The SlDOF9‐SlSWEET17 Module: a Switch for Controlling Sugar Distribution Between Nematode Induced Galls and Roots in Tomato
Abstract In the complex interactions between plants and pathogens, the regulation of nutrient allocation plays a critical role in determining plant health and susceptibility to diseases. Root‐knot nematodes (RKNs, Meloidogyne incognita) extract sugar from plants during their interactions with the ho...
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Wiley
2025-07-01
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| Series: | Advanced Science |
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| Online Access: | https://doi.org/10.1002/advs.202501771 |
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| author | Xiaoyun Wang Zhimei Wang Xinyue Tang Jiamei Qin Xiaoxuan Zhou Lixia Gu Huihui Bian Lulu Sun Huang Huang Rui Yang Jianli Wang Shaohui Wang Shuangchen Chen Zhongren Yang Wenchao Zhao |
| author_facet | Xiaoyun Wang Zhimei Wang Xinyue Tang Jiamei Qin Xiaoxuan Zhou Lixia Gu Huihui Bian Lulu Sun Huang Huang Rui Yang Jianli Wang Shaohui Wang Shuangchen Chen Zhongren Yang Wenchao Zhao |
| author_sort | Xiaoyun Wang |
| collection | DOAJ |
| description | Abstract In the complex interactions between plants and pathogens, the regulation of nutrient allocation plays a critical role in determining plant health and susceptibility to diseases. Root‐knot nematodes (RKNs, Meloidogyne incognita) extract sugar from plants during their interactions with the hosts. SWEET (Sugars Will Eventually be Exported Transporters) proteins are a class of non‐energy‐consuming sugar uniporters that regulate the allocation of sugars in plant. Here, it is find that SlSWEET17 (Solanum lycopersicum SWEET17), a member of the SWEET family in tomato, is localized to the plasma membrane, Golgi body and small vacuoles, and is highly expressed in galls. Further studies show that SlSWEET17 negatively regulates the sugar transport capacity of other SlSWEETs via protein interactions. Overexpression of SlSWEET17 significantly decreases the soluble sugar content in galls and susceptibility to RKNs, while SlSWEET17 knockout‐mutation (ko‐mutation) has the opposite effect. It is also identified SlDOF9 (Solanum lycopersicum DNA binding with one finger 9), an upstream negative regulator of SlSWEET17, using ChIP (chromatin immunoprecipitation) analysis, electrophoretic mobility shift assays and dual‐Luciferase assays. SlDOF9‐overexpressing plants show increased sugar content in galls and susceptibility to RKNs, and sldof9cr ko‐mutants have the opposite phenotype. This results show how SlDOF9‐SlSWEET17 affects RKN infection through sugar partitioning from roots to galls. |
| format | Article |
| id | doaj-art-1e0933a5bc33435cbdf224e85cc9d241 |
| institution | DOAJ |
| issn | 2198-3844 |
| language | English |
| publishDate | 2025-07-01 |
| publisher | Wiley |
| record_format | Article |
| series | Advanced Science |
| spelling | doaj-art-1e0933a5bc33435cbdf224e85cc9d2412025-08-20T02:50:52ZengWileyAdvanced Science2198-38442025-07-011228n/an/a10.1002/advs.202501771The SlDOF9‐SlSWEET17 Module: a Switch for Controlling Sugar Distribution Between Nematode Induced Galls and Roots in TomatoXiaoyun Wang0Zhimei Wang1Xinyue Tang2Jiamei Qin3Xiaoxuan Zhou4Lixia Gu5Huihui Bian6Lulu Sun7Huang Huang8Rui Yang9Jianli Wang10Shaohui Wang11Shuangchen Chen12Zhongren Yang13Wenchao Zhao14College of Plant Science and Technology Beijing University of Agriculture No. 7 Beinong Road, Changping District Beijing 102206 ChinaCollege of Plant Science and Technology Beijing University of Agriculture No. 7 Beinong Road, Changping District Beijing 102206 ChinaCollege of Plant Science and Technology Beijing University of Agriculture No. 7 Beinong Road, Changping District Beijing 102206 ChinaCollege of Plant Science and Technology Beijing University of Agriculture No. 7 Beinong Road, Changping District Beijing 102206 ChinaCollege of Plant Science and Technology Beijing University of Agriculture No. 7 Beinong Road, Changping District Beijing 102206 ChinaCollege of Plant Science and Technology Beijing University of Agriculture No. 7 Beinong Road, Changping District Beijing 102206 ChinaCollege of Plant Science and Technology Beijing University of Agriculture No. 7 Beinong Road, Changping District Beijing 102206 ChinaCollege of Plant Science and Technology Beijing University of Agriculture No. 7 Beinong Road, Changping District Beijing 102206 ChinaCollege of Plant Science and Technology Beijing University of Agriculture No. 7 Beinong Road, Changping District Beijing 102206 ChinaCollege of Plant Science and Technology Beijing University of Agriculture No. 7 Beinong Road, Changping District Beijing 102206 ChinaCollege of Plant Science and Technology Beijing University of Agriculture No. 7 Beinong Road, Changping District Beijing 102206 ChinaCollege of Plant Science and Technology Beijing University of Agriculture No. 7 Beinong Road, Changping District Beijing 102206 ChinaCollege of Horticulture and Plant Protection Henan University of Science and Technology Luoyang 471023 ChinaCollege of Horticulture and Plant Protection Inner Mongolia Agricultural University Inner Mongolia 010010 ChinaCollege of Plant Science and Technology Beijing University of Agriculture No. 7 Beinong Road, Changping District Beijing 102206 ChinaAbstract In the complex interactions between plants and pathogens, the regulation of nutrient allocation plays a critical role in determining plant health and susceptibility to diseases. Root‐knot nematodes (RKNs, Meloidogyne incognita) extract sugar from plants during their interactions with the hosts. SWEET (Sugars Will Eventually be Exported Transporters) proteins are a class of non‐energy‐consuming sugar uniporters that regulate the allocation of sugars in plant. Here, it is find that SlSWEET17 (Solanum lycopersicum SWEET17), a member of the SWEET family in tomato, is localized to the plasma membrane, Golgi body and small vacuoles, and is highly expressed in galls. Further studies show that SlSWEET17 negatively regulates the sugar transport capacity of other SlSWEETs via protein interactions. Overexpression of SlSWEET17 significantly decreases the soluble sugar content in galls and susceptibility to RKNs, while SlSWEET17 knockout‐mutation (ko‐mutation) has the opposite effect. It is also identified SlDOF9 (Solanum lycopersicum DNA binding with one finger 9), an upstream negative regulator of SlSWEET17, using ChIP (chromatin immunoprecipitation) analysis, electrophoretic mobility shift assays and dual‐Luciferase assays. SlDOF9‐overexpressing plants show increased sugar content in galls and susceptibility to RKNs, and sldof9cr ko‐mutants have the opposite phenotype. This results show how SlDOF9‐SlSWEET17 affects RKN infection through sugar partitioning from roots to galls.https://doi.org/10.1002/advs.202501771DOF transcription factormeloidogyne incognitaSolanum lycopersicum L.sugar distributionSWEET protein |
| spellingShingle | Xiaoyun Wang Zhimei Wang Xinyue Tang Jiamei Qin Xiaoxuan Zhou Lixia Gu Huihui Bian Lulu Sun Huang Huang Rui Yang Jianli Wang Shaohui Wang Shuangchen Chen Zhongren Yang Wenchao Zhao The SlDOF9‐SlSWEET17 Module: a Switch for Controlling Sugar Distribution Between Nematode Induced Galls and Roots in Tomato Advanced Science DOF transcription factor meloidogyne incognita Solanum lycopersicum L. sugar distribution SWEET protein |
| title | The SlDOF9‐SlSWEET17 Module: a Switch for Controlling Sugar Distribution Between Nematode Induced Galls and Roots in Tomato |
| title_full | The SlDOF9‐SlSWEET17 Module: a Switch for Controlling Sugar Distribution Between Nematode Induced Galls and Roots in Tomato |
| title_fullStr | The SlDOF9‐SlSWEET17 Module: a Switch for Controlling Sugar Distribution Between Nematode Induced Galls and Roots in Tomato |
| title_full_unstemmed | The SlDOF9‐SlSWEET17 Module: a Switch for Controlling Sugar Distribution Between Nematode Induced Galls and Roots in Tomato |
| title_short | The SlDOF9‐SlSWEET17 Module: a Switch for Controlling Sugar Distribution Between Nematode Induced Galls and Roots in Tomato |
| title_sort | sldof9 slsweet17 module a switch for controlling sugar distribution between nematode induced galls and roots in tomato |
| topic | DOF transcription factor meloidogyne incognita Solanum lycopersicum L. sugar distribution SWEET protein |
| url | https://doi.org/10.1002/advs.202501771 |
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