Evolution of a guarded decoy protease and its receptor in solanaceous plants
Abstract Rcr3 is a secreted protease of tomato that is targeted by fungal effector Avr2, a secreted protease inhibitor of the fungal pathogen Cladosporium fulvum. The Avr2-Rcr3 complex is recognized by receptor-like protein Cf-2, triggering hypersensitive cell death (HR) and disease resistance. Avr2...
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| Format: | Article |
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Nature Portfolio
2020-09-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-020-18069-5 |
| _version_ | 1797259255893458944 |
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| author | Jiorgos Kourelis Shivani Malik Oliver Mattinson Sonja Krauter Parvinderdeep S. Kahlon Judith K. Paulus Renier A. L. van der Hoorn |
| author_facet | Jiorgos Kourelis Shivani Malik Oliver Mattinson Sonja Krauter Parvinderdeep S. Kahlon Judith K. Paulus Renier A. L. van der Hoorn |
| author_sort | Jiorgos Kourelis |
| collection | DOAJ |
| description | Abstract Rcr3 is a secreted protease of tomato that is targeted by fungal effector Avr2, a secreted protease inhibitor of the fungal pathogen Cladosporium fulvum. The Avr2-Rcr3 complex is recognized by receptor-like protein Cf-2, triggering hypersensitive cell death (HR) and disease resistance. Avr2 also targets Rcr3 paralog Pip1, which is not required for Avr2 recognition but contributes to basal resistance. Thus, Rcr3 acts as a guarded decoy in this interaction, trapping the fungus into a recognition event. Here we show that Rcr3 evolved > 50 million years ago (Mya), whereas Cf-2 evolved <6Mya by co-opting the pre-existing Rcr3 in the Solanum genus. Ancient Rcr3 homologs present in tomato, potato, eggplants, pepper, petunia and tobacco can be inhibited by Avr2 with the exception of tobacco Rcr3. Four variant residues in Rcr3 promote Avr2 inhibition, but the Rcr3 that co-evolved with Cf-2 lacks three of these residues, indicating that the Rcr3 co-receptor is suboptimal for Avr2 binding. Pepper Rcr3 triggers HR with Cf-2 and Avr2 when engineered for enhanced inhibition by Avr2. Nicotiana benthamiana (Nb) is a natural null mutant carrying Rcr3 and Pip1 alleles with deleterious frame-shift mutations. Resurrected NbRcr3 and NbPip1 alleles were active proteases and further NbRcr3 engineering facilitated Avr2 inhibition, uncoupled from HR signalling. The evolution of a receptor co-opting a conserved pathogen target contrasts with other indirect pathogen recognition mechanisms. |
| first_indexed | 2024-04-24T23:06:32Z |
| format | Article |
| id | doaj.art-f06f727180e840529b180b777a865dbf |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-04-24T23:06:32Z |
| publishDate | 2020-09-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-f06f727180e840529b180b777a865dbf2024-03-17T12:29:58ZengNature PortfolioNature Communications2041-17232020-09-0111111510.1038/s41467-020-18069-5Evolution of a guarded decoy protease and its receptor in solanaceous plantsJiorgos Kourelis0Shivani Malik1Oliver Mattinson2Sonja Krauter3Parvinderdeep S. Kahlon4Judith K. Paulus5Renier A. L. van der Hoorn6Plant Chemetics Laboratory, Department of Plant Sciences, University of OxfordPlant Chemetics Laboratory, Department of Plant Sciences, University of OxfordPlant Chemetics Laboratory, Department of Plant Sciences, University of OxfordPlant Chemetics Laboratory, Department of Plant Sciences, University of OxfordPlant Chemetics Laboratory, Department of Plant Sciences, University of OxfordPlant Chemetics Laboratory, Department of Plant Sciences, University of OxfordPlant Chemetics Laboratory, Department of Plant Sciences, University of OxfordAbstract Rcr3 is a secreted protease of tomato that is targeted by fungal effector Avr2, a secreted protease inhibitor of the fungal pathogen Cladosporium fulvum. The Avr2-Rcr3 complex is recognized by receptor-like protein Cf-2, triggering hypersensitive cell death (HR) and disease resistance. Avr2 also targets Rcr3 paralog Pip1, which is not required for Avr2 recognition but contributes to basal resistance. Thus, Rcr3 acts as a guarded decoy in this interaction, trapping the fungus into a recognition event. Here we show that Rcr3 evolved > 50 million years ago (Mya), whereas Cf-2 evolved <6Mya by co-opting the pre-existing Rcr3 in the Solanum genus. Ancient Rcr3 homologs present in tomato, potato, eggplants, pepper, petunia and tobacco can be inhibited by Avr2 with the exception of tobacco Rcr3. Four variant residues in Rcr3 promote Avr2 inhibition, but the Rcr3 that co-evolved with Cf-2 lacks three of these residues, indicating that the Rcr3 co-receptor is suboptimal for Avr2 binding. Pepper Rcr3 triggers HR with Cf-2 and Avr2 when engineered for enhanced inhibition by Avr2. Nicotiana benthamiana (Nb) is a natural null mutant carrying Rcr3 and Pip1 alleles with deleterious frame-shift mutations. Resurrected NbRcr3 and NbPip1 alleles were active proteases and further NbRcr3 engineering facilitated Avr2 inhibition, uncoupled from HR signalling. The evolution of a receptor co-opting a conserved pathogen target contrasts with other indirect pathogen recognition mechanisms.https://doi.org/10.1038/s41467-020-18069-5 |
| spellingShingle | Jiorgos Kourelis Shivani Malik Oliver Mattinson Sonja Krauter Parvinderdeep S. Kahlon Judith K. Paulus Renier A. L. van der Hoorn Evolution of a guarded decoy protease and its receptor in solanaceous plants Nature Communications |
| title | Evolution of a guarded decoy protease and its receptor in solanaceous plants |
| title_full | Evolution of a guarded decoy protease and its receptor in solanaceous plants |
| title_fullStr | Evolution of a guarded decoy protease and its receptor in solanaceous plants |
| title_full_unstemmed | Evolution of a guarded decoy protease and its receptor in solanaceous plants |
| title_short | Evolution of a guarded decoy protease and its receptor in solanaceous plants |
| title_sort | evolution of a guarded decoy protease and its receptor in solanaceous plants |
| url | https://doi.org/10.1038/s41467-020-18069-5 |
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