The genus Philodendron exhibits exceptional diversity and ornamental value, but the genetic and evolutionary mechanisms driving its speciation and trait variation remain largely unknown. In this study, we constructed a haplotype-resolved, near-complete genome of Philodendron tatei to investigate its evolutionary origins, resolve its phylogenomic placement within Araceae, reconstruct karyotype evolution, and explore genetic clusters and hybridization patterns within Philodendron cultivars. Additionally, the genetic and regulatory mechanisms underlying leaf color variation, a key horticultural trait, were explored. Phylogenomic analysis placed Philodendron within the Araceae family and provided insights into its karyotype evolution. Comparative genomic analyses identified five major genetic clusters across the genus, highlighting extensive hybridization and allele-specific expression as key contributors to Philodendron’s diversity. To investigate leaf color variation, variant mining and transcriptome profiling were conducted on samples with diverse pigmentation. Functional validation identified PtSGR1 as a critical regulator of pigmentation formation, with differences in promoter activity driving variation in leaf coloration. Overall, this study provides a comprehensive genomic framework for understanding Philodendron evolution and diversity, tracing the significant role of hybridization in shaping its speciation and identifying key genetic mechanisms underlying ornamental traits. These insights advance our understanding of plant evolution, contribute to horticultural innovation, and enhance the genetic resources available for studying this ecologically and economically important genus.

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