RALF22 promotes plant immunity and amplifies the Pep3 immune signal
ABSTRACT Rapid alkalinization factors (RALFs) in plants have been reported to dampen pathogen‐associated molecular pattern (PAMP)‐triggered immunity via suppressing PAMP‐induced complex formation between the pattern recognition receptor (PRR) and its co‐receptor BAK1. However, the direct and positiv...
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| Published in | Journal of integrative plant biology Vol. 65; no. 11; pp. 2519 - 2534 |
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| Main Authors | , , , , , |
| Format | Journal Article |
| Language | English |
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01.11.2023
Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province,Institute of Biotechnology,College of Agriculture and Biotechnology,Zhejiang University,866 Yu Hang Tang Road,Hangzhou 310058,China%Centre of Analysis and Measurement,Zhejiang University,866 Yu Hang Tang Road,Hangzhou 310058,China%Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province,Institute of Biotechnology,College of Agriculture and Biotechnology,Zhejiang University,866 Yu Hang Tang Road,Hangzhou 310058,China Hainan Institute,Zhejiang University,Sanya 572025,China |
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| Abstract | ABSTRACT
Rapid alkalinization factors (RALFs) in plants have been reported to dampen pathogen‐associated molecular pattern (PAMP)‐triggered immunity via suppressing PAMP‐induced complex formation between the pattern recognition receptor (PRR) and its co‐receptor BAK1. However, the direct and positive role of RALFs in plant immunity remains largely unknown. Herein, we report the direct and positive roles of a typical RALF, RALF22, in plant immunity. RALF22 alone directly elicited a variety of typical immune responses and triggered resistance against the devastating necrotrophic fungal pathogen Sclerotinia sclerotiorum in a FERONIA (FER)‐dependent manner. LORELEI (LRE)‐like glycosylphosphatidylinositol (GPI)‐anchored protein 1 (LLG1) and NADPH oxidase RBOHD were required for RALF22‐elicited reactive oxygen species (ROS) generation. The mutation of cysteines conserved in the C terminus of RALFs abolished, while the constitutive formation of two disulfide bridges between these cysteines promoted the RALF22‐elicited ROS production and resistance against S. sclerotiorum, demonstrating the requirement of these cysteines in the functions of RALF22 in plant immunity. Furthermore, RALF22 amplified the Pep3‐induced immune signal by dramatically increasing the abundance of PROPEP3 transcript and protein. Supply with RALF22 induced resistance against S. sclerotiorum in Brassica crop plants. Collectively, our results reveal that RALF22 triggers immune responses and augments the Pep3‐induced immune signal in a FER‐dependent manner, and exhibits the potential to be exploited as an immune elicitor in crop protection.
The rapid alkalinization factor RALF22 elicits plant immunity and augments Pep3‐induced immune signals, providing a paradigm of synergistic promotion of plant immunity by two phytocytokines and suggesting RALF22 as an immune elicitor for potential use in crop protection. |
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| AbstractList | Rapid alkalinization factors (RALFs) in plants have been reported to dampen pathogen‐associated molecular pattern (PAMP)‐triggered immunity via suppressing PAMP‐induced complex formation between the pattern recognition receptor (PRR) and its co‐receptor BAK1. However, the direct and positive role of RALFs in plant immunity remains largely unknown. Herein, we report the direct and positive roles of a typical RALF, RALF22, in plant immunity. RALF22 alone directly elicited a variety of typical immune responses and triggered resistance against the devastating necrotrophic fungal pathogen Sclerotinia sclerotiorum in a FERONIA (FER)‐dependent manner. LORELEI (LRE)‐like glycosylphosphatidylinositol (GPI)‐anchored protein 1 (LLG1) and NADPH oxidase RBOHD were required for RALF22‐elicited reactive oxygen species (ROS) generation. The mutation of cysteines conserved in the C terminus of RALFs abolished, while the constitutive formation of two disulfide bridges between these cysteines promoted the RALF22‐elicited ROS production and resistance against S. sclerotiorum, demonstrating the requirement of these cysteines in the functions of RALF22 in plant immunity. Furthermore, RALF22 amplified the Pep3‐induced immune signal by dramatically increasing the abundance of PROPEP3 transcript and protein. Supply with RALF22 induced resistance against S. sclerotiorum in Brassica crop plants. Collectively, our results reveal that RALF22 triggers immune responses and augments the Pep3‐induced immune signal in a FER‐dependent manner, and exhibits the potential to be exploited as an immune elicitor in crop protection. ABSTRACT Rapid alkalinization factors (RALFs) in plants have been reported to dampen pathogen‐associated molecular pattern (PAMP)‐triggered immunity via suppressing PAMP‐induced complex formation between the pattern recognition receptor (PRR) and its co‐receptor BAK1. However, the direct and positive role of RALFs in plant immunity remains largely unknown. Herein, we report the direct and positive roles of a typical RALF, RALF22, in plant immunity. RALF22 alone directly elicited a variety of typical immune responses and triggered resistance against the devastating necrotrophic fungal pathogen Sclerotinia sclerotiorum in a FERONIA (FER)‐dependent manner. LORELEI (LRE)‐like glycosylphosphatidylinositol (GPI)‐anchored protein 1 (LLG1) and NADPH oxidase RBOHD were required for RALF22‐elicited reactive oxygen species (ROS) generation. The mutation of cysteines conserved in the C terminus of RALFs abolished, while the constitutive formation of two disulfide bridges between these cysteines promoted the RALF22‐elicited ROS production and resistance against S. sclerotiorum, demonstrating the requirement of these cysteines in the functions of RALF22 in plant immunity. Furthermore, RALF22 amplified the Pep3‐induced immune signal by dramatically increasing the abundance of PROPEP3 transcript and protein. Supply with RALF22 induced resistance against S. sclerotiorum in Brassica crop plants. Collectively, our results reveal that RALF22 triggers immune responses and augments the Pep3‐induced immune signal in a FER‐dependent manner, and exhibits the potential to be exploited as an immune elicitor in crop protection. The rapid alkalinization factor RALF22 elicits plant immunity and augments Pep3‐induced immune signals, providing a paradigm of synergistic promotion of plant immunity by two phytocytokines and suggesting RALF22 as an immune elicitor for potential use in crop protection. Rapid alkalinization factors(RALFs)in plants have been reported to dampen pathogen-associated molecular pattern(PAMP)-triggered immunity via suppressing PAMP-induced com-plex formation between the pattern recognition receptor(PRR)and its co-receptor BAK1.How-ever,the direct and positive role of RALFs in plant immunity remains largely unknown.Herein,we report the direct and positive roles of a typical RALF,RALF22,in plant immunity.RALF22 alone directly elicited a variety of typical immune responses and triggered resistance against the devastating necrotrophic fungal pathogen Scle-rotinia sclerotiorum in a FERONIA(FER)-dependent manner.LORELEI(LRE)-like glycosylphosphati-dylinositol(GPI)-anchored protein 1(LLG1)and NADPH oxidase RBOHD were required for RALF22-elicited reactive oxygen species(ROS)generation.The mutation of cysteines conserved in the C ter-minus of RALFs abolished,while the constitutive formation of two disulfide bridges between these cysteines promoted the RALF22-elicited ROS pro-duction and resistance against S.sclerotiorum,demonstrating the requirement of these cysteines in the functions of RALF22 in plant immunity.Fur-thermore,RALF22 amplified the Pep3-induced im-mune signal by dramatically increasing the abun-dance of PROPEP3 transcript and protein.Supply with RALF22 induced resistance against S.scle-rotiorum in Brassica crop plants.Collectively,our results reveal that RALF22 triggers immune re-sponses and augments the Pep3-induced immune signal in a FER-dependent manner,and exhibits the potential to be exploited as an immune elicitor in crop protection. ABSTRACT Rapid alkalinization factors (RALFs) in plants have been reported to dampen pathogen‐associated molecular pattern (PAMP)‐triggered immunity via suppressing PAMP‐induced complex formation between the pattern recognition receptor (PRR) and its co‐receptor BAK1. However, the direct and positive role of RALFs in plant immunity remains largely unknown. Herein, we report the direct and positive roles of a typical RALF, RALF22, in plant immunity. RALF22 alone directly elicited a variety of typical immune responses and triggered resistance against the devastating necrotrophic fungal pathogen Sclerotinia sclerotiorum in a FERONIA (FER)‐dependent manner. LORELEI (LRE)‐like glycosylphosphatidylinositol (GPI)‐anchored protein 1 (LLG1) and NADPH oxidase RBOHD were required for RALF22‐elicited reactive oxygen species (ROS) generation. The mutation of cysteines conserved in the C terminus of RALFs abolished, while the constitutive formation of two disulfide bridges between these cysteines promoted the RALF22‐elicited ROS production and resistance against S. sclerotiorum , demonstrating the requirement of these cysteines in the functions of RALF22 in plant immunity. Furthermore, RALF22 amplified the Pep3‐induced immune signal by dramatically increasing the abundance of PROPEP3 transcript and protein. Supply with RALF22 induced resistance against S. sclerotiorum in Brassica crop plants. Collectively, our results reveal that RALF22 triggers immune responses and augments the Pep3‐induced immune signal in a FER‐dependent manner, and exhibits the potential to be exploited as an immune elicitor in crop protection. |
| Author | Liang, Yan Cai, Xin‐Zhong Chen, Song‐Yu Xu, You‐Ping Chen, Xing‐Yan He, Yu‐Han |
| AuthorAffiliation | Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province,Institute of Biotechnology,College of Agriculture and Biotechnology,Zhejiang University,866 Yu Hang Tang Road,Hangzhou 310058,China%Centre of Analysis and Measurement,Zhejiang University,866 Yu Hang Tang Road,Hangzhou 310058,China%Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province,Institute of Biotechnology,College of Agriculture and Biotechnology,Zhejiang University,866 Yu Hang Tang Road,Hangzhou 310058,China;Hainan Institute,Zhejiang University,Sanya 572025,China |
| AuthorAffiliation_xml | – name: Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province,Institute of Biotechnology,College of Agriculture and Biotechnology,Zhejiang University,866 Yu Hang Tang Road,Hangzhou 310058,China%Centre of Analysis and Measurement,Zhejiang University,866 Yu Hang Tang Road,Hangzhou 310058,China%Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province,Institute of Biotechnology,College of Agriculture and Biotechnology,Zhejiang University,866 Yu Hang Tang Road,Hangzhou 310058,China;Hainan Institute,Zhejiang University,Sanya 572025,China |
| Author_xml | – sequence: 1 givenname: Yu‐Han orcidid: 0009-0004-0974-1347 surname: He fullname: He, Yu‐Han organization: Zhejiang University – sequence: 2 givenname: Song‐Yu orcidid: 0000-0002-4084-2363 surname: Chen fullname: Chen, Song‐Yu organization: Zhejiang University – sequence: 3 givenname: Xing‐Yan orcidid: 0009-0007-5331-1135 surname: Chen fullname: Chen, Xing‐Yan organization: Zhejiang University – sequence: 4 givenname: You‐Ping orcidid: 0009-0003-5404-1836 surname: Xu fullname: Xu, You‐Ping organization: Zhejiang University – sequence: 5 givenname: Yan orcidid: 0000-0002-1248-8563 surname: Liang fullname: Liang, Yan organization: Zhejiang University – sequence: 6 givenname: Xin‐Zhong orcidid: 0000-0002-5625-526X surname: Cai fullname: Cai, Xin‐Zhong email: xzhcai@zju.edu.cn organization: Zhejiang University |
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| CitedBy_id | crossref_primary_10_3389_fpls_2023_1320509 crossref_primary_10_1016_j_tplants_2024_02_005 crossref_primary_10_1007_s44154_024_00161_1 crossref_primary_10_1016_j_plantsci_2024_112085 crossref_primary_10_1016_j_xplc_2024_100931 crossref_primary_10_3390_ijms25115670 |
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| Copyright | 2023 Institute of Botany, Chinese Academy of Sciences. Copyright © Wanfang Data Co. Ltd. All Rights Reserved. |
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| Keywords | Sclerotinia sclerotiorum FER RALF22 Pep3 plant immunity reactive oxygen species |
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| Notes | These authors contributed equally to this work. Dingzhong Tang, Fujian Agriculture and Forestry University in Fuzhou, China Edited by ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 |
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| PublicationTitle | Journal of integrative plant biology |
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| Publisher | Wiley Subscription Services, Inc Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province,Institute of Biotechnology,College of Agriculture and Biotechnology,Zhejiang University,866 Yu Hang Tang Road,Hangzhou 310058,China%Centre of Analysis and Measurement,Zhejiang University,866 Yu Hang Tang Road,Hangzhou 310058,China%Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province,Institute of Biotechnology,College of Agriculture and Biotechnology,Zhejiang University,866 Yu Hang Tang Road,Hangzhou 310058,China Hainan Institute,Zhejiang University,Sanya 572025,China |
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Rapid alkalinization factors (RALFs) in plants have been reported to dampen pathogen‐associated molecular pattern (PAMP)‐triggered immunity via... Rapid alkalinization factors (RALFs) in plants have been reported to dampen pathogen‐associated molecular pattern (PAMP)‐triggered immunity via suppressing... Rapid alkalinization factors (RALFs) in plants have been reported to dampen pathogen-associated molecular pattern (PAMP)-triggered immunity via suppressing... Rapid alkalinization factors(RALFs)in plants have been reported to dampen pathogen-associated molecular pattern(PAMP)-triggered immunity via suppressing... |
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| SubjectTerms | Amplification C-Terminus Complex formation FER Glycosylphosphatidylinositol Immune response NAD(P)H oxidase Pathogens Pattern recognition Pattern recognition receptors Pep3 Plant immunity Plant protection Proteins RALF22 Reactive oxygen species Receptors Sclerotinia sclerotiorum |
| Title | RALF22 promotes plant immunity and amplifies the Pep3 immune signal |
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