or relatively low (Fig. 1B), suggesting that their expression was suppressed during vegetative growth

Summary

Introduction

Fusarium graminearum (teleomorph Gibberella zeae) is a causal agent of Fusarium head blight (FHB) or scab of wheat, barley, and other small grains worldwide [1,2]. This fungal pathogen overwinters on plant debris and produces ascospores in the spring to initiate infection of flowering tissues of wheat and other host plants. Sexual reproduction plays a critical role in the infection cycle of F. graminearum because ascospores are the primary inoculum [3]. Flowering wheat heads are susceptible to Fusarium infection from anthesis through the milk stages. Infested grains are often contaminated with these harmful mycotoxins [4]

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