Genome variations reveal rapid adaptation to domestication and habitat changes in the brown algae Saccharina japonica

• The domestication of S. japonica in China occurred through two distinct phases, each characterized by different selection pressures and genetic responses. The first phase, from wild populations in Japan to northern China, involved intense selective pressure primarily on genes related to temperature and oxygen concentration adaptation, including SjHSP70 and SjLACS5 . In the subsequent phase from northern to southern China, selection focused on nutrient- and abscisic acid-related genes such as SjLACS4.1 , SjGST34 , SjGST35 , and SjGT8 . • Transcriptomic analysis revealed a strong correlation between blade length and width (major economic traits) and three key genes: SjTic20 , SjpeptidaseS8 , and SjpeptidaseS53 . Selective sweep analysis further identified significant selection signals at these loci • Utilizing population genomic data, this study provides the first evidence of genetic introgression from cultivated S. japonica into wild Japanese populations. This finding suggests that human cultivation activities may have caused unintended genetic disturbances in wild populations. • A high-quality genome assembly and annotation were achieved for the wild S. japonica strain (WSJ-1), which will provide a valuable resource for future comparative studies. Saccharina japonica , the first domesticated marine plant in global aquaculture, has been cultivated for nearly a century, adapting to diverse marine environments in China. This domestication has led to significant genetic changes, but the genomic mechanisms driving these adaptations remain unclear. Unraveling these mechanisms is critical for genetic improvement and conservation, especially in the face of environmental challenges. This study investigates the genomic changes and genetic variations underlying the domestication of S. japonica , focusing on its transition from wild populations in Japan to northern China and subsequent adaptation to southern China. Using the newly assembled nuclear genome of S. japonica (WSJ-1) as a reference, we analyzed genetic variations and selective sweeps across wild, northern, and southern populations. Key genes associated with environmental adaptation were identified, and genomic forces driving these adaptations were explored. Furthermore, transcriptome analyses and chemical content were performed to characterize the expression patterns of key economic traits linked to domestication. Our findings firstly examined genetic introgression from cultivars into Japanese wild populations. Stronger selection pressures were observed during the transition from wild to northern populations compared to northern-to-southern adaptations. Selective sweeps revealed genes like heat shock protein 70 and long-chain acyl-CoA synthetase involved in temperature and oxygen adaptation in northern populations. In southern populations, nutrient and abscisic acid-related genes were selected. Blade morphology genes exhibited distinct transcriptional patterns and positive selection, while alginate-related genes showed differential expression without strong selection signals. Additionally, GST gene clusters, potentially influenced by retro transposition events, were positively selected, contributing to stress responses and growth in S. japonica . Our findings unveil key genetic adaptations in the domestication of S. japonica , providing novel insights for its genetic improvement and conservation. These results are also crucial for sustaining seaweed cultivation under changing environments.