Disentangling the complex gene interaction networks between rice and the blast fungus identifies a new pathogen effector

Sugihara, Yu, Abe, Yoshiko, Takagi, Hiroki, Abe, Akira, Shimizu, Motoki, Ito, Kazue, Kanzaki, Eiko, Oikawa, Kaori, Kourelis, Jiorgos ORCID: https://orcid.org/0000-0002-9007-1333, Langner, Thorsten, Win, Joe, Białas, Aleksandra, Lüdke, Daniel, Contreras, Mauricio P., Chuma, Izumi, Saitoh, Hiromasa, Kobayashi, Michie, Zheng, Shuan, Tosa, Yukio, Banfield, Mark J., Kamoun, Sophien ORCID: https://orcid.org/0000-0002-0290-0315, Terauchi, Ryohei and Fujisaki, Koki (2023) Disentangling the complex gene interaction networks between rice and the blast fungus identifies a new pathogen effector. PLoS Biology, 21 (1). ISSN 1545-7885

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Abstract

Studies focused solely on single organisms can fail to identify the networks underlying host–pathogen gene-for-gene interactions. Here, we integrate genetic analyses of rice (Oryza sativa, host) and rice blast fungus (Magnaporthe oryzae, pathogen) and uncover a new pathogen recognition specificity of the rice nucleotide-binding domain and leucine-rich repeat protein (NLR) immune receptor Pik, which mediates resistance to M. oryzae expressing the avirulence effector gene AVR-Pik. Rice Piks-1, encoded by an allele of Pik-1, recognizes a previously unidentified effector encoded by the M. oryzae avirulence gene AVR-Mgk1, which is found on a mini-chromosome. AVR-Mgk1 has no sequence similarity to known AVR-Pik effectors and is prone to deletion from the mini-chromosome mediated by repeated Inago2 retrotransposon sequences. AVR-Mgk1 is detected by Piks-1 and by other Pik-1 alleles known to recognize AVR-Pik effectors; recognition is mediated by AVR-Mgk1 binding to the integrated heavy metal-associated (HMA) domain of Piks-1 and other Pik-1 alleles. Our findings highlight how complex gene-for-gene interaction networks can be disentangled by applying forward genetics approaches simultaneously to the host and pathogen. We demonstrate dynamic coevolution between an NLR integrated domain and multiple families of effector proteins.

Item Type: Article
Additional Information: Funding Information: This study was supported by JSPS KAKENHI 15H05779, 20H05681 to RT, the Royal Society UK-Japan International exchange grants JPJSBP120215702 to RT and the Royal Society UK-Japan International exchange grants IEC\R3 \203081 to SK and MB, the Gatsby Charitable Foundation (https://www.gatsby.org.uk/), the UK Research and Innovation Biotechnology and Biological Sciences Research Council (UKRIBBSRC) grants BB/P012574, BBS/E/J/000PR9797, BBS/E/J/000PR9798 BB/R01356X/1 to SK, and the European Research Council (ERC) BLASTOFF grant 743165 to SK. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Data Availability: All the sequence data used in this study was deposited at European Nucleotide Archive (ENA, https://www.ebi.ac.uk/ena/browser/home) and the DNA Data Bank of Japan (DDBJ, https://www.ddbj.nig.ac.jp/index-e.html) with the study accessions PRJEB53625 and PRJDB13864, respectively. The datasets used in this study are available at Github repository (https://github.com/YuSugihara/Sugihara_et_al_2022) archived in Zenodo (https://doi.org/10.5281/zenodo.7317319).
Uncontrolled Keywords: neuroscience(all),biochemistry, genetics and molecular biology(all),immunology and microbiology(all),agricultural and biological sciences(all) ,/dk/atira/pure/subjectarea/asjc/2800
Faculty \ School: Faculty of Science > The Sainsbury Laboratory
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: 20 Feb 2023 15:30
Last Modified: 30 Jan 2024 03:32
URI: https://ueaeprints.uea.ac.uk/id/eprint/91208
DOI: 10.1371/journal.pbio.3001945

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