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Potato is considered a key component of the global food system and plays a vital role in strengthening world food security. A major constraint to potato production worldwide is the Potato Virus Y (PVY), belonging to the genus Potyvirus in the family of Potyviridae. Selective breeding of potato with resistance to PVY pathogens remains the best method to limit the impact of viral infections. Understanding the genetic diversity and population structure of potato germplasm is important for breeders to improve new cultivars for the sustainable use of genetic materials in potato breeding to PVY pathogens. While, genetic diversity improvement in modern potato breeding is facing increasingly narrow genetic basis and the decline of the genetic diversity. In this research, we performed genotyping-by-sequencing (GBS)-based diversity analysis on 10 commercial potato cultivars and weighted gene co-expression network analysis (WGCNA) to identify candidate genes related to PVY-resistance. WGCNA is a system biology technique that uses the WGCNA R software package to describe the correlation patterns between genes in multiple samples. In terms of consumption, these cultivars are a high rate among Iranian people. Using population structure analysis, the 10 cultivars were clustered into three groups based on the 118343 single nucleotide polymorphisms (SNPs) generated by GBS. Read depth ranged between 5 and 18. The average data size and Q30 of the reads were 145.98 Mb and 93.63%, respectively. Based on the WGCNA and gene expression analysis, the StDUF538, StGTF3C5, and StTMEM161A genes were associated with PVY resistance in the potato genome. Further, these three hub genes were significantly involved in defense mechanism where the StTMEM161A was involved in the regulation of alkalization apoplast, the StDUF538 was activated in the chloroplast degradation program, and the StGTF3C5 regulated the proteins increase related to defense in the PVY infected cells. In addition, in the genetic improvement programs, these hub genes can be used as genetic markers for screening commercial cultivars for PVY resistance. Our survey demonstrated that the combination of GBS-based genetic diversity germplasm analysis and WGCNA can assist breeders to select cultivars resistant to PVY as well as help design proper crossing schemes in potato breeding. [ABSTRACT FROM AUTHOR]