Biogenesis of flavor-related linalool is diverged and genetically conserved in tree peony (Paeonia × suffruticosa)

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Abstract
Floral scent is an important and genetically complex trait in horticultural plants. Tree peony (Paeonia × suffruticosa) originates in the Pan-Himalaya and have nine wild species divided into two subsections, Delavayanae and Vaginatae. Their flowers are beloved worldwide for their sweet floral fragrance, yet the flavor-related volatiles and underlying biosynthetic pathways remain unknown. Here, we characterized the volatile blends of all wild tree peony species and found that the flavor-related volatiles were highly divergent, but linalool was a unique monoterpene in subsect. Delavayanae. Further detection of volatiles in 97 cultivars with various genetic backgrounds showed that linalool was also the characteristic aroma component in P. delavayi hybrid progenies, suggesting that linalool was conserved and dominant within subsect. Delavayanae and its hybrids, instead of species and cultivars from subsect. Vaginatae. Global-transcriptome analysis of all wild tree peony species and 60 cultivars revealed five candidate genes that may be involved in key steps of linalool biosynthesis, especially the expressions of three TPS genes PdTPS1, PdTPS2 and PdTPS4 were significantly positively correlated with linalool emissions across tree peony cultivars. Further biochemical evidence demonstrated that PdTPS1 and PdTPS4 were the pivotal genes determining the species-specific and cultivar-specific emission of linalool. This study revealed a new insight into the floral scent divergence in tree peony and would greatly facilitate our understanding of phylogeny and evolution of Paeonia.

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