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RESEARCH ARTICLE
Contents Vol 37(8)

Identification of the lipoxygenase gene family from Vitis vinifera and biochemical characterisation of two 13-lipoxygenases expressed in grape berries of Sauvignon Blanc

Andriy Podolyan A , Jackie White A , Brian Jordan A and Chris Winefield A B
+ Author Affiliations
- Author Affiliations

A Department of Wine, Food and Molecular Biosciences, Faculty of Agriculture and Life Sciences, Lincoln University, PO Box 84, Lincoln 7647, Canterbury, New Zealand.

B Corresponding author. Email: chris.winefield@lincoln.ac.nz

Functional Plant Biology 37(8) 767-784 https://doi.org/10.1071/FP09271
Submitted: 9 November 2009  Accepted: 12 April 2010   Published: 26 July 2010

Abstract

Lipoxygenases (LOXs) are a group of non-haem iron-containing dioxygenases that catalyse oxygenation of polyunsaturated fatty acids (PUFAs) and lipids, and initiate the formation of biologically active compounds known as oxylipins. Several plant oxylipins comprise important flavours and aromas in food and beverages. Analysis of the grape (Vitis vinifera L.) genome revealed that the grape LOX family consists of 18 individual members. Phylogenetic analysis places all except one of the identified grape LOXs into either a type II 13-LOX cluster or the type I 9-LOX cluster. Four LOX genes (VvLOXA, VvLOXO, VvLOXC, VvLOXD), representative of the major LOX groupings observed in the phylogenetic analyses, were selected for analysis of patterns of transcript abundance in berry tissues. VvLOXA and VvLOXO represent putative 13-LOXs, while VvLOXC represents a putative 9-LOX. VvLOXD represents a unique LOX that differs significantly from other characterised plant LOXs. All four LOXs exhibited a complex pattern of gene expression. Across all developmental stages, VvLOXA was the most abundant LOX and was expressed predominantly in berry skins. The expression pattern of VvLOXC and -D are more evenly distributed between seeds, pulp and skin, while VvLOXO is mostly expressed in the seed. Mechanical wounding and infection of berries with Botrytis cinerea Pers.: Fr resulted in rapid accumulation of VvLOXC and -O transcripts. VvLOXA expression decreased in diseased berries. Biochemical analysis of VvLOXA and -O recombinant proteins confirmed that these LOX genes encode functional 13-LOXs that exhibit different pH and temperature optima. Both enzymes showed activity with linoleic, linolenic and arachidonic acids.

Additional keywords: berry development, grapevine, green leaf volatiles, LOX, oxylipins, plant–pathogen interaction.


Acknowledgements

The authors thank Dr Mike Trought for his invaluable intellectual input into the viticultural aspects of this study. We also thank Pernod Ricard, New Zealand, for their generous use of commercial vines within the Booker vineyard on the Brancott estate for our field materials, and Marlborough Wine Research staff for help in sample collecting. This work was funded by the New Zealand Foundation for Research, Science and Technology, contract number UOAX0404.


References


Agrawal GK, Tamogami S, Han O, Iwahashi H, Rakwal R (2004) Rice octadecanoid pathway. Biochemical and Biophysical Research Communications 317(1), 1–15.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Axelrod B, Cheesborough TM, Laakso S (1981) Lipoxygenase from soybean. Methods in Enzymology 71, 441–451.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Bate NJ, Rothstein SJ (1998) C6-volatiles derived from the lipoxygenase pathway induce a subset of defense-related genes. The Plant Journal 16(5), 561–569.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Baumes R, Bayonove C, Barillère JM, Escudier JL, Cordonnier R (1988) La macération pelliculaire dans la vinification en blanc. Incidence sur la composante volatile des moûts. Connaissance de la Vigne et du Vin 32(3), 209–223. open url image1

Bell E, Creelman RA, Mullet JE (1995) A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 92(19), 8675–8679.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Bostock RM, Yamamoto H, Choi D, Ricker KE, Ward BL (1992) Rapid stimulation of 5-lipoxygenase activity in potato by the fungal elicitor arachidonic acid. Plant Physiology 100(3), 1448–1456.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Casey R, West SI, Hardy D, Robinson DS, Wu Z, Hughes RK (1999) New frontiers in food enzymology: recombinant lipoxygenases. Trends in Food Science & Technology 10(9), 297–302.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Chkaiban L, Botondi R, Bellincontro A, De Santis D, Kefalas P, Mencarelli F (2007) Influence of postharvest water stress on lipoxygenase and alcohol dehydrogenase activities, and on the composition of some volatile compounds of Gewürztraminer grapes dehydrated under controlled and uncontrolled thermohygrometric conditions. Australian Journal of Grape and Wine Research 13(3), 142–149.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Chong J, Le Henanff G, Bertsch C, Walter B (2008) Identification, expression analysis and characterization of defense and signaling genes in Vitis vinifera. Plant Physiology and Biochemistry 46(4), 469–481.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Clarke RJ , Bakker J (2004) ‘Wine flavour chemistry.’ (Blackwell Publishing: Oxford, UK)

Coffa G, Brash AR (2004) A single active site residue directs oxygenation stereospecificity in lipoxygenases: stereocontrol is linked to the position of oxygenation. Proceedings of the National Academy of Sciences of the United States of America 101(44), 15579–15584.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Coombe BG (1992) Research on development and ripening of the grape berry. American Journal of Enology and Viticulture 43(1), 101–110. open url image1

da Silva FG, Iandolino A, Al-Kayal F, Bohlmann MC, Cushman MA , et al . (2005) Characterizing the grape transcriptome. Analysis of expressed sequence tags from multiple Vitis species and development of a compendium of gene expression during berry development. Plant Physiology 139(2), 574–597.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Emanuelsson O, Nielsen H, von Heijne G (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Science 8(5), 978–984.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nature Protocols 2(4), 953–971.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Felsenstein J (1985) Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39, 783–791.
| Crossref |
open url image1

Feussner I, Wasternack C (2002) The lipoxygenase pathway. Annual Review of Plant Biology 53, 275–297.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Gao X, Stumpe M, Feussner I, Kolomiets M (2008) A novel plastidial lipoxygenase of maize (Zea mays) ZmLOX6 encodes for a fatty acid hydroperoxide lyase and is uniquely regulated by phytohormones and pathogen infection. Planta 227(2), 491–503.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Göbel C, Feussner I, Hamberg M, Rosahl S (2002) Oxylipin profiling in pathogen-infected potato leaves. Biochimica et Biophysica Acta (BBA) – Molecular and Cell Biology of Lipids 1584(1), 55–64.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Göbel C, Feussner I, Rosahl S (2003) Lipid peroxidation during the hypersensitive response in potato in the absence of 9-lipoxygenases. The Journal of Biological Chemistry 278(52), 52834–52840.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Hardie WJ, Aggenbach SJ, Jaudzems VG (1996) The plastids of the grape pericarp and their significance in isoprenoid synthesis. Australian Journal of Grape and Wine Research 2(3), 144–154.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Horton P, Park K-J, Obayashi T, Fujita N, Harada H , et al . (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Research 35(Suppl. 2), W585–W587.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Jaillon O, Aury JM, Noel B, Policriti A, Clepet C , et al . (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449(7161), 463–467.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Kalua CM, Boss PK (2009) Evolution of volatile compounds during the development of Cabernet Sauvignon grapes (Vitis vinifera L.). Journal of Agricultural and Food Chemistry 57(9), 3818–3830.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Kondo S, Fukuda K (2001) Changes of jasmonates in grape berries and their possible roles in fruit development. Scientia Horticulturae 91(3–4), 275–288.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Kramer DM, Sacksteder CA, Cruz JA (1999) How acidic is the lumen? Photosynthesis Research 60(2–3), 151–163.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Liavonchanka A, Feussner I (2006) Lipoxygenases: occurrence, functions and catalysis. Journal of Plant Physiology 163(3), 348–357.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods (San Diego, Calif.) 25(4), 402–408.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Lund S, Peng F, Nayar T, Reid K, Schlosser J (2008) Gene expression analyses in individual grape (Vitis vinifera L.) berries during ripening initiation reveal that pigmentation intensity is a valid indicator of developmental staging within the cluster. Plant Molecular Biology 68(3), 301–315.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Lund CM, Thompson MK, Benkwitz F, Wohler MW, Triggs CM , et al . (2009) New Zealand Sauvignon Blanc distinct flavor characteristics: sensory, chemical, and consumer aspects. American Journal of Enology and Viticulture 60(1), 1–12.
|  CAS |
open url image1

Matsui K (2006) Green leaf volatiles: hydroperoxide lyase pathway of oxylipin metabolism. Current Opinion in Plant Biology 9(3), 274–280.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Miele A, Bouard J, Bertrand A (1993) Fatty acids from lipid fractions of leaves and different tissues of Cabernet Sauvignon grapes. American Journal of Enology and Viticulture 44(2), 180–186.
|  CAS |
open url image1

Minor W, Steczko J, Stec B, Otwinowski Z, Bolin JT , et al . (1996) Crystal structure of soybean lipoxygenase L-1 at 1.4 Å resolution. Biochemistry 35(33), 10687–10701.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Peña-Cortés H, Barrios P, Dorta F, Polanco V, Sánchez C , et al . (2004) Involvement of jasmonic acid and derivatives in plant responses to pathogens and insects and in fruit ripening. Journal of Plant Growth Regulation 23(3), 246–260. open url image1

Petit A-N, Wojnarowiez G, Panon M-L, Baillieul F, Clément C , et al . (2009) Botryticides affect grapevine leaf photosynthesis without inducing defense mechanisms. Planta 229(3), 497–506.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Porta H, Rocha-Sosa M (2002) Plant lipoxygenases. Physiological and molecular features. Plant Physiology 130(1), 15–21.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Ramey D, Bertrand A, Ough CS, Singleton VL, Sanders E (1986) Effects of skin contact temperature on Chardonnay must and wine composition. American Journal of Enology and Viticulture 37(2), 99–106.
|  CAS |
open url image1

Reid K, Olsson N, Schlosser J, Peng F, Lund S (2006) An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development. BMC Plant Biology 6(1), 27.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Roufet M, Bayonove C, Cordonnier R (1987) Etude de la composition lipidique du raisin, Vitis vinifera L.: evolution au cours de la maturation et localisation dans la baie [Lipid composition of grapevine berries, Vitis vinifera L.: changes during maturation and localization in the berry]. Vitis 26, 85–97.
|  CAS |
open url image1

Royo J, Vancanneyt G, Pérez AG, Sanz C, Störmann K , et al . (1996) Characterization of three potato lipoxygenases with distinct enzymatic activities and different organ-specific and wound-regulated expression patterns. The Journal of Biological Chemistry 271(35), 21012–21019.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Rubio M, Alvarez-Ortí M, Alvarruiz A, Fernández E, Pardo JE (2009) Characterization of oil obtained from grape seeds collected during berry development. Journal of Agricultural and Food Chemistry 57(7), 2812–2815.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Saitou N, Nei M (1987) The Neighbor–Joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4(4), 406–425.
|  CAS |
open url image1

Sambrook J , Russell DW (Eds) (2001) ‘Molecular cloning: a laboratory manual.’ 3rd edn. (Cold Spring Harbor Laboratory Press: Cold Spring Harbor, New York)

Sánchez J, Harwood JL (2002) Biosynthesis of triacylglycerols and volatiles in olives. European Journal of Lipid Science and Technology 104(9–10), 564–573.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Schneider R, Charrier F, Razungles A, Baumes R (2006) Evidence for an alternative biogenetic pathway leading to 3-mercaptohexanol and 4-mercapto-4-methylpentan-2-one in wines. Analytica Chimica Acta 563(1–2), 58–64.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Schwab W, Davidovich-Rikanati R, Lewinsohn E (2008) Biosynthesis of plant-derived flavor compounds. The Plant Journal 54(4), 712–732.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Shibata D, Axelrod B (1995) Plant lipoxygenases. Journal of Lipid Mediators and Cell Signalling 12(2–3), 213–228.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Shibata D, Slusarenko A, Casey R, Hildebrand D, Bell E (1994) Lipoxygenases. Plant Molecular Biology Reporter 12, S41–S42.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Shin JH, Van K, Kim DH, Kim KD, Jang YE , et al . (2008) The lipoxygenase gene family: a genomic fossil of shared polyploidy between Glycine max and Medicago truncatula. BMC Plant Biology 8(1), 133.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Stumpe M, Feussner I (2006) Formation of oxylipins by CYP74 enzymes. Phytochemistry Reviews 5(2–3), 347–357.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24(8), 1596–1599.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22(22), 4673–4680.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N , et al . (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3(7), research0034.0031–research0034.0011.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Wang WH, Takano T, Shibata D, Kitamura K, Takeda G (1994) Molecular basis of a null mutation in soybean lipoxygenase 2: substitution of glutamine for an iron-ligand histidine. Proceedings of the National Academy of Sciences of the United States of America 91(13), 5828–5832.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Annals of Botany 100(4), 681–697.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Yang H-R, Tang K, Liu H-T, Pan Q-H, Huang W-D (2009) Jasmonic acid is induced in a biphasic manner in response of pea seedlings to wounding. Journal of Integrative Plant Biology 51(6), 562–573.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Zuckerkandl E , Pauling L , Bryson V , Vogel HJ (1965) Evolutionary divergence and convergence in proteins. In ‘Evolving genes and proteins’. (Eds V Bryson, HJ Vogel) pp. 97–166. (Academic Press: New York)