The glycogen synthase kinase MoGsk1, regulated by Mps1 MAP kinase, is required for fungal development and pathogenicity in Magnaporthe oryzae

Tengsheng Zhou,Shiqin Zheng,Liqiong Chen,Zonghua Wang,Nicholas J Talbot,Xiaohan Zhu,Yasin F Dagdas,Zachary Cartwright

doi:10.1038/s41598-017-01006-w

Tengsheng Zhou, Shiqin Zheng + Show 6 more

Open Access

https://doi.org/10.1038/s41598-017-01006-w

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Abstract

Magnaporthe oryzae, the causal agent of blast disease, is one of the most destructive plant pathogens, causing significant yield losses on staple crops such as rice and wheat. The fungus infects plants with a specialized cell called an appressorium, whose development is tightly regulated by MAPK signaling pathways following the activation of upstream sensors in response to environmental stimuli. Here, we show the expression of the Glycogen synthase kinase 3 (GSK3) MoGSK1 in M. oryzae is regulated by Mps1 MAP kinase, particularly under the stressed conditions. Thus, MoGSK1 is functionally characterized in this study. MoGsk1 is functionally homologues to the Saccharomyces cerevisiae GSK3 homolog MCK1. Gene replacement of MoGSK1 caused significant delay in mycelial growth, complete loss of conidiation and inability to penetrate the host surface by mycelia-formed appressorium-like structures, consequently resulting in loss of pathogenicity. However, the developmental and pathogenic defects of Δmogsk1 are recovered via the heterologous expression of Fusarium graminearum GSK3 homolog gene FGK3, whose coding products also shows the similar cytoplasmic localization as MoGsk1 does in M. oryzae. By contrast, overexpression of MoGSK1 produced deformed appressoria in M. oryzae. In summary, our results suggest that MoGsk1, as a highly conservative signal modulator, dictates growth, conidiation and pathogenicity of M. oryzae.

Highlights

Perception of cues on leaf surface is the key to initiation of cellular responses mediating appressorium development
In an initial screen for possible downstream cytoplasmic targets of the Mps[1] MAP kinase pathway in M. oryzae, we found the hydrophobin gene MPG1 and an uncharacterized glycogen synthase kinase 3 (GSK3) homolog MoGSK1 were differentially expressed in the absence of MPS1 and in response to environmental stresses
We studied the functions of the Glycogen synthase kinase 3 (GSK3) homolog in M. oryzae (MoGsk1) transcriptionally regulated by the MPS1 MAPK pathway and revealed its critical role in fungal development and plant infection

Summary

Introduction

Perception of cues on leaf surface is the key to initiation of cellular responses mediating appressorium development. In an initial screen for possible downstream cytoplasmic targets of the Mps[1] MAP kinase pathway in M. oryzae, we found the hydrophobin gene MPG1 and an uncharacterized glycogen synthase kinase 3 (GSK3) homolog MoGSK1 were differentially expressed in the absence of MPS1 and in response to environmental stresses. We studied the functions of the GSK3 homolog in M. oryzae (MoGsk1) transcriptionally regulated by the MPS1 MAPK pathway and revealed its critical role in fungal development and plant infection. The complementation by the Fusarium gramienearum homolog FGK3 fully restores the growth and pathogenicity of Δmogsk[1], and the gene product shows the same cytosolic localization as MoGsk[1] This indicates that the two GSK3 homologs in M. oryzae and F. graminearum shares highly conserved functions. Our results proves that MoGsk[1] is a central signal regulator involved in the stress-responsive mechanism and controls multiple aspects of development in M. oryzae, from growth, asexual production to pathogenesis

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