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Histidine Kinase Sln1 and cAMP/PKA Signaling Pathways Antagonistically Regulate Sporisorium scitamineum Mating and Virulence via Transcription Factor Prf1.

ABSTRACT: Many prokaryotes and eukaryotes utilize two-component signaling pathways to counter environmental stress and regulate virulence genes associated with infection. In this study, we identified and characterized a conserved histidine kinase (SsSln1), which is the sensor of the two-component system of Sln1-Ypd1-Ssk1 in Sporisorium scitamineum. SsSln1 null mutant exhibited enhanced mating and virulence capabilities in S. scitamineum, which is opposite to what has been reported in Candida albicans. Further investigations revealed that the deletion of SsSLN1 enhanced SsHog1 phosphorylation and nuclear localization and thus promoted S. scitamineum mating. Interestingly, SsSln1 and cAMP/PKA signaling pathways antagonistically regulated the transcription of pheromone-responsive transcription factor SsPrf1, for regulating S. scitamineum mating and virulence. In short, the study depicts a novel mechanism in which the cross-talk between SsSln1 and cAMP/PKA pathways antagonistically regulates mating and virulence by balancing the transcription of the SsPRF1 gene in S. scitamineum.

SUBMITTER: Cai E

PROVIDER: S-EPMC8397173 | biostudies-literature | 2021 Jul

REPOSITORIES: biostudies-literature

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Histidine Kinase Sln1 and cAMP/PKA Signaling Pathways Antagonistically Regulate Sporisorium scitamineum Mating and Virulence via Transcription Factor Prf1.

Cai Enping E Sun Shuquan S Deng Yizhen Y Huang Peishen P Sun Xian X Wang Yuting Y Chang Changqing C Jiang Zide Z

Journal of fungi (Basel, Switzerland) 20210728 8

Many prokaryotes and eukaryotes utilize two-component signaling pathways to counter environmental stress and regulate virulence genes associated with infection. In this study, we identified and characterized a conserved histidine kinase (SsSln1), which is the sensor of the two-component system of Sln1-Ypd1-Ssk1 in Sporisorium scitamineum. SsSln1 null mutant exhibited enhanced mating and virulence capabilities in S. scitamineum, which is opposite to what has been reported in ...[more]

PMID: 34436149

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Project description: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.

Project description:Sugarcane is an important sugar crop and energy crop worldwide. Sugarcane smut caused by Sporisorium scitamineum is a serious fungal disease that occurs worldwide, seriously affecting the yield and quality of sugarcane. It is essential to reveal the molecular pathogenesis of S. scitamineum to explore a new control strategy of sugarcane smut. Based on transcriptome sequencing data of two S. scitamineum strains Ss16 and Ss47, each with a different pathogenicity, our laboratory screened out the SsCI80130 gene predicted to encode squalene monooxygenase. In this study, we obtained the knockout mutants (ΔSs80130+ and ΔSs80130-) and complementary mutants (COM80130+ and COM80130-) of this gene by the polyethylene glycol-mediated (PEG-mediated) protoplast transformation technology, and then performed a functional analysis of the gene. The results showed that the deletion of the SsCI80130 gene resulted in the increased content of squalene (substrate for squalene monooxygenase) and decreased content of ergosterol (the final product of the ergosterol synthesis pathway) in S. scitamineum. Meanwhile, the sporidial growth rate of the knockout mutants was significantly slower than that of the wild type and complementary mutants; under cell-wall stress or oxidative stress, the growth of the knockout mutants was significantly inhibited. In addition, the sexual mating ability and pathogenicity of knockout mutants were significantly weakened, while the sexual mating ability could be restored by adding exogenous small-molecular signal substance cAMP (cyclic adenosine monophosphate) or tryptophol. It is speculated that the SsCI80130 gene was involved in the ergosterol biosynthesis in S. scitamineum and played an important role in the sporidial growth, stress response to different abiotic stresses (including cell wall stress and oxidative stress), sexual mating/filamentation and pathogenicity. Moreover, the SsCI80130 gene may affect the sexual mating and pathogenicity of S. scitamineum by regulating the ergosterol synthesis and the synthesis of the small-molecular signal substance cAMP or tryptophol required for sexual mating. This study reveals for the first time that the gene encoding squalene monooxygenase is involved in regulating the sexual mating and pathogenicity of S. scitamineum, providing a basis for the molecular pathogenic mechanism of S. scitamineum.

Dataset Information

Histidine Kinase Sln1 and cAMP/PKA Signaling Pathways Antagonistically Regulate Sporisorium scitamineum Mating and Virulence via Transcription Factor Prf1.

Publications

Histidine Kinase Sln1 and cAMP/PKA Signaling Pathways Antagonistically Regulate <i>Sporisorium scitamineum</i> Mating and Virulence via Transcription Factor Prf1.

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