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A Study of the Green Leaf Volatile Biochemical Pathway As a Source of Important Flavour and Aroma Precursors in Sauvignon Blanc Grape Berries

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A Study of the Green Leaf Volatile Biochemical Pathway As a Source of Important Flavour and Aroma Precursors in Sauvignon Blanc Grape Berries Lincoln University Digital Thesis Copyright Statement The digital copy of this thesis is protected by the Copyright Act 1994 (New Zealand). This thesis may be consulted by you, provided you comply with the provisions of the Act and the following conditions of use: you will use the copy only for the purposes of research or private study you will recognise the author's right to be identified as the author of the thesis and due acknowledgement will be made to the author where appropriate you will obtain the author's permission before publishing any material from the thesis. A Study of the Green Leaf Volatile Biochemical Pathway as a Source of Important Flavour and Aroma Precursors in Sauvignon Blanc Grape Berries A thesis submitted in partial fulfilment of the requirements for the Degree of Doctor of Philosophy at Lincoln University by Andriy Podolyan Lincoln University 2010 Abstract of a thesis submitted in partial fulfilment of the requirements for the Degree of Doctor of Philosophy Abstract A Study of the Green Leaf Volatile Biochemical Pathway as a Source of Precursors of Important Aroma Compounds in Sauvignon Blanc Grape Berries by Andriy Podolyan Green leaf volatiles (GLVs) are short-chain acylic aldehydes, alcohols and esters produced by plants via enzymatic metabolism of polyunsaturated fatty acids (PUFAs). GLVs are known to affect flavour and aroma of fruits and vegetables, including grapes. It has also been suggested that C6 and C5 GLVs are the precursors of volatile thiols, the aroma compounds that are important in Sauvignon blanc wine. GLVs are produced during grape berry development and released in high quantities upon berry crush. GLV aldehydes are formed from PUFAs by the action of two enzymes, lipoxygenase (LOX) and hydroperoxide lyase (HPL). This biochemical pathway is well characterised in other plant species and is known as the GLV pathway. To date, the GLV pathway has not been characterised in grapes. This thesis focuses on identification and initial characterisation of LOX and HPL genes and enzymes involved in the GLV-pathway. LOXs are a group of non-haem iron-containing dioxygenases that catalyse oxygenation of PUFAs producing PUFA-hydroperoxides. The most common PUFA substrates in plants are linoleic acid (LA, 18:2) and α-linolenic acid (LnA, 18:3). Depending on the position of oxygenation of the 18-carbon chain PUFAs, all plant LOXs are classified as 13(S) - and 9(S)-LOXs. 13(S)-LOXs are further regarded as type II and type I enzymes, depending on the presence or absence of transit peptides in the amino acid sequences of these enzymes respectively. ii HPLs belong to the CYP74 enzyme family, which is represented by atypical members of cytochrome P450 oxidases superfamily. HPLs cleave PUFA-hydroperoxides, producing aldehydes and oxoacids. Depending on the substrate specificity, HPLs are classified as 13-HPLs, 9/13-HPLs or 9-HPLs. The research reveals the complexity of the genetic makeup of the GLV metabolic pathway in grapes. Eighteen putative LOX genes and six putative HPL genes were identified in the Pinot noir grape genome. Phylogenetic analysis of the identified grape LOXs classified them as members of two groups, type II 13-LOXs and 9-LOXs, whereas all identified grape HPLs were classified as 13-HPLs (CYP-74B) and 9/13- HPLs (CYP-74C). Several LOX and HPL genes were expressed at different levels in Sauvignon blanc berry. Study of selected LOX and HPL gene expression revealed different levels of expression and differential tissue distribution of individual LOX and HPL genes within the berry. The studied genes also displayed different patterns of expression across different stages of berry development, upon wounding and in berries infected with Botrytis cinerea. Amongst the four LOX gene studied, transcripts of VvLOXA were the most abundant at all stages during berry development. VvLOXO was induced transiently upon berry damage and was a clear candidate involved in berry response to wounding. Expression levels of VvLOXC and VvLOXO were significantly increased in berries infected with Botrytis cinerea compared to the uninfected berries. In vitro biochemical analysis of the reaction products of recombinant VvLOXA (LOXA-TP) and VvLOXO (LOXO-TP) confirmed that these two enzymes are 13- LOXs. Both enzymes preferred LnA as a substrate. Both enzymes had the same temperature optima of 25°C, but preferred different pH conditions. Recombinant LOXA-TP preferred acidic environment and had pH optimum of pH 5.5, while LOXO- TP preferred neutral-to-basic conditions and had pH optimum of pH 7.5. Preliminary experiments with recombinant VvHPLA showed its ability to metabolise 13(S)-hydroperoxides, releasing C6 volatile aldehydes. Recombinant VvHPLA exhibited maximum activity with 13(S)-hydroperoxides of LnA as substrate at pH 5.0. Keywords: grapevine, Vitis vinifera, Sauvignon blanc, aroma compounds, volatile thiols, green leaf volatiles, lipoxygenase, hydroperoxide lyase, PUFA metabolism, plant defence response, plant wounding, grape berry development iv Note in Proof Some aspects of this thesis have been published in: Podolyan A, White J, Jordan B, Winefield C. (2010). Identification of the lipoxygenase gene family from Vitis vinifera and biochemical characterisation of two 13- lipoxygenases expressed in grape berries of Sauvignon Blanc. Functional Plant Biology, 37(8), 767-784. vi Acknowledgements First and foremost, I would like to thank my supervisors for giving me an opportunity to work on this project and for all their continuous support during these years. I am particularly thankful to Dr. Chris Winefield, who taught me the basics of molecular biology and later became my principle project supervisor. I would like to thank Prof. Brian Jordan for his support over the years as my associate supervisor. I am grateful to Chris and Brian for being approachable and always ready to discuss any aspects of the project. A special thankyou for their patient proofreading of my writing. Many thanks to Dr Mike Trought, who provided his help and advice on the viticultural aspects of this study. I thank New Zealand Foundation for Research, Science and Technology (contract number UOAX0404) for funding this project and paying my stipend. I also thank Lincoln University and specifically Agriculture and Life Sciences Division for providing facilities and additional funding during the years of study. I want to thank Pernod Ricard, New Zealand, for allowing me to collect berry samples from the Booker vineyard on the Brancott Estate. I also thank Marlborough Wine Research Staff for their help in sample collection. There are numerous people at Lincoln University and outside, whom I have had the privilege to work and interact with during these years. Their contribution has been invaluable, and has enabled me to complete this body of work. A special thankyou goes to Jackie White for managing the lab and helping me with the sample preparations. I thank Jenny Zhao and Rosy Tung for their assistance in HPLC analysis and Jason Breitmeyer for his help with GC-MS analysis. I would also like to thank my friends and colleagues for support and friendship I needed. My special thanks go to all my family for their invaluable contribution. I am immensely grateful to my wife Anastasija, who always inspired me and helped me to get through all the challenges and emotional struggles during this time. I am eternally indebted to my parents, who raised and educated me. They have made me the person I am today, and this is I am most grateful for. I also thank everyone who contributed to the completion of this project and who was not mentioned here. viii Table of Contents Abstract .......................................................................................................................... ii Note in Proof ................................................................................................................. vi Acknowledgements .................................................................................................... viii Table of Contents .......................................................................................................... x List of Tables ............................................................................................................ xviii List of Figures .............................................................................................................. xx Acronyms .................................................................................................................. xxiv Chapter 1 Introduction ................................................................................................ 1 Chapter 2 Literature review ........................................................................................ 3 2.1 Flavour and aroma compounds in Sauvignon blanc wine ..................................... 3 2.2 Precursors of the volatile thiols in Sauvignon blanc berries ................................. 6 2.2.1 Formation of volatile thiols from cysteinylated precursors ....................... 6 2.2.2 Alternative precursors of volatile thiols .................................................... 9 2.3 Green leaf volatiles (GLVs) ................................................................................ 11 2.4 Lipoxygenases ..................................................................................................... 14 2.4.1 LOX protein structure .............................................................................. 15 2.4.2 Proposed catalytic mechanism
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