Global Genetic Diversity, Provisional Strain Demarcation, and Evolutionary Dynamics of Potato Virus X (PVX)

Potato virus X (PVX) is an economically important pathogen of potato (Solanum tuberosum), causing global yield losses of 30-40% annually in single infections and up to 80% in mixed infections. To analyze genetic diversity and evolution, 413 full-length PVX isolates available in the databases were investigated. Pairwise nucleotide sequence identities using the Sequence Demarcation Tool (SDT) suggested a tentative, dataset-dependent species and strain demarcation threshold of 76% and 89%, respectively, delineating eleven (11) putative strains, named alphabetically from A to K. Phylogenetic analysis strongly supported the provisional strain demarcation, showing distinct and non-overlapping phylogenetic clusters. PVX-A constitutes a phylogenetically heterogeneous lineage, potentially contributing to its evolutionary success and long-term persistence. The PVX population exhibited high nucleotide and haplotype diversity, elevated gene flow and a moderate level of genetic differentiation among the geographically distinct clusters. Recombination analysis, using RDP, identified 20 recombination events involving 50 recombinant isolates, while the GARD program detected only a single breakpoint at position 6229 bp within the coat protein (CP) region. Recombination, alongside the nucleotide substitution rate and gene flow, was identified as a secondary evolutionary force driving PVX diversity. The Andean region was identified as the probable origin of PVX, from which it spread to Europe through early transcontinental human activities and subsequently disseminated across the world. The Andes and Europe likely represent two major evolutionary niches. PVX has a moderate host range, with potato as its prime natural host, and the majority of PVX genotypes infect only potato. Among all PVX genomic lineages, PVX-A shows the widest geographical distribution and host range, reported in almost every potato-growing country, including Pakistan. This study provides a comprehensive framework for understanding PVX diversity, provisional strain demarcation, evolution, and global dispersal, facilitating acquiring sustainable resistance and improving preventive strategies against PVX for global potato cultivation.