Cytochrome c -peroxidase modulates ROS homeostasis to regulate the sexual mating of Sporisorium scitamineum
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 underly...
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Published in | Microbiology spectrum Vol. 11; no. 6; p. e0205723 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
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United States
American Society for Microbiology
12.12.2023
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Abstract | 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, Ss
CCP1
, 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 Ss
CCP1
deletion mutants or under exogenous hydrogen peroxide (H
2
O
2
) conditions. Nevertheless, the addition of exogenous vitamin C for 60 min significantly up-regulated the
SsPRF1
gene in the Ss
CCP1
deletion mutants. Moreover, the constitutive expression of
SsPRF1
essentially reinstated the mating/filamentation of Ss
CCP1
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
.
Reactive oxygen species play an important role in pathogen-plant interactions. In fungi, cytochrome
c
-peroxidase maintains intracellular ROS homeostasis by utilizing H
2
O
2
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 H
2
O
2
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. |
---|---|
AbstractList | 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.IMPORTANCEReactive 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. Reactive oxygen species play an important role in pathogen-plant interactions. In fungi, cytochrome -peroxidase maintains intracellular ROS homeostasis by utilizing H O as an electron acceptor to oxidize ferrocytochrome , thereby contributing to disease pathogenesis. In this study, our investigation reveals that the cytochrome -peroxidase encoding gene, , not only plays a key role in resisting H O toxicity but is also essential for the mating/filamentation and pathogenicity of . We further uncover that SsCcp1 mediates the expression of SsPrf1 by maintaining intracellular ROS homeostasis to regulate mating/filamentation. Our findings provide novel insights into how cytochrome -peroxidase regulates sexual reproduction in phytopathogenic fungi, presenting a theoretical foundation for designing new disease control strategies. 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. 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, Ss CCP1 , 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 Ss CCP1 deletion mutants or under exogenous hydrogen peroxide (H 2 O 2 ) conditions. Nevertheless, the addition of exogenous vitamin C for 60 min significantly up-regulated the SsPRF1 gene in the Ss CCP1 deletion mutants. Moreover, the constitutive expression of SsPRF1 essentially reinstated the mating/filamentation of Ss CCP1 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 . Reactive oxygen species play an important role in pathogen-plant interactions. In fungi, cytochrome c -peroxidase maintains intracellular ROS homeostasis by utilizing H 2 O 2 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 H 2 O 2 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. 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, Ss CCP1 , 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 Ss CCP1 deletion mutants or under exogenous hydrogen peroxide (H 2 O 2 ) conditions. Nevertheless, the addition of exogenous vitamin C for 60 min significantly up-regulated the SsPRF1 gene in the Ss CCP1 deletion mutants. Moreover, the constitutive expression of SsPRF1 essentially reinstated the mating/filamentation of Ss CCP1 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 . ABSTRACT 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. |
Author | Jiang, Zide Feng, Ruqing Cai, Enping Zhang, Li Zheng, Wenqiang Jia, Huan Li, Lei Chang, Changqing |
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Keywords | mating/filamentation Sporisorium scitamineum cytochrome c-peroxidase pheromone response factor reactive oxygen species |
Language | English |
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10.1016/s0304-4165(03)00151-x |
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Snippet | Sugarcane smut, caused by the basidiomycetous fungus
Sporisorium scitamineum,
is a global fungal disease resulting in substantial economic losses. Our previous... Reactive oxygen species play an important role in pathogen-plant interactions. In fungi, cytochrome -peroxidase maintains intracellular ROS homeostasis by... Sugarcane smut, caused by the basidiomycetous fungus Sporisorium scitamineum, is a global fungal disease resulting in substantial economic losses. Our previous... Reactive oxygen species play an important role in pathogen-plant interactions. In fungi, cytochrome c-peroxidase maintains intracellular ROS homeostasis by... ABSTRACT Sugarcane smut, caused by the basidiomycetous fungus Sporisorium scitamineum, is a global fungal disease resulting in substantial economic losses. Our... |
SourceID | doaj pubmedcentral proquest asm2 pubmed crossref |
SourceType | Open Website Open Access Repository Aggregation Database Index Database Enrichment Source |
StartPage | e0205723 |
SubjectTerms | cytochrome c-peroxidase mating/filamentation Mycology pheromone response factor reactive oxygen species Research Article Sporisorium scitamineum |
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Title | Cytochrome c -peroxidase modulates ROS homeostasis to regulate the sexual mating of Sporisorium scitamineum |
URI | https://www.ncbi.nlm.nih.gov/pubmed/37819114 https://journals.asm.org/doi/10.1128/spectrum.02057-23 https://www.proquest.com/docview/2876635329 https://pubmed.ncbi.nlm.nih.gov/PMC10714796 https://doaj.org/article/c599a6c122644325ae33f19ee114a364 |
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