Gap-free genome-based analyses of the origin and adaptation of a globally invasive polyploid hydrophyte

Water hyacinth (Pontederia crassipes), an allotetraploid species, is among the most ecologically successful aquatic plants, exhibiting two remarkable adaptive traits: tristyly, a rare floral polymorphism promoting outcrossing, and inflated petioles (floats) that facilitate buoyancy. However, the genetic and evolutionary mechanisms underlying these traits in a polyploid context remain poorly understood. We assembled a gap-free telomere-to-telomere genome of an M-morph Po. crassipes and integrated whole-genome resequencing, transcriptomic, physiological, and anatomical analyses to investigate its genome evolution, floral polymorphism, and float formation. We detected multiple whole-genome duplication events in the Pontederia lineage. Po. crassipes originated via hybridization between two diploid progenitors and experienced nonreciprocal homoeologous exchanges. The M-morph is associated with a single hemizygous gene, LAZY1-M, and its characteristic long stamen filaments may result from cell elongation mediated by INCREASED LEAF INCLINATION (ILI) genes. By contrast, variation in style length between L- and M-morphs is primarily driven by differences in cell number. In addition, ethylene was identified as a key positive regulator of float formation. Our study provides a comprehensive analysis of the M-locus in a polyploid species, demonstrates its conserved evolutionary origin within Pontederiaceae, and uncovers novel regulatory mechanisms underlying morphological adaptation in aquatic plants.