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The AGC Kinase SsAgc1 Regulates Sporisorium scitamineum 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/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 ssagc1? 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.

SUBMITTER: Wang Y

PROVIDER: S-EPMC6541736 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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The AGC Kinase SsAgc1 Regulates Sporisorium scitamineum Mating/Filamentation and Pathogenicity.

Wang Yixu Y Deng Yi Zhen YZ Cui Guobing G Huang Chengwei C Zhang Bin B Chang Changqing C Jiang Zide Z Zhang Lian-Hui LH

mSphere 20190529 3

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</u ...[more]

PMID: 31142621

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Project description:Sugarcane smut, caused by the basidiomycetous fungus Sporisorium scitamineum, is a global fungal disease resulting in substantial economic losses. Our previous research has highlighted the significant role of reactive oxide species (ROS) in the sexual reproduction of S. scitamineum, yet the underlying mechanisms remain unclear. In this study, we identified the cytochrome c-peroxidase encoding gene, SsCCP1, as crucial for oxidative stress resistance. We further found that absence of SsCcp1 leads to defects in mating/filamentation and disrupts intracellular ROS homeostasis. However, restoration of mating/filamentation of SsCCP1 deletion mutants was partially achieved with exogenous antioxidants (vitamin C or vitamin E). Notably, transcription of the pheromone response factor SsPRF1, pivotal for mating/filamentation of S. scitamineum, is significantly reduced in the SsCCP1 deletion mutants or under exogenous hydrogen peroxide (H2O2) conditions. Nevertheless, the addition of exogenous vitamin C for 60 min significantly up-regulated the SsPRF1 gene in the SsCCP1 deletion mutants. Moreover, the constitutive expression of SsPRF1 essentially reinstated the mating/filamentation of SsCCP1 deletion mutants, suggesting that SsCcp1 mediates the transcriptional activity of SsPRF1 by maintaining ROS homeostasis to regulate the mating/filamentation of S. scitamineum. Further investigations revealed that SsCcp1 is necessary for ROS detoxification and full pathogenicity in planta. Overall, this study not only unveils the importance of SsCcp1 in S. scitamineum mating/filamentation, ROS detoxification, and virulence but also provides insights into the role of SsCcp1-regulated ROS homeostasis in sexual reproduction of S. scitamineum. IMPORTANCE Reactive oxygen species play an important role in pathogen-plant interactions. In fungi, cytochrome c-peroxidase maintains intracellular ROS homeostasis by utilizing H2O2 as an electron acceptor to oxidize ferrocytochrome c, thereby contributing to disease pathogenesis. In this study, our investigation reveals that the cytochrome c-peroxidase encoding gene, SsCCP1, not only plays a key role in resisting H2O2 toxicity but is also essential for the mating/filamentation and pathogenicity of S. scitamineum. We further uncover that SsCcp1 mediates the expression of SsPrf1 by maintaining intracellular ROS homeostasis to regulate S. scitamineum mating/filamentation. Our findings provide novel insights into how cytochrome c-peroxidase regulates sexual reproduction in phytopathogenic fungi, presenting a theoretical foundation for designing new disease control strategies.

Dataset Information

The AGC Kinase SsAgc1 Regulates Sporisorium scitamineum Mating/Filamentation and Pathogenicity.

Publications

The AGC Kinase SsAgc1 Regulates <i>Sporisorium scitamineum</i> Mating/Filamentation and Pathogenicity.

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