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Maidment, Josephine H.R., Shimizu, Motoki, Bentham, Adam R., Vera, Sham, Franceschetti, Marina, Longya, Apinya, Stevenson, Clare E.M., De la Concepcion, Juan Carlos, Białas, Aleksandra, Kamoun, Sophien 
ORCID: https://orcid.org/0000-0002-0290-0315, Terauchi, Ryohei and Banfield, Mark J.
(2023)
Effector target-guided engineering of an integrated domain expands the disease resistance profile of a rice NLR immune receptor.
eLife, 12.
ISSN 2050-084X
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Abstract
A subset of plant intracellular NLR immune receptors detect effector proteins, secreted by phytopathogens to promote infection, through unconventional integrated domains which resemble the effector’s host targets. Direct binding of effectors to these integrated domains activates plant defenses. The rice NLR receptor Pik-1 binds the Magnaporthe oryzae effector AVR-Pik through an integrated heavy metal-associated (HMA) domain. However, the stealthy alleles AVR-PikC and AVR-PikF avoid interaction with Pik-HMA and evade host defenses. Here, we exploited knowledge of the biochemical interactions between AVR-Pik and its host target, OsHIPP19, to engineer novel Pik-1 variants that respond to AVR-PikC/F. First, we exchanged the HMA domain of Pikp-1 for OsHIPP19-HMA, demonstrating that effector targets can be incorporated into NLR receptors to provide novel recognition profiles. Second, we used the structure of OsHIPP19-HMA to guide the mutagenesis of Pikp-HMA to expand its recognition profile. We demonstrate that the extended recognition profiles of engineered Pikp-1 variants correlate with effector binding in planta and in vitro, and with the gain of new contacts across the effector/HMA interface. Crucially, transgenic rice producing the engineered Pikp-1 variants was resistant to blast fungus isolates carrying AVR-PikC or AVR-PikF. These results demonstrate that effector target-guided engineering of NLR receptors can provide new-to-nature disease resistance in crops.
| Item Type: | Article |
|---|---|
| Additional Information: | Data availability: All data generated or analysed during this study are included in the manuscript and supporting files. Funding Information: This work was supported by the UKRI Biotechnology and Biological Sciences Research Council (BBSRC) Norwich Research Park Biosciences Doctoral Training Partnership, UK [grant BB/M011216/1]; the UKRI BBSRC, UK [grants BB/P012574, BBS/E/J/000PR9795, BB/M02198X], the European Research Council [ERC; proposal 743165]; The Thailand Research Fund through The Royal Golden Jubilee Ph.D. Program [PHD/0152/2556]; the John Innes Foundation; the Gatsby Charitable Foundation; The British Society for Plant Pathology (undergraduate vacation bursary); JSPS KAKENHI 15H05779 and 20H05681; JSPS/The Royal Society Bilateral Research for the project 'Retooling rice immunity for resistance against rice blast disease' (2018–2019). We would also like to thank Julia Mundy and David Lawson from the JIC Biophysical Analysis and X-ray Crystallography platform for their support with protein crystallization and X-ray data collection, Andrew Davies and Phil Robinson from JIC Scientific Photography for their help with leaf imaging, Gerhard Saalbach and Carlo de Oliveira Martins from the JIC Proteomics platform for intact mass spectrometry analysis, and Dan Maclean from The Sainsbury Laboratory for support with statistical analyses. We also thank all members of the Banfield, Kamoun, and Terauchi groups for their discussions. |
| Uncontrolled Keywords: | nlr immune receptor,plant biology,plant immunity,protein engineering,rice blast disease,biochemistry, genetics and molecular biology(all),immunology and microbiology(all),neuroscience(all) ,/dk/atira/pure/subjectarea/asjc/1300 |
| Faculty \ School: | Faculty of Science > School of Biological Sciences |
| UEA Research Groups: | Faculty of Science > Research Groups > Plant Sciences |
| Related URLs: | |
| Depositing User: | LivePure Connector |
| Date Deposited: | 31 Oct 2024 15:30 |
| Last Modified: | 13 Nov 2024 09:30 |
| URI: | https://ueaeprints.uea.ac.uk/id/eprint/97383 |
| DOI: | 10.7554/eLife.81123 |
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