Heartwood-specific transcriptome and metabolite signatures of tropical sandalwood (Santalum album) reveal the final step of (Z)-santalol fragrance biosynthesis

J.M. Celedon, A. Chiang, M.M.S. Yuen, M.L. Diaz-Chavez, L.L. Madilao, Patrick M. Finnegan, Elizabeth L. Barbour, J. Bohlmann

    Research output: Contribution to journalArticle

    38 Citations (Scopus)

    Abstract

    © 2016 The Authors The Plant Journal © 2016 John Wiley & Sons Ltd

    Tropical sandalwood (Santalum album) produces one of the world's most highly prized fragrances, which is extracted from mature heartwood. However, in some places such as southern India, natural populations of this slow-growing tree are threatened by over-exploitation. Sandalwood oil contains four major and fragrance-defining sesquiterpenols: (Z)-a-santalol, (Z)-ß-santalol, (Z)-epi-ß-santalol and (Z)-a-exo-bergamotol. The first committed step in their biosynthesis is catalyzed by a multi-product santalene/bergamotene synthase. Sandalwood cytochromes P450 of the CYP76F sub-family were recently shown to hydroxylate santalenes and bergamotene; however, these enzymes produced mostly (E)-santalols and (E)-a-exo-bergamotol. We hypothesized that different santalene/bergamotene hydroxylases evolved in S. album to stereo-selectively produce (E)- or (Z)-sesquiterpenols, and that genes encoding (Z)-specific P450s contribute to sandalwood oil formation if co-expressed in the heartwood with upstream genes of sesquiterpene biosynthesis. This hypothesis was validated by the discovery of a heartwood-specific transcriptome signature for sesquiterpenoid biosynthesis, including highly expressed SaCYP736A167 transcripts. We characterized SaCYP736A167 as a multi-substrate P450, which stereo-selectively produces (Z)-a-santalol, (Z)-ß-santalol, (Z)-epi-ß-santalol and (Z)-a-exo-bergamotol, matching authentic sandalwood oil. This work completes the discovery of the biosynthetic enzymes of key components of sandalwood fragrance, and highlights the evolutionary diversification of stereo-selective P450s in sesquiterpenoid biosynthesis. Bioengineering of microbial systems using SaCYP736A167, combined with santalene/bergamotene synthase, has potential for development of alternative industrial production systems for sandalwood oil fragrances.

    Original languageEnglish
    Pages (from-to)289-299
    JournalThe Plant Journal
    Volume86
    Issue number4
    Early online date15 Apr 2016
    DOIs
    Publication statusPublished - May 2016

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