Multi-omics of the endangered Acer miaotaiense reveal nervonic acid biosynthesis, population evolution, and environmental adaptation.

Climate change threatens global forest biodiversity, particularly affecting long-lived, endangered tree species. However, the molecular mechanisms underlying their population evolution and environmental adaptation remain unclear. Here, we employed multi-omics analyses, including pan-genomes, transcriptomics, metabolomics, population genomics, and epigenomics, to decipher nervonic acid biosynthesis and population evolutionary history of the endangered tree Acer miaotaiense. A high-quality, chromosome-level genome of A. miaotaiense was first assembled (645.94 Mb). Pan-genome characterization showed that core genes and structural variation of seven Acer species were enriched in long-chain fatty acid metabolism. Metabolomic and transcriptomic analyses identified AmiaKCS7 and AmiaKCS9 as key regulators of nervonic acid biosynthesis. Population genomics demonstrated east-west divergence, with eastern populations showing elevated inbreeding and deleterious mutations. Especially, the eastern marginal populations represented priority conservation units under global warming due to their heightened genomic vulnerability. Landscape genomics revealed 747 candidate genes involved in local adaptation, particularly to temperature fluctuations and drought stress (eg heat shock protein 20 and major intrinsic protein). Integrated epigenomic analyses further confirmed transposon-associated methylation and lncRNAs modulated heat-responsive environmental adaptation. Our findings establish a foundational resource for understanding the adaptive evolution of A. miaotaiense and pinpoint critical genes and populations essential for its future conservation.