Integrative multi-omics analysis traces the divergent evolution of Chinese and Vietnamese Cinnamon and elucidates the biosynthetic pathway of cinnamaldehyde derivatives

Abstract Background Human interaction with plants reshapes genetic diversity across species and lineages, yet this process remains poorly understood in perennial woody plants cultivated for non-fruit products. Cinnamon, primarily derived from Cinnamomum cassia , represents a compelling subject to investigate how ecological adaptation and long-term cultivation have shaped its genomic diversity and driven variation in its key bioactive compounds, namely cinnamaldehyde and its derivatives. Results To investigate the divergence of Chinese cinnamon ( C. cassia var. cassia ) and Vietnamese cinnamon ( C. cassia var. macrophyllum ), we integrated a de novo genome assembly, whole-genome resequencing of 98 accessions, and metabolomic and transcriptomic profiling of multiple tissues of both varieties. Phylogenomic and demographic analyses revealed that the two varieties diverged prior to documented human utilization. Vietnamese cinnamon formed a basal lineage with high genetic diversity, whereas Chinese cinnamon exhibited reduced genetic diversity and weak population structure, likely resulting from prolonged intensive cultivation. Genome-wide selection scans indicated genes involved in phenylpropanoid biosynthesis were under divergent selection. Metabolomic and transcriptomic profiling uncovered differentiation in cinnamaldehyde derivatives across tissues and varieties and pinpointed candidate enzymes in their biosynthesis. Functional validation demonstrated that two O-methyltransferases, Ccas10G000326 and Ccas05G001459, effectively enhance the transformation of 2-hydroxycinnamaldehyde into 2-methoxycinnamaldehyde. Conclusions Our findings demonstrate that persistent cultivation of a limited gene pool diminishes genetic diversity in perennial trees, whereas lineages under lower utilization pressure preserve greater evolutionary potential. It highlights that conserving and integrating underutilized genetic resources is essential for the sustainable use and improvement of woody crops.