Ancient pangenomic origins of noncanonical NLR genes underlying the recent evolutionary rescue of a staple crop
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Abstract
The recent adaptation of the cereal crop sorghum to a global aphid outbreak was a fortuitous case of evolutionary rescue, but the pangenomic and molecular basis is not known. We show that RMES1 disrupts phloem feeding via activation of conserved immunity networks, with a growth-to-defense transition mediated by phytohormone signaling and activated by nucleotide-binding site–leucine-rich repeat receptor (NLR) resistance genes on a structural variant. The causative NLRs [resistance to Melanaphis sorghi 1A (RMES1A) and RMES1B] lack signaling domains and have adenosine triphosphatase mutations expected to abrogate function, suggesting that RMES1 NLRs regulate immunity via a noncanonical mechanism. The RMES1 NLR family is ancient, orthologous to phloem-feeding resistance genes in rice and syntenic across the grass superpangenome. Thus, gene birth-and-death processes at an ancient gene cluster created rare standing variation and provided the adaptive allele for evolutionary rescue.
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Sorghum Growth and Development
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Regulation of dhurrin pathway gene expression during Sorghum bicolor development
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Animal NLRs continue to inform plant NLR structure and function
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Seedling growth and fall armyworm feeding preference influenced by dhurrin production in sorghum
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Proteome-wide structural analysis quantifies structural conservation across distant speciesPreprint
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Self-citationHow variable are rates of colonisation
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A sorghum pangenome reference improves global crop trait discovery
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Self-citationFrom structural pangenomes to functional panomics in plants
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Self-citationGenomic structural variation rescues a classic biological invader from a population bottleneck
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Domain-less defenders: evolutionary innovations and agricultural promise of noncanonical NLRs
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Two atypical resistance proteins confer plant resistance to Melanaphis sorghi in sorghum
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Pangenomics and machine learning reveal genetic variation to optimize carotenoids in sorghum grainPreprint
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- Authors
- VanGessel, C. J., Felderhoff, T. J., Prigozhin, D. M., Cui, M., Pressoir, G., Healey, A. L., Lovell, J. T., Nalam, V. J., Nishimura, M. T., & Morris, G. P.
- Affiliations
- Colorado State University (US)
- Kansas State University (US)
- Lawrence Berkeley National Laboratory (US)
- CHIBAS, Centre Haitien d’Innovation en Biotechnologies pour une Agriculture Soutenable, #13 Rue EDH Lathan, Croix des Bouquets, Haiti.
- HudsonAlpha Institute for Biotechnology (US)
- Corresponding author
- Morris, Geoffrey P.
- ORCID
- Venue
- Science Advances
- Published
- 2025-10-10
- Volume
- 11
- Issue
- 41
- Pages
- eady1667-eady1667
- ISSN
- 2375-2548 (ISSN-L)
- PMC
- PMC12513424
- OpenAlex
- W4415035297
- Cited by
- 10
- References
- 108
- Citations by year
- 2026: 10
- FWCI
- 5.37
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Science Advances (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- Funders
- United States Agency for International Development (AIDOAALA1600003)
- Bill and Melinda Gates Foundation (INV-053669, INV-009319)
- Joint Genome Institute
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
- Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Keywords
- sorghum, evolutionary rescue, aphid outbreaks, Melanaphis sorghi, phloem feeding, plant immunity, structural variants, gene birth and death, gene family evolution, plant hormone signaling, pan-genome, rice, standing genetic variation
- MeSH terms
- NLR Proteins, Animals, Aphids, Phylogeny, Plant Diseases, Plant Proteins, Crops, Agricultural, Evolution, Molecular, Sorghum, Disease Resistance
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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