An integrative “omics” approach identifies new candidate genes to impact aroma volatiles in peach fruit

BackgroundEver since the recent completion of the peach genome, the focus of genetic research in this area has turned to the identification of genes related to important traits, such as fruit aroma volatiles. Of the over 100 volatile compounds described in peach, lactones most likely have the strongest effect on fruit aroma, while esters, terpenoids, and aldehydes have minor, yet significant effects. The identification of key genes underlying the production of aroma compounds is of interest for any fruit-quality improvement strategy.ResultsVolatile (52 compounds) and gene expression (4348 genes) levels were profiled in peach fruit from a maturity time-course series belonging to two peach genotypes that showed considerable differences in maturation characteristics and postharvest ripening. This data set was analyzed by complementary correlation-based approaches to discover the genes related to the main aroma-contributing compounds: lactones, esters, and phenolic volatiles, among others. As a case study, one of the candidate genes was cloned and expressed in yeast to show specificity as an ω-6 Oleate desaturase, which may be involved in the production of a precursor of lactones/esters.ConclusionsOur approach revealed a set of genes (an alcohol acyl transferase, fatty acid desaturases, transcription factors, protein kinases, cytochromes, etc.) that are highly associated with peach fruit volatiles, and which could prove useful in breeding or for biotechnological purposes.

[1]  David Zilberman,et al.  How quality relates to price in California fresh peaches , 1991 .

[2]  P. Mendes,et al.  The origin of correlations in metabolomics data , 2005, Metabolomics.

[3]  Nikhil A. Joshi,et al.  Whole genome sequencing of peach (Prunus persica L.) for SNP identification and selection , 2011, BMC Genomics.

[4]  J. Fernandes,et al.  Transcriptomic, proteomic and metabolomic analysis of UV-B signaling in maize , 2011, BMC Genomics.

[5]  X. Qiu,et al.  A Peroxygenase Pathway Involved in the Biosynthesis of Epoxy Fatty Acids in Oat[W][OA] , 2011, Plant Physiology.

[6]  B. Møller,et al.  CYP703 Is an Ancient Cytochrome P450 in Land Plants Catalyzing in-Chain Hydroxylation of Lauric Acid to Provide Building Blocks for Sporopollenin Synthesis in Pollen[W] , 2007, The Plant Cell Online.

[7]  Christina E. Wells,et al.  The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution , 2013, Nature Genetics.

[8]  M. Hirai,et al.  Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis , 2007, Proceedings of the National Academy of Sciences.

[9]  S. Boddupalli,et al.  A bifunctional oleate 12-hydroxylase: desaturase from Lesquerella fendleri. , 1998, The Plant journal : for cell and molecular biology.

[10]  M. Zanor,et al.  Integrated Analysis of Metabolite and Transcript Levels Reveals the Metabolic Shifts That Underlie Tomato Fruit Development and Highlight Regulatory Aspects of Metabolic Network Behavior1[W] , 2006, Plant Physiology.

[11]  M. Hirai,et al.  Elucidation of Gene-to-Gene and Metabolite-to-Gene Networks in Arabidopsis by Integration of Metabolomics and Transcriptomics* , 2005, Journal of Biological Chemistry.

[12]  G. Casadoro,et al.  A simple protocol for transient gene expression in ripe fleshy fruit mediated by Agrobacterium. , 2001, Journal of experimental botany.

[13]  H. Ten Have,et al.  Fao , 1950, Social Service Review.

[14]  Kun-song Chen,et al.  Changes in aroma-related volatiles and gene expression during low temperature storage and subsequent shelf-life of peach fruit , 2011 .

[15]  Michel Zivy,et al.  The use of metabolomics integrated with transcriptomic and proteomic studies for identifying key steps involved in the control of nitrogen metabolism in crops such as maize. , 2012, Journal of experimental botany.

[16]  J. Giovannoni,et al.  MOLECULAR BIOLOGY OF FRUIT MATURATION AND RIPENING. , 2001, Annual review of plant physiology and plant molecular biology.

[17]  Yury Tikunov,et al.  A Novel Approach for Nontargeted Data Analysis for Metabolomics. Large-Scale Profiling of Tomato Fruit Volatiles1[w] , 2005, Plant Physiology.

[18]  Ian L. Gatfield,et al.  Biotechnological Production of Natural Flavor Materials , 1999 .

[19]  J. Giovannoni,et al.  Branched-chain and aromatic amino acid catabolism into aroma volatiles in Cucumis melo L. fruit , 2010, Journal of experimental botany.

[20]  Kun-song Chen,et al.  Expression of genes associated with aroma formation derived from the fatty acid pathway during peach fruit ripening. , 2010, Journal of agricultural and food chemistry.

[21]  M. Vanoli,et al.  Volatile compound production during growth and ripening of peaches and nectarines , 1997 .

[22]  C. Bonghi,et al.  The use of microarray μPEACH1.0 to investigate transcriptome changes during transition from pre-climacteric to climacteric phase in peach fruit , 2006 .

[23]  Elizabeth A. Baldwin,et al.  Flavor trivia and tomato aroma: biochemistry and possible mechanisms for control of important aroma components. , 2000 .

[24]  Shaohua Li,et al.  Volatile characteristics of 50 peaches and nectarines evaluated by HP-SPME with GC-MS , 2009 .

[25]  J. Ehlting,et al.  Arabidopsis thaliana CYP77A4 is the first cytochrome P450 able to catalyze the epoxidation of free fatty acids in plants , 2009, The FEBS journal.

[26]  D. Nelson,et al.  A P450-centric view of plant evolution. , 2011, The Plant journal : for cell and molecular biology.

[27]  C. Bruhn,et al.  CONSUMER PERCEPTIONS OF QUALITY: APRICOTS, CANTALOUPES, PEACHES, PEARS, STRAWBERRIES, AND TOMATOES , 1991 .

[28]  J. Forment,et al.  Development of ChillPeach genomic tools and identification of cold-responsive genes in peach fruit , 2008, Plant Molecular Biology.

[29]  Fidel Ramírez,et al.  Computing topological parameters of biological networks , 2008, Bioinform..

[30]  S. Bureau,et al.  Aroma characterization of various apricot varieties using headspace–solid phase microextraction combined with gas chromatography–mass spectrometry and gas chromatography–olfactometry , 2006 .

[31]  R. Baeza-Yates,et al.  A rapid and efficient method for purifying high quality total RNA from peaches (Prunus persica) for functional genomics analyses. , 2005, Biological research.

[32]  R. Baumes,et al.  Changes in physicochemical characteristics and volatile constituents of yellow- and white-fleshed nectarines during maturation and artificial ripening. , 2003, Journal of agricultural and food chemistry.

[33]  Santiago F. Elena,et al.  Fine-Tuning Tomato Agronomic Properties by Computational Genome Redesign , 2012, PLoS Comput. Biol..

[34]  Kazuki Saito,et al.  Metabolomics for functional genomics, systems biology, and biotechnology. , 2010, Annual review of plant biology.

[35]  Laura Rossini,et al.  Identification of key odor volatile compounds in the essential oil of nine peach accessions. , 2010, Journal of the science of food and agriculture.

[36]  Henry-Éric Spinnler,et al.  Importance des lactones dans les arômes alimentaires : structure, distribution, propriétés sensorielles et biosynthèse , 1994 .

[37]  M. Troggio,et al.  Genetic dissection of aroma volatile compounds from the essential oil of peach fruit: QTL analysis and identification of candidate genes using dense SNP maps , 2013, Tree Genetics & Genomes.

[38]  W. Boland,et al.  Biosynthesis of Dodecano‐4‐lactone in Ripening Fruits: Crucial Role of an Epoxide‐Hydrolase in Enantioselective Generation of Aroma Components of the Nectarine (Prunus persica var. nucipersica) and the Strawberry (Fragaria ananassa) , 1996 .

[39]  P. Broun,et al.  Catalytic plasticity of fatty acid modification enzymes underlying chemical diversity of plant lipids. , 1998, Science.

[40]  P. Arús,et al.  The peach genome , 2012, Tree Genetics & Genomes.

[41]  J. Garin,et al.  Plant Seed Peroxygenase Is an Original Heme-oxygenase with an EF-hand Calcium Binding Motif* , 2006, Journal of Biological Chemistry.

[42]  J. D’Auria.  Acyltransferases in plants: a good time to be BAHD. , 2006, Current opinion in plant biology.

[43]  G. Cipriani,et al.  Development of an oligo-based microarray (µPEACH 1.0) for genomics studies in peach fruit , 2005 .

[44]  P. Shannon,et al.  Cytoscape: a software environment for integrated models of biomolecular interaction networks. , 2003, Genome research.

[45]  M. R. Tabilio,et al.  Effects of cold storage on aroma compounds of white- and yellow-fleshed peaches , 2008 .

[46]  W. R. Forbus,et al.  Physical and chemical changes during the maturation of peaches (cv. Majestic). , 1991 .

[47]  R. Tibshirani,et al.  Significance analysis of microarrays applied to the ionizing radiation response , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[48]  E. Cahoon,et al.  Transgenic Production of Epoxy Fatty Acids by Expression of a Cytochrome P450 Enzyme from Euphorbia lagascaeSeed , 2002, Plant Physiology.

[49]  W. Schwab,et al.  Biosynthesis of plant-derived flavor compounds. , 2008, The Plant journal : for cell and molecular biology.

[50]  A. Murphy,et al.  Identification, Purification, and Molecular Cloning of N-1-Naphthylphthalmic Acid-Binding Plasma Membrane-Associated Aminopeptidases from Arabidopsis1 , 2002, Plant Physiology.

[51]  I. Mignani,et al.  Diverse metabolism of cell wall components of melting and non-melting peach genotypes during ripening after harvest or cold storage , 2006 .

[52]  Catherine Deborde,et al.  Gene and Metabolite Regulatory Network Analysis of Early Developing Fruit Tissues Highlights New Candidate Genes for the Control of Tomato Fruit Composition and Development1[C][W][OA] , 2009, Plant Physiology.

[53]  Dorrie Main,et al.  Development and Evaluation of a 9K SNP Array for Peach by Internationally Coordinated SNP Detection and Validation in Breeding Germplasm , 2012, PloS one.

[54]  Antonio Granell,et al.  A Non-Targeted Approach Unravels the Volatile Network in Peach Fruit , 2012, PloS one.

[55]  P. Schieberle,et al.  Differences in key odorants of handmade juice of yellow-flesh peaches (Prunus persica L.) induced by the workup procedure. , 1999, Journal of agricultural and food chemistry.

[56]  A. Vecchietti,et al.  Comparative analysis of expressed sequence tags from tissues in ripening stages of peach (Prunus persica L. Batsch) , 2009, Tree Genetics & Genomes.

[57]  John Shanklin,et al.  DESATURATION AND RELATED MODIFICATIONS OF FATTY ACIDS1. , 1998, Annual review of plant physiology and plant molecular biology.

[58]  J. Napier,et al.  The sunflower plastidial omega3-fatty acid desaturase (HaFAD7) contains the signalling determinants required for targeting to, and retention in, the endoplasmic reticulum membrane in yeast but requires co-expressed ferredoxin for activity. , 2010, Phytochemistry.

[59]  K. Patel,et al.  Role of lipid bodies and lipid-body proteins in seeds and other tissues , 2001 .

[60]  G. Casadoro,et al.  The involvement of auxin in the ripening of climacteric fruits comes of age: the hormone plays a role of its own and has an intense interplay with ethylene in ripening peaches. , 2007, Journal of experimental botany.

[61]  P. Broun,et al.  An oleate 12-hydroxylase from Ricinus communis L. is a fatty acyl desaturase homolog. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[62]  Edna Pesis,et al.  The role of the anaerobic metabolites, acetaldehyde and ethanol, in fruit ripening, enhancement of fruit quality and fruit deterioration , 2005 .

[63]  Alessandro Liverani,et al.  Study of 'Redhaven' peach and its white-fleshed mutant suggests a key role of CCD4 carotenoid dioxygenase in carotenoid and norisoprenoid volatile metabolism , 2011, BMC Plant Biology.

[64]  A. Fernie,et al.  Metabolic Profiling during Peach Fruit Development and Ripening Reveals the Metabolic Networks That Underpin Each Developmental Stage1[C][W] , 2011, Plant Physiology.