Whole-genome resequencing of 495 Pyrus accessions provides insights into the genetics of agronomic traits and evolutionary history of pear

Abstract Pear (Pyrus L.) is a fruit tree of global commercial importance. Its genetic relationships, evolutionary history, dissemination routes, and genetic determinants of most agronomic traits remain to be elucidated. We conducted whole-genome resequencing of 495 Pyrus accessions. Phylogenetic and demographic analyses resolved geographic groupings of the accessions, identifying the Yunnan–Guizhou Plateau as the putative dissemination center for cultivated Pyrus pyrifolia and P. bretschneideri. Identification of two evolutionary bottlenecks provides insights into the population dynamics of pear species. Admixture and introgression analyses revealed both intraspecific and interspecific genetic exchanges, substantiating the complex emergence of cultivated populations. Genome-wide association study (GWAS) identified loci associated with nine crucial agronomic traits, together with eight candidate genes. The GWAS, molecular, and biochemical analyses suggested that PbeMADS25, PbeSPP, PbeDHQ-SDH, PbeARF2, PbePPO, PbePIN3, PbeCXE, and PbeMYB38 participate in the regulation of number of stigmas and number of locules, number of stamens, young leaf color, sepal persistence, astringency, acidity, aroma, and fruit skin color, respectively. Overexpression and metabonomic analysis of PbeCXE indicated that it affects the fruit aroma by affecting the balance between ester biosynthesis and substrate consumption. These findings expand our understanding of Pyrus evolution and provide a genomic foundation for genetic improvement of agronomic traits.