Hybridization Drives Trait Integration in Telomere-To-Telomere Apocynum Genomes

Hybridization drives plant adaptation, yet its genomic mechanisms in non-model perennials remain elusive. Apocynum species thrive in extreme saline-alkaline environments. This study establishes A. pictum (APZ) as a homoploid hybrid of A. venetum (AVX) and A. hendersonii (AHG), exemplifying hybrid-driven resilience. Leveraging telomere-to-telomere (T2T) genome assemblies of AVX, APZ, and AHG, we confirmed APZ's hybrid origin ~0.95 million years ago (Mya), following species divergence ~2.08 Mya, with AHG plastid inheritance. Nuclear and plastid analyses resolve taxonomic disputes among three Apocynum species. APZ exhibits large heterozygous inversions on chromosomes 3 and 8 with suppressed recombination, preserving AHG stress-tolerance haplotypes. The study also showed that allele-specific expression (ASE) dynamically regulates salt tolerance: AHG-biased stress MAPK signalling pathway prevails at 200 mM NaCl, shifting to AVX-bias at 400 mM NaCl, while flavonoid biosynthesis genes such as AvFLS and AvCHS5 consistently favour AVX alleles. Transgenic assays validate AVX-derived AvFLS for superior salt tolerance and ROS scavenging, with AvCHS5 diversification driven by tandem duplication dosage effects. Homoploid hybrid speciation (HHS) analysis indicates AvCHS5 and circadian LHY genes under positive selection enhance hybrid stability, supporting breeding potential. This study reveals how hybridization drives trait integration via dynamic ASE, identifying AvFLS, AvCHS5, and stress-responsive loci as breeding targets for stress-resilient, flavonoid-rich cultivars, offering a genomic foundation for crop improvement in extreme environments.