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Peer-reviewedCC BYPLoS Genetics

Contrasting evolutionary patterns of helper and sensor NRC NLRs in lettuce reflect functional divergence following subfunctionalization

  • Hsuan Pai1
  • Toshiyuki Sakai2
  • Andrés Posbeyikian1
  • Raoul Frijters3
  • Yu Sugihara2,1
  • Mauricio P. Contreras1
  • Jiorgos Kourelis4
  • Hiroaki Adachi5,2
  • Sophien Kamoun1
  • AmirAli Toghani1
5 affiliations
  1. 1The Sainsbury Laboratory, University of East Anglia, Norwich Research Park, Norwich, United Kingdom
  2. 2Laboratory of Crop Evolution, Graduate School of Agriculture, Kyoto University, Kyoto, Japan
  3. 3Rijk Zwaan Breeding B.V., Department of Biotechnology, Fijnaart, The Netherlands
  4. 4Department of Life Sciences, Imperial College, London, United Kingdom
  5. 5JST-PRESTO, Saitama, Japan
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Abstract

Nucleotide-binding domain and leucine-rich repeat immune receptors (NLRs) are known for their rapid evolution, even at the intraspecific level, yet the rates of evolution differ significantly across NLRs. However, the degree to which evolutionary patterns reflect functional divergence remains poorly understood, notably in important crop species. Within the NRC (NLR Required for Cell Death) network in Asterids, sensor NLRs detect pathogen presence but require NRC helpers for signaling and to confer immunity. We conducted a comparative analysis of NLRs across 40 Solanales and 29 Asterales genomes to explore NRC network expansion and diversification within the less-studied Asterales order. Our findings reveal that the NRC network has expanded less in Asterales compared to Solanales. We functionally validated an Asterales NRC network with 2 helpers and 9 sensors in common lettuce (Lactuca sativa). Through selection analysis and structural modeling of NRC gene family in the Lactuca genus, we found distinct evolutionary trajectories between NRC helpers and sensors. Sensors reliant on the phylogenetically conserved helper NRC0 experience limited diversification, whereas sensors dependent on other NRC helpers show higher rates of positive selection and gene duplication. Our results highlight the lineage- and function-specific evolution of the NRC network, offering insights into the evolutionary pressures shaping plant immune receptor networks.

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Cite

BibTeXRIS
BibTeX
@article{pai2026contrasting,
  title = {{Contrasting evolutionary patterns of helper and sensor NRC NLRs in lettuce reflect functional divergence following subfunctionalization}},
  author = {Hsuan Pai and Toshiyuki Sakai and Andrés Posbeyikian and Raoul Frijters and Yu Sugihara and Mauricio P. Contreras and Jiorgos Kourelis and Hiroaki Adachi and Sophien Kamoun and AmirAli Toghani},
  journal = {PLoS Genetics},
  year = {2026},
  month = jul,
  doi = {10.1371/journal.pgen.1012245},
  url = {https://doi.org/10.1371/journal.pgen.1012245},
  note = {CC BY},
}
RIS
TY  - JOUR
TI  - Contrasting evolutionary patterns of helper and sensor NRC NLRs in lettuce reflect functional divergence following subfunctionalization
AU  - Hsuan Pai
AU  - Toshiyuki Sakai
AU  - Andrés Posbeyikian
AU  - Raoul Frijters
AU  - Yu Sugihara
AU  - Mauricio P. Contreras
AU  - Jiorgos Kourelis
AU  - Hiroaki Adachi
AU  - Sophien Kamoun
AU  - AmirAli Toghani
PY  - 2026
DA  - 2026/07/16
JO  - PLoS Genetics
DO  - 10.1371/journal.pgen.1012245
UR  - https://doi.org/10.1371/journal.pgen.1012245
AB  - Nucleotide-binding domain and leucine-rich repeat immune receptors (NLRs) are known for their rapid evolution, even at the intraspecific level, yet the rates of evolution differ significantly across NLRs. However, the degree to which evolutionary patterns reflect functional divergence remains poorly understood, notably in important crop species. Within the NRC (NLR Required for Cell Death) network in Asterids, sensor NLRs detect pathogen presence but require NRC helpers for signaling and to confer immunity. We conducted a comparative analysis of NLRs across 40 Solanales and 29 Asterales genomes to explore NRC network expansion and diversification within the less-studied Asterales order. Our findings reveal that the NRC network has expanded less in Asterales compared to Solanales. We functionally validated an Asterales NRC network with 2 helpers and 9 sensors in common lettuce (Lactuca sativa). Through selection analysis and structural modeling of NRC gene family in the Lactuca genus, we found distinct evolutionary trajectories between NRC helpers and sensors. Sensors reliant on the phylogenetically conserved helper NRC0 experience limited diversification, whereas sensors dependent on other NRC helpers show higher rates of positive selection and gene duplication. Our results highlight the lineage- and function-specific evolution of the NRC network, offering insights into the evolutionary pressures shaping plant immune receptor networks.
SN  - 1553-7390
SN  - 1553-7404
ER  -