Evolution of a guarded decoy protease and its receptor in solanaceous plants
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 tar...
| Main Authors: | , , , , , , |
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| Format: | Journal article |
| Language: | English |
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Springer Nature
2020
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| _version_ | 1797074807688265728 |
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| author | Kourelis, J Malik, S Mattinson, O Krauter, S Kahlon, PS Paulus, JK van der Hoorn, RAL |
| author_facet | Kourelis, J Malik, S Mattinson, O Krauter, S Kahlon, PS Paulus, JK van der Hoorn, RAL |
| author_sort | Kourelis, J |
| collection | OXFORD |
| description | 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 | 2024-03-06T23:41:33Z |
| format | Journal article |
| id | oxford-uuid:6f80613f-0930-495f-aebb-26b795ec300e |
| institution | University of Oxford |
| language | English |
| last_indexed | 2024-03-06T23:41:33Z |
| publishDate | 2020 |
| publisher | Springer Nature |
| record_format | dspace |
| spelling | oxford-uuid:6f80613f-0930-495f-aebb-26b795ec300e2022-03-26T19:31:01ZEvolution of a guarded decoy protease and its receptor in solanaceous plantsJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:6f80613f-0930-495f-aebb-26b795ec300eEnglishSymplectic ElementsSpringer Nature2020Kourelis, JMalik, SMattinson, OKrauter, SKahlon, PSPaulus, JKvan der Hoorn, RALRcr3 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. |
| spellingShingle | Kourelis, J Malik, S Mattinson, O Krauter, S Kahlon, PS Paulus, JK van der Hoorn, RAL Evolution of a guarded decoy protease and its receptor in solanaceous plants |
| 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 |
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