Genome Assembly and Winged Fruit Gene Regulation of Chinese Wingnut: Insights from Genomic and Transcriptomic Analyses

The genomic basis and biology of winged fruit are interesting issues in ecological and evolutionary biology. Chinese wingnut (Pterocarya stenoptera) is an important horticultural and economic tree species in China. The genomic resources of this hardwood tree could advance the genomic studies of Juglandaceae species and elucidate their evolutionary relationships. Here, we reported a high-quality reference genome of P. stenoptera (N50 = 35.15 Mb) and performed a comparative genomic analysis across Juglandaceae species. Paralogous relationships among the 16 chromosomes of P. stenoptera revealed eight main duplications representing the subgenomes. Molecular dating suggested that the most recent common ancestor of P. stenoptera and Cyclocarya paliurus diverged from Juglans species around 56.7 million years ago (MYA). The expanded and contracted gene families were associated with cutin, suberine, and wax biosynthesis, cytochrome P450, and anthocyanin biosynthesis. We identified large inversion blocks between P. stenoptera and its relatives, which were enriched with genes involved in lipid biosynthesis and metabolism, as well as starch and sucrose metabolism. Whole-genome resequencing of 28 individuals revealed clearly phylogenetic clustering into three groups corresponding to Pterocarya macroptera, Pterocarya hupehensis, and P. stenoptera. Morphological and transcriptomic analyses showed that CAD, COMT, LOX, and MADS-box play important roles during the five developmental stages of wingnuts. This study highlights the evolutionary history of the P. stenoptera genome and supports P. stenoptera as an appropriate Juglandaceae model for studying winged fruits. Our findings provide a theoretical basis for understanding the evolution, development, and diversity of winged fruits in woody plants.