A root-specific NLR network mediates immune signaling of resistance genes against plant parasitic nematodes
Plant nucleotide-binding domain and leucine-rich repeat immune receptors (NLRs) confer disease resistance to many foliar and root parasites. However, the extent to which NLR-mediated immunity is differentially regulated between plant organs is poorly known. Here, we show that a large cluster of tomato (Solanum lycopersicum) genes, encoding the cyst and root-knot nematode disease resistance proteins Hero and MeR1 as well as the NLR helper NLR required for cell death 6 (NRC6), is nearly exclusively expressed in the roots. This root-specific gene cluster emerged in Solanum species about 21 million years ago through gene duplication of the ancient asterid NRC network. NLR sensors in this gene cluster function exclusively through NRC6 helpers to trigger hypersensitive cell death. These findings indicate that the NRC6 gene cluster has sub-functionalized from the larger NRC network to specialize in mediating resistance against root pathogens, including cyst and root-knot nematodes. We propose that some NLR gene clusters and networks may have evolved organ-specific gene expression as an adaptation to particular parasites and to reduce the risk of autoimmunity.
Authors
- Hiroaki Adachi (ORCID: https://orcid.org/0000-0002-7184-744X)
- Bozeng Tang (ORCID: https://orcid.org/0000-0002-3986-9622)
- Adriaan Verhage (ORCID: https://orcid.org/0009-0003-0416-9030)
- Sophien Kamoun (ORCID: https://orcid.org/0000-0002-0290-0315)
- Raoul Frijters (ORCID: https://orcid.org/0009-0006-6520-9552)
- Martin W. Ganal (ORCID: https://orcid.org/0000-0002-6649-8441)
- Adeline Harant (ORCID: https://orcid.org/0000-0001-7636-4917)
- AmirAli Toghani (ORCID: https://orcid.org/0000-0002-0644-699X)
- Toshiyuki Sakai (ORCID: https://orcid.org/0000-0003-2737-3299)
- Hsuan Pai (ORCID: https://orcid.org/0000-0002-7284-6131)
- Karin Ernst (ORCID: https://orcid.org/0009-0002-7254-1749)
- Daniel Lüdke (ORCID: https://orcid.org/0000-0002-0064-0695)
- Jiorgos Kourelis (ORCID: https://orcid.org/0000-0002-9007-1333)
- Chih‐Hang Wu (ORCID: https://orcid.org/0000-0003-1616-1872)
- Andrés Posbeyikian (ORCID: https://orcid.org/0000-0002-9368-6659)
- Juan Carlos Lopez‐Agudelo (ORCID: https://orcid.org/0009-0000-2152-3853)
Institutions
- University of East Anglia (GB)
- Kyoto University (JP)
- Sainsbury Laboratory (GB)
- Rijk Zwaan (Netherlands) (NL)
- Institute of Plant and Microbial Biology, Academia Sinica (TW)
- SGS Institut Fresenius (Germany) (DE)
- Heinrich Heine University Düsseldorf (DE)
Publication Details
- Journal
- The Plant Cell
- Published
- 2025-06-24
- DOI
- https://doi.org/10.1093/plcell/koaf145
- Citations
- 6
- Primary Topic
- Plant-Microbe Interactions and Immunity
- Type
- article
- Field-Weighted Citation Impact
- 10.50
Funders
- Gatsby Charitable Foundation
- Deutsche Forschungsgemeinschaft
- Academia Sinica
- National Science and Technology Council
- Directorate for Biological Sciences
- Biotechnology and Biological Sciences Research Council
- European Research Council
- Japan Science and Technology Agency
- Precursory Research for Embryonic Science and Technology