Whole-genome sequencing and comparative genomics reveal the potential pathogenic mechanism of Neoscytalidium dimidiatum on pitaya
ABSTRACT Neoscytalidium dimidiatum (class Dothideomycetes) is a fungus responsible for canker disease in pitaya stems and fruits, leading to significant economic losses. However, little is known about the pathogenesis, family evolution, and genetic variants of this species. In this study, we report...
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2023-12-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.02733-23 |
| _version_ | 1797393624064851968 |
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| author | Meng Wang Min Xu Zhouwen Wang Yi Ding Shaoling Kang Senrong Jiang Shuangshuang Wei Jun Xie Jiaquan Huang Dongdong Li Wenbin Hu Hongli Li Xingyu Jiang Hua Tang |
| author_facet | Meng Wang Min Xu Zhouwen Wang Yi Ding Shaoling Kang Senrong Jiang Shuangshuang Wei Jun Xie Jiaquan Huang Dongdong Li Wenbin Hu Hongli Li Xingyu Jiang Hua Tang |
| author_sort | Meng Wang |
| collection | DOAJ |
| description | ABSTRACT Neoscytalidium dimidiatum (class Dothideomycetes) is a fungus responsible for canker disease in pitaya stems and fruits, leading to significant economic losses. However, little is known about the pathogenesis, family evolution, and genetic variants of this species. In this study, we report a high-quality genome sequence of N. dimidiatum based on the Nanopore sequencing technology platform for sequencing and Hi-C assembly technology for genome assembly. The genome contains 12 chromosomes (2n = 2× = 12; diploid), with a sequencing depth of 186.1×, encoding 12,349 proteins. Molecular phylogenetic analysis showed that N. dimidiatum is evolutionarily close to Botryosphaeria dothidea. Compared to other fungi, the N. dimidiatum genome contains many carbohydrate-active enzymes and secondary metabolites. Additionally, we predict that N. dimidiatum contains 121 candidate effectors that may play important roles in infection and colonization, promoting pathogenicity in pitaya. Nine of these effectors were confirmed to contain signal peptides and inhibit BAX/INF1-induced necrosis in Nicotiana benthamiana, demonstrating their importance during infection. Finally, we also confirm that N. dimidiatum does not form an appressorium or infection thread but instead infects pitaya via open stomata. In conclusion, the results provide a foundation for future research on N. dimidiatum and the control of pitaya canker. IMPORTANCE Pitaya canker is a significant disease in the pitaya industry in China, causing significant economic losses. Therefore, systematic research on Neoscytalidium dimidiatum, the fungus implicated in pitaya canker, is essential for comprehending the pathogenesis of this disease and developing effective control strategies. We applied comparative genomics to reveal the genetic evolution, metabolic diversity, environmental adaptation, and pathogenicity of N. dimidiatum, providing ideal targets for studies of pathogenesis and molecular targets for fungicide development. Moreover, the systematic study of the N. dimidiatum growth cycle, morphological characteristics, and molecular phylogenetic analysis can promote a comprehensive understanding of its genetic basis. |
| first_indexed | 2024-03-09T00:06:33Z |
| format | Article |
| id | doaj.art-b2df1b9e597a46429384f35a25756832 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-09T00:06:33Z |
| publishDate | 2023-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-b2df1b9e597a46429384f35a257568322023-12-12T13:17:20ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-12-0111610.1128/spectrum.02733-23Whole-genome sequencing and comparative genomics reveal the potential pathogenic mechanism of Neoscytalidium dimidiatum on pitayaMeng Wang0Min Xu1Zhouwen Wang2Yi Ding3Shaoling Kang4Senrong Jiang5Shuangshuang Wei6Jun Xie7Jiaquan Huang8Dongdong Li9Wenbin Hu10Hongli Li11Xingyu Jiang12Hua Tang13School of Breeding and Multiplication, Hainan University , Sanya, ChinaCollege of Life Sciences, China Jiliang University , Hangzhou, ChinaSchool of Breeding and Multiplication, Hainan University , Sanya, ChinaSchool of Breeding and Multiplication, Hainan University , Sanya, ChinaSchool of Breeding and Multiplication, Hainan University , Sanya, ChinaSchool of Breeding and Multiplication, Hainan University , Sanya, ChinaCollege of Life Sciences, Hainan University , Haikou, ChinaCollege of Life Sciences, Hainan University , Haikou, ChinaSchool of Breeding and Multiplication, Hainan University , Sanya, ChinaSchool of Breeding and Multiplication, Hainan University , Sanya, ChinaTropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences , Haikou, ChinaTropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences , Haikou, ChinaSchool of Tropical Agriculture and Forestry, Hainan University , Haikou, ChinaSchool of Breeding and Multiplication, Hainan University , Sanya, ChinaABSTRACT Neoscytalidium dimidiatum (class Dothideomycetes) is a fungus responsible for canker disease in pitaya stems and fruits, leading to significant economic losses. However, little is known about the pathogenesis, family evolution, and genetic variants of this species. In this study, we report a high-quality genome sequence of N. dimidiatum based on the Nanopore sequencing technology platform for sequencing and Hi-C assembly technology for genome assembly. The genome contains 12 chromosomes (2n = 2× = 12; diploid), with a sequencing depth of 186.1×, encoding 12,349 proteins. Molecular phylogenetic analysis showed that N. dimidiatum is evolutionarily close to Botryosphaeria dothidea. Compared to other fungi, the N. dimidiatum genome contains many carbohydrate-active enzymes and secondary metabolites. Additionally, we predict that N. dimidiatum contains 121 candidate effectors that may play important roles in infection and colonization, promoting pathogenicity in pitaya. Nine of these effectors were confirmed to contain signal peptides and inhibit BAX/INF1-induced necrosis in Nicotiana benthamiana, demonstrating their importance during infection. Finally, we also confirm that N. dimidiatum does not form an appressorium or infection thread but instead infects pitaya via open stomata. In conclusion, the results provide a foundation for future research on N. dimidiatum and the control of pitaya canker. IMPORTANCE Pitaya canker is a significant disease in the pitaya industry in China, causing significant economic losses. Therefore, systematic research on Neoscytalidium dimidiatum, the fungus implicated in pitaya canker, is essential for comprehending the pathogenesis of this disease and developing effective control strategies. We applied comparative genomics to reveal the genetic evolution, metabolic diversity, environmental adaptation, and pathogenicity of N. dimidiatum, providing ideal targets for studies of pathogenesis and molecular targets for fungicide development. Moreover, the systematic study of the N. dimidiatum growth cycle, morphological characteristics, and molecular phylogenetic analysis can promote a comprehensive understanding of its genetic basis.https://journals.asm.org/doi/10.1128/spectrum.02733-23Neoscytalidium dimidiatumgenome sequencingcomparative genome analysispitaya canker |
| spellingShingle | Meng Wang Min Xu Zhouwen Wang Yi Ding Shaoling Kang Senrong Jiang Shuangshuang Wei Jun Xie Jiaquan Huang Dongdong Li Wenbin Hu Hongli Li Xingyu Jiang Hua Tang Whole-genome sequencing and comparative genomics reveal the potential pathogenic mechanism of Neoscytalidium dimidiatum on pitaya Microbiology Spectrum Neoscytalidium dimidiatum genome sequencing comparative genome analysis pitaya canker |
| title | Whole-genome sequencing and comparative genomics reveal the potential pathogenic mechanism of Neoscytalidium dimidiatum on pitaya |
| title_full | Whole-genome sequencing and comparative genomics reveal the potential pathogenic mechanism of Neoscytalidium dimidiatum on pitaya |
| title_fullStr | Whole-genome sequencing and comparative genomics reveal the potential pathogenic mechanism of Neoscytalidium dimidiatum on pitaya |
| title_full_unstemmed | Whole-genome sequencing and comparative genomics reveal the potential pathogenic mechanism of Neoscytalidium dimidiatum on pitaya |
| title_short | Whole-genome sequencing and comparative genomics reveal the potential pathogenic mechanism of Neoscytalidium dimidiatum on pitaya |
| title_sort | whole genome sequencing and comparative genomics reveal the potential pathogenic mechanism of neoscytalidium dimidiatum on pitaya |
| topic | Neoscytalidium dimidiatum genome sequencing comparative genome analysis pitaya canker |
| url | https://journals.asm.org/doi/10.1128/spectrum.02733-23 |
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