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Background  Linkage of DNA markers with phenotypic traits provides essential information to dissect clustered genes with potential phenotypic contributions in a target genome region.  Pinus flexilis  E. James (limber pine) is a keystone five-needle pine species in mountain-top ecosystems of North America. White pine blister rust (WPBR), caused by a non-native fungal pathogen  Cronartium ribicola  (J.C. Fisch.), has resulted in mortality in this conifer species and is still spreading through the distribution. The objective of this research was to develop  P. flexilis  transcriptome-wide single nucleotide polymorphism (SNP) markers using RNA-seq analysis for genetic mapping of the major gene ( Cr4 ) that confers complete resistance to  C. ribicola .    Results  Needle tissues of one resistant and two susceptible seedling families were subjected to RNA-seq analysis.  In silico  SNP markers were uncovered by mapping the RNA-seq reads back to the  de novo  assembled transcriptomes. A total of 110,573  in silico  SNPs and 2,870 indels were identified with an average of 3.7 SNPs per Kb. These SNPs were distributed in 17,041 unigenes. Of these polymorphic  P. flexilis  unigenes, 6,584 were highly conserved as compared to the genome sequence of  P. taeda  L (loblolly pine). High-throughput genotyping arrays were designed and were used to search for  Cr4 -linked genic SNPs in megagametophyte populations of four maternal trees by haploid-segregation analysis. A total of 32 SNP markers in 25 genes were localized on the  Cr4  linkage group (LG). Syntenic relationships of this  Cr4 -LG map with the model conifer species  P. taeda  anchored  Cr4  on  Pinus  consensus LG8, indicating that R genes against  C. ribicola  have evolved independently in different five-needle pines. Functional genes close to  Cr4  were annotated and their potential roles in  Cr4 -mediated resistance were further discussed.    Conclusions  We demonstrated a very effective, low-cost strategy for developing a SNP genetic map of a phenotypic trait of interest. SNP discovery through transcriptome comparison was integrated with high-throughput genotyping of a small set of  in silico  SNPs. This strategy may be applied to mapping any trait in non-model plant species that have complex genomes. Whole transcriptome sequencing provides a powerful tool for SNP discovery in conifers and other species with complex genomes, for which sequencing and annotation of complex genomes is still challenging. The genic SNP map for the consensus  Cr4 -LG may help future molecular breeding efforts by enabling both  Cr4  positional characterization and selection of this gene against WPBR.    Electronic supplementary material  The online version of this article (doi:10.1186/s12864-016-3079-2) contains supplementary material, which is available to authorized users.

Genetic mapping of Pinus flexilis major gene (Cr4) for resistance to white pine blister rust using transcriptome-based SNP genotyping