Peroxisome dynamics determines host-derived ROS accumulation and infectious growth of the rice blast fungus
ABSTRACTDuring the early stages of host-pathogen interaction, the production of reactive oxygen species (ROS) in host cells is a critical strategy to halt the spread of pathogens. Pathogens have to minimize the deleterious effects of host-generated ROS for successful invasion. However, the underlyin...
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| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2023-12-01
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| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mbio.02381-23 |
| _version_ | 1827573174534930432 |
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| author | Jun Zhang Huimin Li Wangliu Gu Kexin Zhang Xinyu Liu Muxing Liu Leiyun Yang Gang Li Zhengguang Zhang Haifeng Zhang |
| author_facet | Jun Zhang Huimin Li Wangliu Gu Kexin Zhang Xinyu Liu Muxing Liu Leiyun Yang Gang Li Zhengguang Zhang Haifeng Zhang |
| author_sort | Jun Zhang |
| collection | DOAJ |
| description | ABSTRACTDuring the early stages of host-pathogen interaction, the production of reactive oxygen species (ROS) in host cells is a critical strategy to halt the spread of pathogens. Pathogens have to minimize the deleterious effects of host-generated ROS for successful invasion. However, the underlying mechanism remains largely elusive. Here, we report that a peroxisomal 3-ketoacyl-CoA thiolase of rice blast fungus Magnaporthe oryzae, MoKat2, functions in host ROS homeostasis likely through regulating fungal peroxisome morphology during infection. M. oryzae peroxisome elongates in response to ROS stress, and this is attributed to the function of peroxisome localized MoKat2. MoKat2 forms homodimer in vivo while the homodimer is dissociated into monomer in response to host-derived ROS. The MoKat2 monomer binds to peroxisome membranes through its amphipathic helices to control peroxisome elongation, resulting in host ROS depletion and subsequent M. oryzae invasion in rice cells. Our findings shed light on the interplay between pathogenic peroxisome dynamics and host ROS accumulation, expanding the crucial role of organelle-mediated infection in plant-microbe interactions.IMPORTANCEThe interplay between plant and pathogen is a dynamic process, with the host’s innate defense mechanisms serving a crucial role in preventing infection. In response to many plant pathogen infections, host cells generate the key regulatory molecule, reactive oxygen species (ROS), to limit the spread of the invading organism. In this study, we reveal the effects of fungal peroxisome dynamics on host ROS homeostasis, during the rice blast fungus Magnaporthe oryzae infection. The elongation of the peroxisome appears contingent upon ROS and links to the accumulation of ROS within the host and the infectious growth of the pathogen. Importantly, we identify a peroxisomal 3-ketoacyl-CoA thiolase, MoKat2, responsible for the elongation of the peroxisome during the infection. In response to host-derived ROS, the homodimer of MoKat2 undergoes dissociation to bind peroxisome membranes for peroxisome elongation. This process, in turn, inhibits the accumulation of host ROS, which is necessary for successful infection. Overall, our study is the first to highlight the intricate relationship between fungal organelle dynamics and ROS-mediated host immunity, extending the fundamental knowledge of pathogen-host interaction. |
| first_indexed | 2024-03-08T20:14:29Z |
| format | Article |
| id | doaj.art-e0b6855ce39047efae8aa341efbf4cfe |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-03-08T20:14:29Z |
| publishDate | 2023-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-e0b6855ce39047efae8aa341efbf4cfe2023-12-22T19:53:43ZengAmerican Society for MicrobiologymBio2150-75112023-12-0114610.1128/mbio.02381-23Peroxisome dynamics determines host-derived ROS accumulation and infectious growth of the rice blast fungusJun Zhang0Huimin Li1Wangliu Gu2Kexin Zhang3Xinyu Liu4Muxing Liu5Leiyun Yang6Gang Li7Zhengguang Zhang8Haifeng Zhang9Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, ChinaDepartment of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, ChinaDepartment of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, ChinaDepartment of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, ChinaDepartment of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, ChinaDepartment of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, ChinaDepartment of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, ChinaDepartment of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, ChinaDepartment of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, ChinaDepartment of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, ChinaABSTRACTDuring the early stages of host-pathogen interaction, the production of reactive oxygen species (ROS) in host cells is a critical strategy to halt the spread of pathogens. Pathogens have to minimize the deleterious effects of host-generated ROS for successful invasion. However, the underlying mechanism remains largely elusive. Here, we report that a peroxisomal 3-ketoacyl-CoA thiolase of rice blast fungus Magnaporthe oryzae, MoKat2, functions in host ROS homeostasis likely through regulating fungal peroxisome morphology during infection. M. oryzae peroxisome elongates in response to ROS stress, and this is attributed to the function of peroxisome localized MoKat2. MoKat2 forms homodimer in vivo while the homodimer is dissociated into monomer in response to host-derived ROS. The MoKat2 monomer binds to peroxisome membranes through its amphipathic helices to control peroxisome elongation, resulting in host ROS depletion and subsequent M. oryzae invasion in rice cells. Our findings shed light on the interplay between pathogenic peroxisome dynamics and host ROS accumulation, expanding the crucial role of organelle-mediated infection in plant-microbe interactions.IMPORTANCEThe interplay between plant and pathogen is a dynamic process, with the host’s innate defense mechanisms serving a crucial role in preventing infection. In response to many plant pathogen infections, host cells generate the key regulatory molecule, reactive oxygen species (ROS), to limit the spread of the invading organism. In this study, we reveal the effects of fungal peroxisome dynamics on host ROS homeostasis, during the rice blast fungus Magnaporthe oryzae infection. The elongation of the peroxisome appears contingent upon ROS and links to the accumulation of ROS within the host and the infectious growth of the pathogen. Importantly, we identify a peroxisomal 3-ketoacyl-CoA thiolase, MoKat2, responsible for the elongation of the peroxisome during the infection. In response to host-derived ROS, the homodimer of MoKat2 undergoes dissociation to bind peroxisome membranes for peroxisome elongation. This process, in turn, inhibits the accumulation of host ROS, which is necessary for successful infection. Overall, our study is the first to highlight the intricate relationship between fungal organelle dynamics and ROS-mediated host immunity, extending the fundamental knowledge of pathogen-host interaction.https://journals.asm.org/doi/10.1128/mbio.02381-23M. oryzae-rice interactionperoxisome dynamicshost-derived ROSMoKat2infectious growth |
| spellingShingle | Jun Zhang Huimin Li Wangliu Gu Kexin Zhang Xinyu Liu Muxing Liu Leiyun Yang Gang Li Zhengguang Zhang Haifeng Zhang Peroxisome dynamics determines host-derived ROS accumulation and infectious growth of the rice blast fungus mBio M. oryzae-rice interaction peroxisome dynamics host-derived ROS MoKat2 infectious growth |
| title | Peroxisome dynamics determines host-derived ROS accumulation and infectious growth of the rice blast fungus |
| title_full | Peroxisome dynamics determines host-derived ROS accumulation and infectious growth of the rice blast fungus |
| title_fullStr | Peroxisome dynamics determines host-derived ROS accumulation and infectious growth of the rice blast fungus |
| title_full_unstemmed | Peroxisome dynamics determines host-derived ROS accumulation and infectious growth of the rice blast fungus |
| title_short | Peroxisome dynamics determines host-derived ROS accumulation and infectious growth of the rice blast fungus |
| title_sort | peroxisome dynamics determines host derived ros accumulation and infectious growth of the rice blast fungus |
| topic | M. oryzae-rice interaction peroxisome dynamics host-derived ROS MoKat2 infectious growth |
| url | https://journals.asm.org/doi/10.1128/mbio.02381-23 |
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