The blast pathogen effector AVR-Pik binds and stabilizes rice heavy metal-associated (HMA) proteins to co-opt their function in immunity
Intracellular nucleotide-binding domain and leucine-rich repeat-containing (NLR) receptors play crucial roles in immunity across multiple domains of life. In plants, a subset of NLRs contain noncanonical integrated domains that are thought to have evolved from host targets of pathogen effectors to serve as pathogen baits. However, the functions of host proteins with similarity to NLR integrated domains and the extent to which they are targeted by pathogen effectors remain largely unknown. Here, we show that the blast fungus effector AVR-Pik binds a subset of related rice proteins containing a heavy metal-associated (HMA) domain, one of the domains that has repeatedly integrated into plant NLR immune receptors. We find that AVR-Pik binding stabilizes the rice small HMA (sHMA) proteins OsHIPP19 and OsHIPP20. Knockout of OsHIPP20 causes enhanced disease resistance towards the blast pathogen, indicating that OsHIPP20 is a susceptibility gene (S-gene). We propose that AVR-Pik has evolved to bind HMA domain proteins and co-opt their function to suppress immunity. Yet this binding carries a trade-off, it triggers immunity in plants carrying NLR receptors with integrated HMA domains.
Authors
- Koki Fujisaki (ORCID: https://orcid.org/0000-0002-8247-6381)
- Tolga O. Bozkurt (ORCID: https://orcid.org/0000-0003-0507-6875)
- Hiromasa Saitoh (ORCID: https://orcid.org/0000-0002-0124-9276)
- Motoki Shimizu (ORCID: https://orcid.org/0000-0002-5622-5554)
- Sophien Kamoun (ORCID: https://orcid.org/0000-0002-0290-0315)
- Ryohei Terauchi (ORCID: https://orcid.org/0000-0002-0095-4651)
- Thorsten Langner (ORCID: https://orcid.org/0000-0002-3401-8888)
- Mark J. Banfield (ORCID: https://orcid.org/0000-0001-8921-3835)
- Yukie Hiraka
- Thomas Kroj (ORCID: https://orcid.org/0000-0002-3752-1788)
- Stella Césari (ORCID: https://orcid.org/0000-0001-8558-0371)
- Aleksandra Białas (ORCID: https://orcid.org/0000-0002-1135-2189)
- Ronny Kellner (ORCID: https://orcid.org/0000-0002-4618-0110)
- Keiichiro Nemoto
- Akiko Hirabuchi
- Takumi Takeda (ORCID: https://orcid.org/0000-0002-2321-4437)
- Kaori Oikawa
- Naomi Miyaji
Institutions
- John Innes Centre (GB)
- University of East Anglia (GB)
- Centre de Coopération Internationale en Recherche Agronomique pour le Développement (FR)
- Université de Montpellier (FR)
- Kyoto University (JP)
- Institut Agro Montpellier (FR)
- Norwich Research Park (GB)
- Sainsbury Laboratory (GB)
- Biologie et Génétique des Interactions Plante-Parasite (FR)
- Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR)
- Iwate Biotechnology Research Center (JP)
- Imperial College London (GB)
Publication Details
- Journal
- PLoS Pathogens
- Published
- 2024-11-18
- DOI
- https://doi.org/10.1371/journal.ppat.1012647
- Citations
- 12
- Primary Topic
- Plant-Microbe Interactions and Immunity
- Type
- article
- Field-Weighted Citation Impact
- 7.20
Funders
- UK Research and Innovation
- Royal Society
- John Innes Foundation
- Directorate for Biological Sciences
- Biotechnology and Biological Sciences Research Council
- European Research Council
- Japan Society for the Promotion of Science