Mgaloblishvili, a grapevine variety from Georgia (Southern Caucasus), exhibits a unique resistance mechanism against downy mildew. Mgaloblishvili resistance mechanism, involving pathogen recognition, activation of ethylene signalling pathway, and structural and chemical defences, is mediated by the resistance loci Rpv29, Rpv30, and Rpv31. Mgaloblishvili genome was sequenced using PacBio HiFi, resulting in a chromosome-scale diploid assembly of 986 Mbp, including 58 912 predicted protein-coding genes across two phased chromosome sets. Comparative analysis with the susceptible PN40024 genome allowed us to identify differences in structure, gene content, and gene expression, as well as the impact of structural variants (SVs) and single nucleotide polymorphisms (SNPs) between Mgaloblishvili and PN40024 loci. Resistance haplotypes were identified through DNA sequencing of a self-pollinated Mgaloblishvili population. Compared to orthologous regions in PN40024, the Rpv29 locus in Mgaloblishvili exhibits reduced gene content, while the Rpv31 locus has similar gene content. In both Mgaloblishvili and PN40024, most genes within these loci are associated with plant defence pathways. While genes in both genotypes perform similar functions, SVs and SNPs were identified as key determinants of the structural differences between the genomes. Defining the Rpv30 locus was challenging due to ambiguous marker localization. DNA sequencing allowed us to identify resistance haplotypes for both Rpv30 and Rpv31 on Mgaloblishvili haplotype 2, though insights into the Rpv29 locus remain limited. Our results indicate that Mgaloblishvili’s resistance is driven by numerous small SVs and SNPs, which lead to the loss of susceptibility factors and unique transcriptional regulation of defence-related genes.

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