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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American Society for Microbiology
2019
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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) |
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AGC kinase Sporisorium scitamineum cAMP filamentous growth Microbiology QR1-502 |
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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 |
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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 |
work_keys_str_mv |
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