Evidence map›Paper›PMID 32879321›Full record

ArticleNature communications2020

Evolution of a guarded decoy protease and its receptor in solanaceous plants.

Jiorgos Kourelis, Shivani Malik, Oliver Mattinson, Sonja Krauter, Parvinderdeep S Kahlon, Judith K Paulus, Renier A L van der Hoorn

Erratum issuedAbstract read
In one paragraph

Article in Nature communications, 2020. The graph could read no effect estimate from its abstract, so it casts no vote on the map. An erratum has been issued. Cited by 31 papers.

0numbers the graph read from it
0cells of the map it votes in
31citing papers in PubMed
–field-weighted citation impact
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

31 citing papers in PubMed.

  1. Review
  2. A secreted citrus protease cleaves an outer membrane protein of the Huanglongbing pathogen.Proceedings of the National Academy of Sciences of the United States of America · 2026
    Article
  3. Pathogen-inspired engineering of plant protease enhances late blight resistance.Proceedings of the National Academy of Sciences of the United States of America · 2026
    Article
  4. Review
  5. Review
  6. Review
  7. Article
  8. Article
  9. Review
  10. Plants (Basel, Switzerland) · 2024
    Article
  11. Article
  12. Article
  13. Article
  14. Article
  15. Article
  16. Article
  17. Article
  18. Article
  19. Review
  20. Review
4 · The record

Corrections and comments

5 · Who and what money

Authors and funding

7 authors.

Jiorgos KourelisPlant Chemetics Laboratory, Department of Plant Sciences, University of Oxford, South Parks Road, OX1 3RB, Oxford, UK.ORCID http://orcid.org/0000-0002-9007-1333
Shivani MalikPlant Chemetics Laboratory, Department of Plant Sciences, University of Oxford, South Parks Road, OX1 3RB, Oxford, UK.
Oliver MattinsonPlant Chemetics Laboratory, Department of Plant Sciences, University of Oxford, South Parks Road, OX1 3RB, Oxford, UK.ORCID http://orcid.org/0000-0001-8374-0837
Sonja KrauterPlant Chemetics Laboratory, Department of Plant Sciences, University of Oxford, South Parks Road, OX1 3RB, Oxford, UK.
Parvinderdeep S KahlonPlant Chemetics Laboratory, Department of Plant Sciences, University of Oxford, South Parks Road, OX1 3RB, Oxford, UK.
Judith K PaulusPlant Chemetics Laboratory, Department of Plant Sciences, University of Oxford, South Parks Road, OX1 3RB, Oxford, UK.
Renier A L van der HoornPlant Chemetics Laboratory, Department of Plant Sciences, University of Oxford, South Parks Road, OX1 3RB, Oxford, UK. renier.vanderhoorn@plants.ox.ac.uk.ORCID http://orcid.org/0000-0002-3692-7487

Funding

Biotechnology and Biological Sciences Research Council BB/S003193/1
6 · The paper itself

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.

Indexed as

CladosporiumNicotianaSolanumDisease ResistanceEvolution, MolecularFungal ProteinsGenes, PlantHost-Parasite InteractionsPeptide HydrolasesPhylogenyPlant DiseasesPlant ImmunityPlant ProteinsProtease InhibitorsFungal ProteinsPeptide HydrolasesPlant ProteinsProtease Inhibitors

Identifiers

PMID32879321
PMCPMC7468133

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Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.