Dynamic regulation of volatile terpenoid production and emission from Chrysanthemum morifolium capitula.

ABSTRACT

Flower-associated communities consist of both mutualistic and antagonistic organisms. We have limited knowledge on how flowers regulate volatiles to balance their defense against antagonists and the attraction of beneficial organisms necessary for reproductive success. Asteraceae is the largest family among flowering plants. Its representatives are characterized by unique inflorescence called capitulum, which has been reduced to a reproduction unit resembling a single flower. Here, we chose Chrysanthemum morifolium, a model species of Asteraceae, to investigate how the capitulum balances the accumulation and emission of floral terpenoid volatiles that are implicated in defense and pollinator attraction, respectively. Our results showed that the capitula of C. morifolium produce and emit complex mixtures of monoterpenoids and sesquiterpenoids. The highest concentrations of terpenoids were detected in the bud stage of the capitula. In contrast, the capitulum reached the highest emission level prior to full blooming. The disc florets were the dominant organs of terpenoid accumulation and emission in the full-openness stage. To understand the molecular basis of volatile terpenoid biosynthesis in C. morifolium, experiments were designed to study terpene synthase (TPS) genes, which are pivotal for terpene biosynthesis. Eight CmCJTPS genes were identified in the transcriptomes of C. morifolium, and the proteins encoded by five genes were found to be biochemically functional. CmCJTPS5 and CmCJTPS8 were the multi-product enzymes catalyzing the monoterpenoid and sesquiterpenoid formation, which closely matched the major terpenoids produced in the flower heads. The five functional terpene synthase genes exhibited similar temporal expression patterns but diverse spatial expression levels, suggesting tissue-specific functions. Altogether, our results illustrate the dynamic patterns of accumulation and emission of floral volatile terpenoids implicated in defense and attracting pollinators in C. morifolium, for which both the regulation of TPS gene expression and the regulation of release may play critical roles.