Jiorgos Kourelis, Mariana Schuster, Fatih Demir, Oliver Mattinson, Sonja Krauter, Parvinderdeep S Kahlon, Ruby O'Grady, Samantha Royston, Ana Lucía Bravo-Cazar, Brian C Mooney, Pitter F Huesgen, Sophien Kamoun, Renier A L van der Hoorn
{"title":"生物工程分泌蛋白酶将不同的 Rcr3 直向同源物和旁系同源物转化为细胞外免疫共受体。","authors":"Jiorgos Kourelis, Mariana Schuster, Fatih Demir, Oliver Mattinson, Sonja Krauter, Parvinderdeep S Kahlon, Ruby O'Grady, Samantha Royston, Ana Lucía Bravo-Cazar, Brian C Mooney, Pitter F Huesgen, Sophien Kamoun, Renier A L van der Hoorn","doi":"10.1093/plcell/koae183","DOIUrl":null,"url":null,"abstract":"<p><p>Secreted immune proteases \"Required for Cladosporium resistance-3\" (Rcr3) and \"Phytophthora-inhibited protease-1\" (Pip1) of tomato (Solanum lycopersicum) are both inhibited by Avirulence-2 (Avr2) from the fungal plant pathogen Cladosporium fulvum. However, only Rcr3 acts as a decoy co-receptor that detects Avr2 in the presence of the Cf-2 immune receptor. Here, we identified crucial residues in tomato Rcr3 that are required for Cf-2-mediated signaling and bioengineered various proteases to trigger Avr2/Cf-2-dependent immunity. Despite substantial divergence in Rcr3 orthologs from eggplant (Solanum melongena) and tobacco (Nicotiana spp.), minimal alterations were sufficient to trigger Avr2/Cf-2-mediated immune signaling. By contrast, tomato Pip1 was bioengineered with 16 Rcr3-specific residues to initiate Avr2/Cf-2-triggered immune signaling. These residues cluster on one side of the protein next to the substrate-binding groove, indicating a potential Cf-2 interaction site. Our findings also revealed that Rcr3 and Pip1 have distinct substrate preferences determined by two variant residues and that both are suboptimal for binding Avr2. This study advances our understanding of Avr2 perception and opens avenues to bioengineer proteases to broaden pathogen recognition in other crops.</p>","PeriodicalId":20186,"journal":{"name":"Plant Cell","volume":null,"pages":null},"PeriodicalIF":10.0000,"publicationDate":"2024-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11371160/pdf/","citationCount":"0","resultStr":"{\"title\":\"Bioengineering secreted proteases converts divergent Rcr3 orthologs and paralogs into extracellular immune co-receptors.\",\"authors\":\"Jiorgos Kourelis, Mariana Schuster, Fatih Demir, Oliver Mattinson, Sonja Krauter, Parvinderdeep S Kahlon, Ruby O'Grady, Samantha Royston, Ana Lucía Bravo-Cazar, Brian C Mooney, Pitter F Huesgen, Sophien Kamoun, Renier A L van der Hoorn\",\"doi\":\"10.1093/plcell/koae183\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Secreted immune proteases \\\"Required for Cladosporium resistance-3\\\" (Rcr3) and \\\"Phytophthora-inhibited protease-1\\\" (Pip1) of tomato (Solanum lycopersicum) are both inhibited by Avirulence-2 (Avr2) from the fungal plant pathogen Cladosporium fulvum. However, only Rcr3 acts as a decoy co-receptor that detects Avr2 in the presence of the Cf-2 immune receptor. Here, we identified crucial residues in tomato Rcr3 that are required for Cf-2-mediated signaling and bioengineered various proteases to trigger Avr2/Cf-2-dependent immunity. Despite substantial divergence in Rcr3 orthologs from eggplant (Solanum melongena) and tobacco (Nicotiana spp.), minimal alterations were sufficient to trigger Avr2/Cf-2-mediated immune signaling. By contrast, tomato Pip1 was bioengineered with 16 Rcr3-specific residues to initiate Avr2/Cf-2-triggered immune signaling. These residues cluster on one side of the protein next to the substrate-binding groove, indicating a potential Cf-2 interaction site. Our findings also revealed that Rcr3 and Pip1 have distinct substrate preferences determined by two variant residues and that both are suboptimal for binding Avr2. This study advances our understanding of Avr2 perception and opens avenues to bioengineer proteases to broaden pathogen recognition in other crops.</p>\",\"PeriodicalId\":20186,\"journal\":{\"name\":\"Plant Cell\",\"volume\":null,\"pages\":null},\"PeriodicalIF\":10.0000,\"publicationDate\":\"2024-09-03\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11371160/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Plant Cell\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1093/plcell/koae183\",\"RegionNum\":1,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"BIOCHEMISTRY & MOLECULAR BIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Plant Cell","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1093/plcell/koae183","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
Bioengineering secreted proteases converts divergent Rcr3 orthologs and paralogs into extracellular immune co-receptors.
Secreted immune proteases "Required for Cladosporium resistance-3" (Rcr3) and "Phytophthora-inhibited protease-1" (Pip1) of tomato (Solanum lycopersicum) are both inhibited by Avirulence-2 (Avr2) from the fungal plant pathogen Cladosporium fulvum. However, only Rcr3 acts as a decoy co-receptor that detects Avr2 in the presence of the Cf-2 immune receptor. Here, we identified crucial residues in tomato Rcr3 that are required for Cf-2-mediated signaling and bioengineered various proteases to trigger Avr2/Cf-2-dependent immunity. Despite substantial divergence in Rcr3 orthologs from eggplant (Solanum melongena) and tobacco (Nicotiana spp.), minimal alterations were sufficient to trigger Avr2/Cf-2-mediated immune signaling. By contrast, tomato Pip1 was bioengineered with 16 Rcr3-specific residues to initiate Avr2/Cf-2-triggered immune signaling. These residues cluster on one side of the protein next to the substrate-binding groove, indicating a potential Cf-2 interaction site. Our findings also revealed that Rcr3 and Pip1 have distinct substrate preferences determined by two variant residues and that both are suboptimal for binding Avr2. This study advances our understanding of Avr2 perception and opens avenues to bioengineer proteases to broaden pathogen recognition in other crops.
期刊介绍:
Title: Plant Cell
Publisher:
Published monthly by the American Society of Plant Biologists (ASPB)
Produced by Sheridan Journal Services, Waterbury, VT
History and Impact:
Established in 1989
Within three years of publication, ranked first in impact among journals in plant sciences
Maintains high standard of excellence
Scope:
Publishes novel research of special significance in plant biology
Focus areas include cellular biology, molecular biology, biochemistry, genetics, development, and evolution
Primary criteria: articles provide new insight of broad interest to plant biologists and are suitable for a wide audience
Tenets:
Publish the most exciting, cutting-edge research in plant cellular and molecular biology
Provide rapid turnaround time for reviewing and publishing research papers
Ensure highest quality reproduction of data
Feature interactive format for commentaries, opinion pieces, and exchange of information in review articles, meeting reports, and insightful overviews.