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  A BAHD acyltransferase catalyzing 19-O-acetylation of tabersonine derivatives in roots of Catharanthus roseus enables combinatorial synthesis of monoterpene indole alkaloids

Carqueijeiro, I., de Bernonville, T. D., Lanoue, A., Dang, T.-T., Teijaro, C., Paetz, C., et al. (2018). A BAHD acyltransferase catalyzing 19-O-acetylation of tabersonine derivatives in roots of Catharanthus roseus enables combinatorial synthesis of monoterpene indole alkaloids. The Plant Journal, 49(3), 469-484. doi:10.1111/tpj.13868.

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 Creators:
Carqueijeiro, Inês, Author
de Bernonville, Thomas Dugé, Author
Lanoue, Arnaud, Author
Dang, Thu-Thuy, Author
Teijaro, Christiana, Author
Paetz, Christian1, Author              
Billet, Kevin, Author
Mosquera, Angela, Author
Oudin, Audrey, Author
Besseau, Sébastien, Author
Papon, Nicolas, Author
Glévarec, Gaëlle, Author
Atehortùa, Lucia, Author
Clastre, Marc, Author
Giglioli-Guivarc'h, Nathalie, Author
Schneider, Bernd1, Author              
St-Pierre, Benoit, Author
Andrade, Rodrigo B., Author
O’Connor, Sarah E.2, Author              
Courdavault, Vincent, Author
Affiliations:
1Research Group Biosynthesis / NMR, MPI for Chemical Ecology, Max Planck Society, ou_421898              
2External Organizations, ou_persistent22              

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 Abstract: While the characterization of the biosynthetic pathway of monoterpene indole alkaloids (MIAs) in leaves of Catharanthus roseus is now reaching completion, only two enzymes from the root counterpart dedicated to tabersonine metabolism have been identified to date, namely tabersonine 19-hydroxylase (T19H) and minovincine 19-O-acetyltransferase (MAT). Albeit the recombinant MAT catalyzes MIA acetylation at low efficiency in vitro, we demonstrated that MAT was inactive when expressed in yeast and in planta, suggesting an alternative function for this enzyme. Therefore, through transcriptomic analysis of periwinkle adventitious roots, several other BAHD acyltransferase candidates were identified based on the correlation of their expression profile with T19H and found to localize in small genomic clusters. Only one, named tabersonine derivative 19-O-acetyltransferase (TAT) was able to acetylate the 19-hydroxytabersonine derivatives from roots, such as minovincinine and hörhammericine, following expression in yeast. Kinetic studies also showed that the recombinant TAT was specific for root MIAs and displayed an up to 200-fold higher catalytic efficiency than MAT. In addition, gene expression analysis, protein subcellular localization and heterologous expression in Nicotiana benthamiana were in agreement with the prominent role of TAT in acetylation of root-specific MIAs, thereby redefining the molecular determinants of the root MIA biosynthetic pathway. Finally, identification of TAT provided a convenient tool for metabolic engineering of MIAs in yeast enabling efficiently mixing different biosynthetic modules spatially separated in the whole plant. This combinatorial synthesis associating several enzymes from Catharanthus roseus resulted in the conversion of tabersonine in tailor-made MIAs bearing both leaf and root-type decorations.

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 Dates: 2018-03-272018-042018-05
 Publication Status: Published in print
 Pages: -
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 Rev. Type: -
 Identifiers: Other: NMR249
DOI: 10.1111/tpj.13868
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Title: The Plant Journal
  Other : Plant J.
Source Genre: Journal
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Publ. Info: Oxford : Blackwell Science
Pages: - Volume / Issue: 49 (3) Sequence Number: - Start / End Page: 469 - 484 Identifier: ISSN: 0960-7412
CoNE: https://pure.mpg.de/cone/journals/resource/954925579095_1