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, 224 (1), 367-379

Subsets of NLR Genes Show Differential Signatures of Adaptation During Colonization of New Habitats


Subsets of NLR Genes Show Differential Signatures of Adaptation During Colonization of New Habitats

Remco Stam et al. New Phytol.


Nucleotide binding site, leucine-rich repeat receptors (NLRs) are canonical resistance (R) genes in plants, fungi and animals, functioning as central (helper) and peripheral (sensor) genes in a signalling network. We investigate NLR evolution during the colonization of novel habitats in a model tomato species, Solanum chilense. We used R-gene enrichment sequencing to obtain polymorphism data at NLRs of 140 plants sampled across 14 populations covering the whole species range. We inferred the past demographic history of habitat colonization by resequencing whole genomes from three S. chilense plants from three key populations and performing approximate Bayesian computation using data from the 14 populations. Using these parameters, we simulated the genetic differentiation statistics distribution expected under neutral NLR evolution and identified small subsets of outlier NLRs exhibiting signatures of selection across populations. NLRs under selection between habitats are more often helper genes, whereas those showing signatures of adaptation in single populations are more often sensor-NLRs. Thus, centrality in the NLR network does not constrain NLR evolvability, and new mutations in central genes in the network are key for R-gene adaptation during colonization of different habitats.

Keywords: evolutionary genomics; network evolution; population genetics; resistance genes; tomato.

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Cited by 4 PubMed Central articles


    1. Andolfo G, Jupe F, Witek K, Etherington GJ, Ercolano MR, Jones JDG. 2014. Defining the full tomato NB-LRR resistance gene repertoire using genomic and cDNA RenSeq. BMC Plant Biology 14: e120.
    1. Ariga H, Katori T, Tsuchimatsu T, Hirase T, Tajima Y, Parker JE, Alcázar R, Koornneef M, Hoekenga O, Lipka AE et al. 2017. NLR locus-mediated trade-off between abiotic and biotic stress adaptation in Arabidopsis. Nature Plants 3: e17072.
    1. Arunyawat U, Stephan W, Städler T. 2007. Using multilocus sequence data to assess population structure, natural selection, and linkage disequilibrium in wild tomatoes. Molecular Biology and Evolution 24: 2310-2322.
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    1. Beaumont MA, Zhang WY, Balding DJ. 2002. Approximate Bayesian computation in population genetics. Genetics 162: 2025-2035.

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