Adaptive genomic signatures in PEBP genes reveal flowering plasticity and ecological specialization in Orchidaceae

Orchidaceae, representing approximately 10% of seed plant diversity, thrive across a wide range of ecosystems from rainforests to tundra. However, the genetic basis underlying this remarkable adaptability has remained elusive, largely due to the scarcity of chromosome-level orchid genomes. Here, we investigate the evolution of flowering strategies by analyzing central flowering regulators in the phosphatidylethanolamine-binding protein gene family across 27 representative orchid genomes. Our analyses reveal an extensive expansion of orchid FLOWERING LOCUS T-like genes through whole-genome, transposed, and tandem duplications, highlighting their central role in flowering control. In contrast, MOTHER OF FT AND TFL1-like and TERMINAL FLOWER 1-like genes primarily originate from transposed duplications and have been frequently lost. Using phylogenomic and synteny network analyses, we identify four FT clusters, including a canonical floral-induction cluster and another cluster harboring natural variants that attenuate flowering promotion, as demonstrated by transgenic analyses. Moreover, transposable element insertions within intronic and coding regions, together with transcript variants derived from SNPs, genomic structural variation, and lineage-specific insertions bearing novel MYB-binding motifs, collectively modulate the regulatory diversification and environmental adaptability of these genes. These multilayered genomic innovations underpin the evolution of flowering responses across ecological gradients, shedding light on orchid reproductive diversification and identifying promising targets for breeding.