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Role of Cytochromes P450 in Wine Aroma Tina Ilc

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Role of Cytochromes P450 in Wine Aroma Tina Ilc Role of cytochromes P450 in wine aroma Tina Ilc To cite this version: Tina Ilc. Role of cytochromes P450 in wine aroma. Vegetal Biology. Université de Strasbourg, 2015. English. NNT : 2015STRAJ083. tel-01394380 HAL Id: tel-01394380 https://tel.archives-ouvertes.fr/tel-01394380 Submitted on 9 Nov 2016 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. UNIVERSITÉ DE STRASBOURG École doctorale des sciences de la vie et de la santé Institut de Biologie Moléculaire des Plantes (CNRS) TH ÈSE présentée par : Tin a ILC soutenue le : 18 décembre 20 15 pour obtenir le grade de : Docteur de l’université de Strasbourg Discipline : Aspects moléculaires et cellulaires de la biologie Role of cytochromes P450 in wine aroma THÈSE dirigée par : Dr WERCK-REICHHART Danièle Directeur de recherche, CNRS, IBMP RAPPORTEURS : Prof BAUDINO Sylvie Professeur, Université de Lyon Saint-Étienne Prof WÜST Matthias Professeur, Universität Bonn EXAMINATEUR : Dr SCHALLER Hubert Directeur de recherche, CNRS, IBMP ii Table of Contents Acknowledgements ................................................................................................................. iv Preface ..................................................................................................................................... vi Résumé en français ............................................................................................................... viii Chapter 1 Meta-analysis of grape and wine aroma ............................................................................ 1 Chapter 2 Biosynthesis of terpenoids in plants ............................................................................... 32 Chapter 3 Cytochromes P450 ................................................................................................................ 35 Chapter 4 Plant monoterpenols: role and oxidative metabolism ............................................... 39 Chapter 5 Annotation, classification, genomic organization an d expression of the Vitis vinifera CYPo m e ................................................................................................................... 65 Chapter 6 CYP76F14 catalyzes biosynthesis of wine lactone pre cursor from linalool ......... 93 Chapter 7 Additional results ................................................................................................................ 135 Chapter 8 Conclusions and perspectives .......................................................................................... 159 Appendix I Expression of Vitis vinifera cytochrome P450 sequences ................................... 165 Appendix II DNA and protein sequence alignments of gene candidate s fo r (E)-8-carboxylinalool biosynthesi s ............................................................................. 177 iii Acknowledgements I would like to thank Daniele Werck for initiating this project and giving me the great opportunity to do my PhD thesis under her supervision. Thank you for your trust, for the opportunity to bring my own ideas to the project and for your continuous availability for discussion. I also wish to thank Nicolas Navrot for his day-to-day supervision, support and encouragement, as well as all of his help when I came to Strasbourg 3 years ago. I am grateful to Prof Sylvie Baudino, Prof Matthias Wüst and Dr Hubert Schaller for accepting to participate in my jury. This work would not be possible without strong collaborations. I am grateful to all the collaborators from INRA Colmar, for teaching me a lot about grape and aroma in particular, for the many useful discussions, as well as the practical help: Philippe Hugueney, Camille Rustenholz, Eric Duchene, Gautier Arista, Gisele Butterlin, Andrea Ilg and Marc Fischer. I want to thank Laurence Miesch and her team for synthesis of standards, as well as for many interesting discussions. I am also grateful to Raquel Tavares from University of Lyon for the collaboration on phylogeny. I am grateful to all the members of Marie Curie ITN “P4fifty”. It was a great pleasure to take part in this network and to get to know so many excellent scientists. In particular, I would like to thank everyone who welcomed me for one of my secondments: Fanny Lambert (Mane S.A.); Sabine Flitsch, Slavomira Husarova (University of Manchester), Bernhard Hauer, Stefan Hammer and Silke Bastian (University of Stuttgart). I also wish to thank my mentor Birger Lindberg Møller for many interesting discussions and useful guidelines. Special thanks also to Margaret Cafferky for administrating the network and being always available for help. I also thank the European Union for funding the “P4fifty” project. I want to thank the current and former colleagues from the “Cytochrome P450” team: Francois Bernier, Benoit Boachon, Carole Gavira, Thierry Heitz, Lucie Kriegshauser, Agnès Lesot, Rozenn Menard, Fabienne Philippon, Emmanuelle Pineau, Franck Pinot, Hugues Renault, Pascaline Ullman, Gaetan Verdier, and Emilie Widemann. Thank you all for your help, all the discussions, useful tips and challenging questions. My very special thanks go to Annette Alber, Claire Parage, Juliana Iglesias and Zhenhua Liu for always taking time for my scientific as well as “real-life” problems. I also wish to thank everyone from the Metabolomics platform (Dimitri Heintz, Julien Delecolle, Arnaud Agin, Maximilien Nuel, Julie Zumsteg and Raphael Lugan) and Gene expression platform (Malek Alioua) for your help and training. I want to thank my family for teaching me the importance of education in my mind from an early age. Thanks to my grandma for bringing me up to be so stubborn. I also want to thank iv my friends in Slovenia for not letting the distance come between us. Finally, a massive thank you to my big “Strasbourg family” who have supported me throughout this PhD and made Strasbourg my home. v Preface This work was part of the Marie Curie Initial Training Network “P4fifty”, the goal of which was the application of cytochrome P450 enzymes for white biotechnological processes. My principal role in this network was the discovery of P450 enzymes with novel functions. Wine is a rich source of chemically diverse aroma compounds, yet the underlying enzymes are largely unknown. The aim of this work is therefore to identify cytochromes P450 that synthesize aroma in grapes. These cytochromes P450 could be used for industrial production of flavor and fragrance compounds. In addition, grapevine is one of the most important crops in France and worldwide and aroma is of crucial importance for the quality of the final product. The knowledge of aroma biosynthetic pathways could thus also help to improve the quality of grapes and wines. This work was also supported by the funding of collaboration with the team of Dr Philippe Hugueney of the French National Institute for Agricultural Research (INRA) in Colmar by ANR (the French National Agency of Research). In the first part of my thesis, I review the current knowledge on wine aroma and its biosynthesis in the form of a meta-analysis of 19 published datasets of grape and wine aroma profiles. The objective of this work was to identify aroma compounds that are possibly synthesized in grapes by cytochromes P450. This reviewing and compiling study, presented here as Chapter 1 : Meta-analysis of grape and wine aroma (to be submitted to Journal of Agricultural and Food Chemistry), revealed an elaborate oxidative metabolism of the monoterpenol linalool, and convinced us to focus our efforts on biotransformations of this compound in grape and wine. After briefly introducing biosynthesis of terpenoids ( Chapter 2 ) and cytochromes P450 (Chapter 3 ), I review in detail recent progress in oxidations of monoterpenols by cytochromes P450 in Chapter 4 : Cytochrome P450-catalyzed oxidations of monoterpenols in plants (invited publication in Frontiers in Plant Science). In collaboration with the INRA group, we built an exhaustive and reliable annotation of cytochrome P450 genes in the reference grapevine genome. We then used this annotation to study the expression of these genes using publically available and INRA’s newly-generated transcriptomic data ( Chapter 5 : Annotation, classification, genomic organization and expression of the Vitis vinifera CYPome, to be submitted to BMC Genomics). This allowed us to identify several gene candidates for biosynthesis of aroma in grapes. In addition, it pointed to other cytochromes P450 of interest, involved for instance in the plant interactions with pathogens, and will provide the argument for future projects. The second part of the results and main experimental section addresses the formation of an important wine aroma compound, the wine lactone ( Chapter 6 : CYP76F14 catalyzes vi biosynthesis of wine lactone precursor from linalool, to be submitted to New Phytologist). I first show that this potent aroma is formed during wine ageing from a grapevine-derived precursor, ( E)-8-carboxylinalool. I then demonstrate that ( E)-8-carboxylinalool is synthesized from linalool by the grapevine cytochrome
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