Molecular and biochemical basis of interspecific variations in the organ-specific synthesis of floral terpenes between the domesticated cultivars and their wild relatives in Chrysanthemum.

Terpenoids, as the main components of the floral scent, exhibit interspecific variations and spatial specificity in Chrysanthemum genus. Here, we selected two primary species as the ancestors of C. morifolium along with two classic cultivars to investigate the influence of domestication on the variations in emission and production of floral terpenoids. The results indicated that the wild relatives emitted and accumulated higher levels of terpenoids in their disc florets and phyllaries & receptacles compared to the cultivars. Six gene modules associated with terpenoid production in three floral organs were characterized through WGCNA. Furthermore, 28 terpene synthase (TPS) genes were identified from both wild relatives and cultivars by comparative transcriptome database. In vitro enzymatic activity assay revealed that several products of monoterpenoids (α-pinene and α-terpinene) and sesquiterpenoids (β-farnesene, α-copaene and γ-curcumene), were commonly catalyzed by TPSs identified from wild relatives and cultivars. Nevertheless, we found that β-myrcene, β-elemene, β-cadinene and β-caryophyllene were predominantly produced by TPSs in the wild relatives, while d-limonene and β-copaene were specifically catalyzed by TPSs in the cultivars. It was also observed that the expression of the CiLSTPS3 gene could be associated with the emission and accumulation of β-caryophyllene in floral scent. Overall, the complex biochemical functions of TPSs, along with their varying expression patterns, significantly contribute to the interspecific variations of floral terpenoids in the Chrysanthemum genus. Our findings provide new insights into the molecular and biochemical mechanisms underlying the impact of domestication on the production of floral terpenoids in Chrysanthemum.