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Background  Proteins with nucleotide binding site (NBS) and leucine-rich repeat (LRR) domains (NLR) make up one of most important resistance (R) families for plants to resist attacks from various pathogens and pests. The available transcriptomes of limber pine ( Pinus flexilis ) allow us to characterize NLR genes and related resistance gene analogs (RGAs) in host resistance against  Cronartium ribicola,  the causal fungal pathogen of white pine blister rust (WPBR) on five-needle pines throughout the world. We previously mapped a limber pine major gene locus ( Cr4 ) that confers complete resistance to  C. ribicola  on the  Pinus  consensus linkage group 8 (LG-8). However, genetic distribution of NLR genes as well as their divergence between resistant and susceptible alleles are still unknown.    Results  To identify NLR genes at the  Cr4  locus, the present study re-sequenced a total of 480 RGAs using targeted sequencing in a  Cr4 -segregated seed family. Following a call of single nucleotide polymorphisms (SNPs) and genetic mapping, a total of 541 SNPs from 155 genes were mapped across 12 LGs. Three putative NLR genes were newly mapped in the  Cr4  region, including one that co-segregated with  Cr4 . The tight linkage of NLRs with  Cr4 -controlled phenotypes was further confirmed by bulked segregation analysis (BSA) using extreme-phenotype genome-wide association study (XP-GWAS) for significance test. Local tandem duplication in the  Cr4  region was further supported by syntenic analysis using the sugar pine genome sequence. Significant gene divergences have been observed in the NLR family, revealing that diversifying selection pressures are relatively higher in local duplicated genes. Most genes showed similar expression patterns at low levels, but some were affected by genetic background related to disease resistance. Evidence from fine genetic dissection, evolutionary analysis, and expression profiling suggests that two NLR genes are the most promising candidates for  Cr4  against WPBR.    Conclusion  This study provides fundamental insights into genetic architecture of the  Cr4  locus as well as a set of NLR variants for marker-assisted selection in limber pine breeding. Novel NLR genes were identified at the  Cr4  locus and the  Cr4  candidates will aid deployment of this R gene in combination with other major/minor genes in the limber pine breeding program.    Supplementary Information  The online version contains supplementary material available at 10.1186/s12864-021-07885-8.

Fine dissection of limber pine resistance to Cronartium ribicola using targeted sequencing of the NLR family