Polyethyleneimine-coated MXene quantum dots improve cotton tolerance to Verticillium dahliae by maintaining ROS homeostasis
Abstract Verticillium dahliae is a soil-borne hemibiotrophic fungal pathogen that threatens cotton production worldwide. In this study, we assemble the genomes of two V. dahliae isolates: the more virulence and defoliating isolate V991 and nondefoliating isolate 1cd3-2. Transcriptome and comparative...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-11-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-43192-4 |
| _version_ | 1797557956095508480 |
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| author | Ping Qiu Jiayue Li Lin Zhang Kun Chen Jianmin Shao Baoxin Zheng Hang Yuan Jie Qi Lin Yue Qin Hu Yuqing Ming Shiming Liu Lu Long Jiangjiang Gu Xianlong Zhang Keith Lindsey Wei Gao Honghong Wu Longfu Zhu |
| author_facet | Ping Qiu Jiayue Li Lin Zhang Kun Chen Jianmin Shao Baoxin Zheng Hang Yuan Jie Qi Lin Yue Qin Hu Yuqing Ming Shiming Liu Lu Long Jiangjiang Gu Xianlong Zhang Keith Lindsey Wei Gao Honghong Wu Longfu Zhu |
| author_sort | Ping Qiu |
| collection | DOAJ |
| description | Abstract Verticillium dahliae is a soil-borne hemibiotrophic fungal pathogen that threatens cotton production worldwide. In this study, we assemble the genomes of two V. dahliae isolates: the more virulence and defoliating isolate V991 and nondefoliating isolate 1cd3-2. Transcriptome and comparative genomics analyses show that genes associated with pathogen virulence are mostly induced at the late stage of infection (Stage II), accompanied by a burst of reactive oxygen species (ROS), with upregulation of more genes involved in defense response in cotton. We identify the V991-specific virulence gene SP3 that is highly expressed during the infection Stage II. V. dahliae SP3 knock-out strain shows attenuated virulence and triggers less ROS production in cotton plants. To control the disease, we employ polyethyleneimine-coated MXene quantum dots (PEI-MQDs) that possess the ability to remove ROS. Cotton seedlings treated with PEI-MQDs are capable of maintaining ROS homeostasis with enhanced peroxidase, catalase, and glutathione peroxidase activities and exhibit improved tolerance to V. dahliae. These results suggest that V. dahliae trigger ROS production to promote infection and scavenging ROS is an effective way to manage this disease. This study reveals a virulence mechanism of V. dahliae and provides a means for V. dahliae resistance that benefits cotton production. |
| first_indexed | 2024-03-10T17:23:33Z |
| format | Article |
| id | doaj.art-94f904d297ff4a15ad9e77253a0b610d |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-10T17:23:33Z |
| publishDate | 2023-11-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-94f904d297ff4a15ad9e77253a0b610d2023-11-20T10:15:34ZengNature PortfolioNature Communications2041-17232023-11-0114111210.1038/s41467-023-43192-4Polyethyleneimine-coated MXene quantum dots improve cotton tolerance to Verticillium dahliae by maintaining ROS homeostasisPing Qiu0Jiayue Li1Lin Zhang2Kun Chen3Jianmin Shao4Baoxin Zheng5Hang Yuan6Jie Qi7Lin Yue8Qin Hu9Yuqing Ming10Shiming Liu11Lu Long12Jiangjiang Gu13Xianlong Zhang14Keith Lindsey15Wei Gao16Honghong Wu17Longfu Zhu18National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural UniversityHubei Hongshan Laboratory, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural UniversityHubei Hongshan Laboratory, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural UniversityHubei Hongshan Laboratory, Huazhong Agricultural UniversityHubei Hongshan Laboratory, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural UniversityState Key Laboratory of Cotton Biology, Henan Key Laboratory of Plant Stress Biology, Henan UniversityMOA Key Laboratory of Crop Ecophysiology and Farming System in the Middle Reaches of the Yangtze River, The Center of Crop Nanobiotechnology, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural UniversityDepartment of Biosciences, Durham UniversityState Key Laboratory of Cotton Biology, Henan Key Laboratory of Plant Stress Biology, Henan UniversityNational Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural UniversityAbstract Verticillium dahliae is a soil-borne hemibiotrophic fungal pathogen that threatens cotton production worldwide. In this study, we assemble the genomes of two V. dahliae isolates: the more virulence and defoliating isolate V991 and nondefoliating isolate 1cd3-2. Transcriptome and comparative genomics analyses show that genes associated with pathogen virulence are mostly induced at the late stage of infection (Stage II), accompanied by a burst of reactive oxygen species (ROS), with upregulation of more genes involved in defense response in cotton. We identify the V991-specific virulence gene SP3 that is highly expressed during the infection Stage II. V. dahliae SP3 knock-out strain shows attenuated virulence and triggers less ROS production in cotton plants. To control the disease, we employ polyethyleneimine-coated MXene quantum dots (PEI-MQDs) that possess the ability to remove ROS. Cotton seedlings treated with PEI-MQDs are capable of maintaining ROS homeostasis with enhanced peroxidase, catalase, and glutathione peroxidase activities and exhibit improved tolerance to V. dahliae. These results suggest that V. dahliae trigger ROS production to promote infection and scavenging ROS is an effective way to manage this disease. This study reveals a virulence mechanism of V. dahliae and provides a means for V. dahliae resistance that benefits cotton production.https://doi.org/10.1038/s41467-023-43192-4 |
| spellingShingle | Ping Qiu Jiayue Li Lin Zhang Kun Chen Jianmin Shao Baoxin Zheng Hang Yuan Jie Qi Lin Yue Qin Hu Yuqing Ming Shiming Liu Lu Long Jiangjiang Gu Xianlong Zhang Keith Lindsey Wei Gao Honghong Wu Longfu Zhu Polyethyleneimine-coated MXene quantum dots improve cotton tolerance to Verticillium dahliae by maintaining ROS homeostasis Nature Communications |
| title | Polyethyleneimine-coated MXene quantum dots improve cotton tolerance to Verticillium dahliae by maintaining ROS homeostasis |
| title_full | Polyethyleneimine-coated MXene quantum dots improve cotton tolerance to Verticillium dahliae by maintaining ROS homeostasis |
| title_fullStr | Polyethyleneimine-coated MXene quantum dots improve cotton tolerance to Verticillium dahliae by maintaining ROS homeostasis |
| title_full_unstemmed | Polyethyleneimine-coated MXene quantum dots improve cotton tolerance to Verticillium dahliae by maintaining ROS homeostasis |
| title_short | Polyethyleneimine-coated MXene quantum dots improve cotton tolerance to Verticillium dahliae by maintaining ROS homeostasis |
| title_sort | polyethyleneimine coated mxene quantum dots improve cotton tolerance to verticillium dahliae by maintaining ros homeostasis |
| url | https://doi.org/10.1038/s41467-023-43192-4 |
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