The AGC Kinase SsAgc1 Regulates <italic toggle="yes">Sporisorium scitamineum</italic> Mating/Filamentation and Pathogenicity

ABSTRACT Sporisorium scitamineum is the fungal pathogen causing severe sugarcane smut disease that leads to massive economic losses globally. S. scitamineum invades host cane by dikaryotic hyphae, formed after sexual mating of two haploid sporidia of opposite mating type. Therefore, mating/filamenta...

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Autores principales: Yixu Wang, Yi Zhen Deng, Guobing Cui, Chengwei Huang, Bin Zhang, Changqing Chang, Zide Jiang, Lian-Hui Zhang
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Publicado: American Society for Microbiology 2019
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spelling oai:doaj.org-article:d0494195cfc9469eb8b43ebfd4f22fb42021-11-15T15:22:20ZThe AGC Kinase SsAgc1 Regulates <italic toggle="yes">Sporisorium scitamineum</italic> Mating/Filamentation and Pathogenicity10.1128/mSphere.00259-192379-5042https://doaj.org/article/d0494195cfc9469eb8b43ebfd4f22fb42019-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00259-19https://doaj.org/toc/2379-5042ABSTRACT Sporisorium scitamineum is the fungal pathogen causing severe sugarcane smut disease that leads to massive economic losses globally. S. scitamineum invades host cane by dikaryotic hyphae, formed after sexual mating of two haploid sporidia of opposite mating type. Therefore, mating/filamentation is critical for S. scitamineum pathogenicity, while its molecular mechanisms remain largely unknown. The AGC (cyclic AMP [cAMP]-dependent protein kinase 1 [protein kinase A {PKA}], cGMP-dependent protein kinase [PKG], and protein kinase C [PKC]) kinase family is a group of serine/threonine (Ser/Thr) protein kinases conserved among eukaryotic genomes, serving a variety of physiological functions, including cell growth, metabolism, differentiation, and cell death. In this study, we identified an AGC kinase, named SsAgc1 (for S. scitamineum Agc1), and characterized its function by reverse genetics. Our results showed that SsAgc1 is critical for S. scitamineum mating/filamentation and pathogenicity, and oxidative stress tolerance under some circumstances. Transcriptional profiling revealed that the SsAgc1 signaling pathway may control expression of the genes governing fungal mating/filamentation and tryptophan metabolism, especially for tryptophol production. We showed that tryptophan and tryptophol could at least partially restore ssagc1Δ mating/filamentation. Overall, our work revealed a signaling pathway mediated by AGC protein kinases to regulate fungal mating/filamentation, possibly through sensing and responding to tryptophol as signal molecules. IMPORTANCE The AGC signaling pathway represents a conserved distinct signaling pathway in regulation of fungal differentiation and virulence, while it has not been identified or characterized in the sugarcane smut fungus Sporisorium scitamineum. In this study, we identified a PAS domain-containing AGC kinase, SsAgc1, in S. scitamineum. Functional analysis revealed that SsAgc1 plays a regulatory role on the fungal dimorphic switch.Yixu WangYi Zhen DengGuobing CuiChengwei HuangBin ZhangChangqing ChangZide JiangLian-Hui ZhangAmerican Society for MicrobiologyarticleAGC kinaseSporisorium scitamineumcAMPfilamentous growthMicrobiologyQR1-502ENmSphere, Vol 4, Iss 3 (2019)
institution DOAJ
collection DOAJ
language EN
topic AGC kinase
Sporisorium scitamineum
cAMP
filamentous growth
Microbiology
QR1-502
spellingShingle AGC kinase
Sporisorium scitamineum
cAMP
filamentous growth
Microbiology
QR1-502
Yixu Wang
Yi Zhen Deng
Guobing Cui
Chengwei Huang
Bin Zhang
Changqing Chang
Zide Jiang
Lian-Hui Zhang
The AGC Kinase SsAgc1 Regulates <italic toggle="yes">Sporisorium scitamineum</italic> Mating/Filamentation and Pathogenicity
description ABSTRACT Sporisorium scitamineum is the fungal pathogen causing severe sugarcane smut disease that leads to massive economic losses globally. S. scitamineum invades host cane by dikaryotic hyphae, formed after sexual mating of two haploid sporidia of opposite mating type. Therefore, mating/filamentation is critical for S. scitamineum pathogenicity, while its molecular mechanisms remain largely unknown. The AGC (cyclic AMP [cAMP]-dependent protein kinase 1 [protein kinase A {PKA}], cGMP-dependent protein kinase [PKG], and protein kinase C [PKC]) kinase family is a group of serine/threonine (Ser/Thr) protein kinases conserved among eukaryotic genomes, serving a variety of physiological functions, including cell growth, metabolism, differentiation, and cell death. In this study, we identified an AGC kinase, named SsAgc1 (for S. scitamineum Agc1), and characterized its function by reverse genetics. Our results showed that SsAgc1 is critical for S. scitamineum mating/filamentation and pathogenicity, and oxidative stress tolerance under some circumstances. Transcriptional profiling revealed that the SsAgc1 signaling pathway may control expression of the genes governing fungal mating/filamentation and tryptophan metabolism, especially for tryptophol production. We showed that tryptophan and tryptophol could at least partially restore ssagc1Δ mating/filamentation. Overall, our work revealed a signaling pathway mediated by AGC protein kinases to regulate fungal mating/filamentation, possibly through sensing and responding to tryptophol as signal molecules. IMPORTANCE The AGC signaling pathway represents a conserved distinct signaling pathway in regulation of fungal differentiation and virulence, while it has not been identified or characterized in the sugarcane smut fungus Sporisorium scitamineum. In this study, we identified a PAS domain-containing AGC kinase, SsAgc1, in S. scitamineum. Functional analysis revealed that SsAgc1 plays a regulatory role on the fungal dimorphic switch.
format article
author Yixu Wang
Yi Zhen Deng
Guobing Cui
Chengwei Huang
Bin Zhang
Changqing Chang
Zide Jiang
Lian-Hui Zhang
author_facet Yixu Wang
Yi Zhen Deng
Guobing Cui
Chengwei Huang
Bin Zhang
Changqing Chang
Zide Jiang
Lian-Hui Zhang
author_sort Yixu Wang
title The AGC Kinase SsAgc1 Regulates <italic toggle="yes">Sporisorium scitamineum</italic> Mating/Filamentation and Pathogenicity
title_short The AGC Kinase SsAgc1 Regulates <italic toggle="yes">Sporisorium scitamineum</italic> Mating/Filamentation and Pathogenicity
title_full The AGC Kinase SsAgc1 Regulates <italic toggle="yes">Sporisorium scitamineum</italic> Mating/Filamentation and Pathogenicity
title_fullStr The AGC Kinase SsAgc1 Regulates <italic toggle="yes">Sporisorium scitamineum</italic> Mating/Filamentation and Pathogenicity
title_full_unstemmed The AGC Kinase SsAgc1 Regulates <italic toggle="yes">Sporisorium scitamineum</italic> Mating/Filamentation and Pathogenicity
title_sort agc kinase ssagc1 regulates <italic toggle="yes">sporisorium scitamineum</italic> mating/filamentation and pathogenicity
publisher American Society for Microbiology
publishDate 2019
url https://doaj.org/article/d0494195cfc9469eb8b43ebfd4f22fb4
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