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

Abstract

Floral scent is an important and genetically complex trait in horticultural plants. Tree peony (Paeonia × suffruticosa) originates in the Pan-Himalaya and has 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 Paeonia 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 floral scent divergence in tree peony and would greatly facilitate our understanding of the phylogeny and evolution of Paeonia.

Acknowledgements

This work was supported by the National Key R&D Program of China (grant no. 2018YFD1000400). We would like to thank Professor Lixia He (Gansu Forestry Science and Technology Extension Station), Professor Fangyun Cheng and Dr Yuan Zhong (Beijing Forestry University, China), and Engineer Peng Jiao (National Chinese Botanical Garden) for their kind help in offering us wild tree peony species and P. delavayi hybrids, respectively. We thank Dr Dandan Yin from the State Key Laboratory of Tree Genetics and Breeding, Chinese Academy of Forestry, for her excellent technical assistance in WES operation. We thank Dr Yan Zhu and Engineer Jingquan Li from the Plant Science Facility of the Institute of Botany, Chinese Academy of Sciences, for their assistance with GC–MS analysis and subcellular localization, respectively.

Author contributions

L.S.W. and S.S.L. conceived and designed the study. L.S.W. and W.Z.X. supervised the experiments and revised the manuscript. S.S.L. and L.Z. performed the experiments, analyzed the data, and wrote the manuscript. M.S. amplified the full-length sequences of genes. M.S. and M.W.L. helped with enzyme activity analysis. Y.Y. helped with material collection.

Data availability

All the sequence read data are deposited in the NCBI Sequence Read Archive (SRA) under accession number PRJNA827976.

Conflict of interest

The authors have no conflicts to declare.

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