Biosynthesis, function and metabolic engineering of plant volatile organic compounds.

Plants synthesize an amazing diversity of volatile organic compounds (VOCs) that facilitate interactions with their environment, from attracting pollinators and seed dispersers to protecting themselves from pathogens, parasites and herbivores. Recent progress in -omics technologies resulted in the isolation of genes encoding enzymes responsible for the biosynthesis of many volatiles and contributed to our understanding of regulatory mechanisms involved in VOC formation. In this review, we largely focus on the biosynthesis and regulation of plant volatiles, the involvement of floral volatiles in plant reproduction as well as their contribution to plant biodiversity and applications in agriculture via crop-pollinator interactions. In addition, metabolic engineering approaches for both the improvement of plant defense and pollinator attraction are discussed in light of methodological constraints and ecological complications that limit the transition of crops with modified volatile profiles from research laboratories to real-world implementation.

[1]  Coby Schal,et al.  Seed odor mediates an obligate ant–plant mutualism in Amazonian rainforests , 2008, Proceedings of the National Academy of Sciences.

[2]  U. Grossniklaus,et al.  The Genetic Basis of Pollinator Adaptation in a Sexually Deceptive Orchid , 2012, PLoS genetics.

[3]  E. M. Friis,et al.  Cretaceous angiosperm flowers: Innovation and evolution in plant reproduction , 2006 .

[4]  Shan Lu,et al.  Cloning and Functional Characterization of a β-Pinene Synthase from Artemisia annua That Shows a Circadian Pattern of Expression1 , 2002, Plant Physiology.

[5]  S. Bouzid,et al.  Peroxisomal localisation of the final steps of the mevalonic acid pathway in planta , 2011, Planta.

[6]  S. Hsu,et al.  Chloroplast localization of methylerythritol 4-phosphate pathway enzymes and regulation of mitochondrial genes in ispD and ispE albino mutants in Arabidopsis , 2008, Plant Molecular Biology.

[7]  R. Dexter Ethylene-regulated floral volatile synthesis in Petunia × , 2007 .

[8]  J. Gershenzon,et al.  Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. , 2009, Current opinion in plant biology.

[9]  B. Spitzer-Rimon,et al.  EOBII, a Gene Encoding a Flower-Specific Regulator of Phenylpropanoid Volatiles' Biosynthesis in Petunia[C][W] , 2010, Plant Cell.

[10]  N. Leonhardt,et al.  A Novel Pathway for Sesquiterpene Biosynthesis from Z,Z-Farnesyl Pyrophosphate in the Wild Tomato Solanum habrochaites[W] , 2009, The Plant Cell Online.

[11]  Alison M. Smith,et al.  Plastidial glycolysis in developing Arabidopsis embryos. , 2010, The New phytologist.

[12]  Ivo Feussner,et al.  The lipoxygenase pathway. , 2003, Annual review of plant biology.

[13]  F. Schiestl On the success of a swindle: pollination by deception in orchids , 2005, Naturwissenschaften.

[14]  Beverly A. Underwood,et al.  Petunia floral volatile benzenoid/phenylpropanoid genes are regulated in a similar manner. , 2010, Phytochemistry.

[15]  M. Lerdau,et al.  The Challenge of Attracting Pollinators While Evading Floral Herbivores: Patterns of Fragrance Emission in Cirsium arvense and Cirsium repandum (Asteraceae) , 2007, International Journal of Plant Sciences.

[16]  J. Y. Kim,et al.  PhMYB4 fine-tunes the floral volatile signature of Petunia×hybrida through PhC4H , 2010, Journal of experimental botany.

[17]  T. Riley,et al.  Antifungal activity of the components of Melaleuca alternifolia (tea tree) oil , 2003, Journal of applied microbiology.

[18]  J. Gershenzon,et al.  Diversity and distribution of floral scent , 2006, The Botanical Review.

[19]  M. Haring,et al.  Differential Timing of Spider Mite-Induced Direct and Indirect Defenses in Tomato Plants1[w] , 2004, Plant Physiology.

[20]  H. Weiner,et al.  Involvement of snapdragon benzaldehyde dehydrogenase in benzoic acid biosynthesis. , 2009, The Plant journal : for cell and molecular biology.

[21]  E. Pichersky,et al.  Enhanced levels of the aroma and flavor compound S-linalool by metabolic engineering of the terpenoid pathway in tomato fruits. , 2001, Plant physiology.

[22]  G. Glevarec,et al.  A single gene encodes isopentenyl diphosphate isomerase isoforms targeted to plastids, mitochondria and peroxisomes in Catharanthus roseus , 2012, Plant Molecular Biology.

[23]  M. Haring,et al.  Regulators of floral fragrance production and their target genes in petunia are not exclusively active in the epidermal cells of petals , 2012, Journal of experimental botany.

[24]  S. Dötterl,et al.  Spatial fragrance patterns in flowers of Silene latifolia: Lilac compounds as olfactory nectar guides? , 2005, Plant Systematics and Evolution.

[25]  M. Farhi,et al.  Identification of rose phenylacetaldehyde synthase by functional complementation in yeast , 2010, Plant Molecular Biology.

[26]  M. Mescher,et al.  Tracing the history of plant traits under domestication in cranberries: potential consequences on anti-herbivore defences. , 2011, Journal of experimental botany.

[27]  M. A. Medeiros,et al.  Odour masking of tomato volatiles by coriander volatiles in host plant selection of Bemisia tabaci biotype B , 2010 .

[28]  Elazar Fallik,et al.  Enrichment of tomato flavor by diversion of the early plastidial terpenoid pathway , 2007, Nature Biotechnology.

[29]  M. Haring,et al.  ODORANT1 Regulates Fragrance Biosynthesis in Petunia Flowersw⃞ , 2005, The Plant Cell Online.

[30]  H. Klee,et al.  Tomato phenylacetaldehyde reductases catalyze the last step in the synthesis of the aroma volatile 2-phenylethanol. , 2007, Phytochemistry.

[31]  M. Birkett,et al.  Maize landraces recruit egg and larval parasitoids in response to egg deposition by a herbivore. , 2011, Ecology letters.

[32]  N. Dudareva,et al.  Completion of the core β-oxidative pathway of benzoic acid biosynthesis in plants , 2012, Proceedings of the National Academy of Sciences.

[33]  Renate A Weizbauer,et al.  Role of aromatic aldehyde synthase in wounding/herbivory response and flower scent production in different Arabidopsis ecotypes. , 2011, The Plant journal : for cell and molecular biology.

[34]  E. Pichersky,et al.  Reduction of Benzenoid Synthesis in Petunia Flowers Reveals Multiple Pathways to Benzoic Acid and Enhancement in Auxin Transport[W] , 2006, The Plant Cell Online.

[35]  A. Schaffer,et al.  Functional characterization of CmCCD1, a carotenoid cleavage dioxygenase from melon. , 2006, Phytochemistry.

[36]  D. Severson,et al.  Comparative analysis of steam distilled floral oils of cacao cultivars (Theobroma cacao L., Sterculiaceae) and attraction of flying insects: Implications for aTheobroma pollination syndrome , 1994, Journal of Chemical Ecology.

[37]  E. Pichersky,et al.  Characterization of a petunia acetyltransferase involved in the biosynthesis of the floral volatile isoeugenol. , 2007, The Plant journal : for cell and molecular biology.

[38]  N. Lewis,et al.  Nitrogen recycling in phenylpropanoid metabolism , 1996 .

[39]  E. Pichersky,et al.  Contribution of CoA Ligases to Benzenoid Biosynthesis in Petunia Flowers[W] , 2012, Plant Cell.

[40]  S. Shafir,et al.  Volatile compounds emitted by rose cultivars: Fragrance perception by man and honeybees , 2004 .

[41]  윤호주 전사인자(transcription factor)와 기관지천식 , 1999 .

[42]  A. Widmer,et al.  Postpollination Changes in Floral Odor in Silene latifolia: Adaptive Mechanisms for Seed-Predator Avoidance? , 2006, Journal of Chemical Ecology.

[43]  I. Baldwin,et al.  Petunia flowers solve the defence/apparency dilemma of pollinator attraction by deploying complex floral blends. , 2013, Ecology letters.

[44]  M. Birkett,et al.  Herbivory by a Phloem-Feeding Insect Inhibits Floral Volatile Production , 2012, PloS one.

[45]  N. Dudareva,et al.  Developmental Regulation of Methyl Benzoate Biosynthesis and Emission in Snapdragon Flowers , 2000, Plant Cell.

[46]  S. Cobb,et al.  The Size of the Olfactory Bulb in 108 Species of Birds , 1968 .

[47]  R. Rouseff,et al.  Carotenoid-Derived Aroma Compounds: An Introduction , 2001 .

[48]  J. Gómez,et al.  Phenotypic selection on floral scent: trade-off between attraction and deterrence? , 2011, Evolutionary Ecology.

[49]  E. Wurtele,et al.  Acetyl-CoA—Life at the metabolic nexus , 2009 .

[50]  C. Kost,et al.  Herbivore-induced, indirect plant defences. , 2005, Biochimica et biophysica acta.

[51]  W. Schwab,et al.  Increased and Altered Fragrance of Tobacco Plants after Metabolic Engineering Using Three Monoterpene Synthases from Lemon , 2004, Plant Physiology.

[52]  M. Rodríguez-Concepcíon,et al.  New insights into plant isoprenoid metabolism. , 2012, Molecular plant.

[53]  A. Mosandl,et al.  Biosynthesis of mono- and sesquiterpenes in carrot roots and leaves (Daucus carota L.): metabolic cross talk of cytosolic mevalonate and plastidial methylerythritol phosphate pathways. , 2005, Phytochemistry.

[54]  M. Schalk,et al.  Redirection of cytosolic or plastidic isoprenoid precursors elevates terpene production in plants , 2006, Nature Biotechnology.

[55]  Xinlu Chen,et al.  Generation of Phenylpropanoid Pathway-Derived Volatiles in Transgenic Plants: Rose Alcohol Acetyltransferase Produces Phenylethyl Acetate and Benzyl Acetate in Petunia Flowers , 2006, Plant Molecular Biology.

[56]  Beverly A. Underwood,et al.  Regulation of Methylbenzoate Emission after Pollination in Snapdragon and Petunia Flowers Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.016766. , 2003, The Plant Cell Online.

[57]  M. Gutensohn,et al.  Involvement of Compartmentalization in Monoterpene and Sesquiterpene Biosynthesis in Plants , 2012 .

[58]  Alisdair R Fernie,et al.  Tomato aromatic amino acid decarboxylases participate in synthesis of the flavor volatiles 2-phenylethanol and 2-phenylacetaldehyde. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[59]  B. M. Lange,et al.  Metabolic cross talk between cytosolic and plastidial pathways of isoprenoid biosynthesis: unidirectional transport of intermediates across the chloroplast envelope membrane. , 2003, Archives of biochemistry and biophysics.

[60]  M. M. Ben Zvi,et al.  Interlinking showy traits: co-engineering of scent and colour biosynthesis in flowers. , 2008, Plant biotechnology journal.

[61]  T. Ashman POLLINATOR SELECTIVITY AND ITS IMPLICATIONS FOR THE EVOLUTION OF DIOECY AND SEXUAL DIMORPHISM , 2000 .

[62]  A. Aharoni,et al.  Terpenoid Metabolism in Wild-Type and Transgenic Arabidopsis Plants Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.016253. , 2003, The Plant Cell Online.

[63]  Natalia Dudareva,et al.  The shikimate pathway and aromatic amino Acid biosynthesis in plants. , 2012, Annual review of plant biology.

[64]  K. Nabeta Chlorophyll a and β-carotene syntheses from 2H and 13C labelled mevalonates and 13C labelled glycine in cultured cells of liverworts, Heteroscyphus planus and Lophocolea heterophylla , 1997 .

[65]  D. Cane 2.06 – Sesquiterpene Biosynthesis: Cyclization Mechanisms , 1999 .

[66]  S. Shafir,et al.  PAP1 transcription factor enhances production of phenylpropanoid and terpenoid scent compounds in rose flowers. , 2012, The New phytologist.

[67]  J. Knudsen,et al.  Trends in floral scent chemistry in pollination syndromes: floral scent composition in moth-pollinated taxa , 1993 .

[68]  H. Ohta,et al.  Two distinct isopentenyl diphosphate isomerases in cytosol and plastid are differentially induced by environmental stresses in tobacco , 2001, FEBS letters.

[69]  R. Raguso,et al.  The ecology and evolution of fly dispersed dung mosses (Family Splachnaceae): Manipulating insect behaviour through odour and visual cues , 2010, Symbiosis.

[70]  Claudia E Vickers,et al.  A unified mechanism of action for volatile isoprenoids in plant abiotic stress. , 2009, Nature chemical biology.

[71]  Wolfram Weckwerth,et al.  Proteome Analysis of Arabidopsis Leaf Peroxisomes Reveals Novel Targeting Peptides, Metabolic Pathways, and Defense Mechanisms[W] , 2007, The Plant Cell Online.

[72]  M. Maffei,et al.  Foraging activity of bumblebees (Bombus terrestris L.) on Bt-expressing eggplants , 2011, Arthropod-Plant Interactions.

[73]  D. Tholl,et al.  The biochemistry of homoterpenes--common constituents of floral and herbivore-induced plant volatile bouquets. , 2011, Phytochemistry.

[74]  M. Hewlins,et al.  An Investigation of the Metabolism of Isoleucine to Active Amyl Alcohol in Saccharomyces cerevisiae * , 2000, The Journal of Biological Chemistry.

[75]  H. Klee,et al.  The Carotenoid Cleavage Dioxygenase 1 Enzyme Has Broad Substrate Specificity, Cleaving Multiple Carotenoids at Two Different Bond Positions* , 2008, Journal of Biological Chemistry.

[76]  E. Pichersky,et al.  Plant Phenylacetaldehyde Synthase Is a Bifunctional Homotetrameric Enzyme That Catalyzes Phenylalanine Decarboxylation and Oxidation* , 2006, Journal of Biological Chemistry.

[77]  A. Kessler,et al.  Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant-pollinator interactions. , 2011, Ecology.

[78]  S. Schütz,et al.  Nursery pollination by a moth in Silene latifolia: the role of odours in eliciting antennal and behavioural responses. , 2006, The New phytologist.

[79]  M. Mazelis Amino Acid Catabolism , 1980 .

[80]  E. Pichersky,et al.  Overexpression of the lemon basil alpha-zingiberene synthase gene increases both mono- and sesquiterpene contents in tomato fruit. , 2008, The Plant journal : for cell and molecular biology.

[81]  M. Marra,et al.  Genomics of hybrid poplar (Populus trichocarpa× deltoides) interacting with forest tent caterpillars (Malacosoma disstria): normalized and full‐length cDNA libraries, expressed sequence tags, and a cDNA microarray for the study of insect‐induced defences in poplar , 2006, Molecular ecology.

[82]  J. Daniel Hare Ecological role of volatiles produced by plants in response to damage by herbivorous insects. , 2011, Annual review of entomology.

[83]  Chang-qing Yang,et al.  The rice (E)-beta-caryophyllene synthase (OsTPS3) accounts for the major inducible volatile sesquiterpenes. , 2007, Phytochemistry.

[84]  A. Widmer,et al.  Floral odour and reproductive isolation in two species of Silene , 2008, Journal of evolutionary biology.

[85]  Carotenoid cleavage , 1997, Science.

[86]  T. C. Turlings,et al.  The Effects of Abiotic Factors on Induced Volatile Emissions in Corn Plants1 , 2002, Plant Physiology.

[87]  H. Bouwmeester,et al.  Genetic engineering of plant volatile terpenoids: effects on a herbivore, a predator and a parasitoid. , 2013, Pest management science.

[88]  R. Croteau,et al.  Terpenoid metabolism. , 1995, The Plant cell.

[89]  Nina Theis Fragrance of Canada Thistle (Cirsium arvense) Attracts Both Floral Herbivores and Pollinators , 2006, Journal of Chemical Ecology.

[90]  S. Dötterl,et al.  Qualitative and quantitative analyses of flower scent in Silene latifolia. , 2005, Phytochemistry.

[91]  M. Lerdau,et al.  Ecology and evolution of light-dependent and light-independent phytogenic volatile organic carbon. , 2003, The New phytologist.

[92]  Ian T. Baldwin,et al.  Volatile Signaling in Plant-Plant Interactions: "Talking Trees" in the Genomics Era , 2006, Science.

[93]  H. E. Dobson,et al.  Floral volatiles in insect biology , 1994 .

[94]  E. Pichersky,et al.  A plant thiolase involved in benzoic acid biosynthesis and volatile benzenoid production. , 2009, The Plant journal : for cell and molecular biology.

[95]  Beverly A. Underwood,et al.  Ethylene-Regulated Floral Volatile Synthesis in Petunia Corollas1[w] , 2005, Plant Physiology.

[96]  A. Aharoni,et al.  Gain and Loss of Fruit Flavor Compounds Produced by Wild and Cultivated Strawberry Species , 2004, The Plant Cell Online.

[97]  J. Gershenzon,et al.  Two sesquiterpene synthases are responsible for the complex mixture of sesquiterpenes emitted from Arabidopsis flowers. , 2005, The Plant journal : for cell and molecular biology.

[98]  A. Aharoni,et al.  Shikimate Pathway and Aromatic Amino Acid , 2012 .

[99]  M. Reichelt,et al.  The nonmevalonate pathway supports both monoterpene and sesquiterpene formation in snapdragon flowers. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[100]  A. Aharoni,et al.  Genetic Engineering of Terpenoid Metabolism Attracts Bodyguards to Arabidopsis , 2005, Science.

[101]  J. Noel,et al.  Eugenol and isoeugenol, characteristic aromatic constituents of spices, are biosynthesized via reduction of a coniferyl alcohol ester. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[102]  M. Erb,et al.  Specific herbivore-induced volatiles defend plants and determine insect community composition in the field. , 2012, Ecology letters.

[103]  H. Bouwmeester,et al.  Molecular engineering of floral scent , 2005 .

[104]  J. Bohlmann,et al.  Plant terpenoid synthases: molecular biology and phylogenetic analysis. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[105]  R. Isaacs,et al.  Implications of Three Biofuel Crops for Beneficial Arthropods in Agricultural Landscapes , 2010, BioEnergy Research.

[106]  B. Smith,et al.  Intensity and the ratios of compounds in the scent of snapdragon flowers affect scent discrimination by honeybees (Apis mellifera) , 2005, Journal of Comparative Physiology A.

[107]  J. Bohlmann,et al.  Herbivore-Induced Defense Response in a Model Legume. Two-Spotted Spider Mites Induce Emission of (E)-β-Ocimene and Transcript Accumulation of (E)-β-Ocimene Synthase in Lotus japonicus1 , 2004, Plant Physiology.

[108]  Anthony L. Schilmiller,et al.  Monoterpenes in the glandular trichomes of tomato are synthesized from a neryl diphosphate precursor rather than geranyl diphosphate , 2009, Proceedings of the National Academy of Sciences.

[109]  J. Losey,et al.  The Economic Value of Ecological Services Provided by Insects , 2006 .

[110]  R. Herrera,et al.  Aroma development during ripening of Fragaria chiloensis fruit and participation of an alcohol acyltransferase (FcAAT1) gene. , 2009, Journal of agricultural and food chemistry.

[111]  M. Ayasse,et al.  Chemical ecology and pollinator-driven speciation in sexually deceptive orchids. , 2011, Phytochemistry.

[112]  W. Eisenreich,et al.  The deoxyxylulose phosphate pathway of isoprenoid biosynthesis: Studies on the mechanisms of the reactions catalyzed by IspG and IspH protein , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[113]  Christoph Grüter,et al.  Flower constancy in insect pollinators: Adaptive foraging behaviour or cognitive limitation? , 2011, Communicative & integrative biology.

[114]  C. Kuhlemeier,et al.  Pollinator Choice in Petunia Depends on Two Major Genetic Loci for Floral Scent Production , 2011, Current Biology.

[115]  Asaph Aharoni,et al.  Expression of a bacterial feedback-insensitive 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase of the shikimate pathway in Arabidopsis elucidates potential metabolic bottlenecks between primary and secondary metabolism. , 2012, The New phytologist.

[116]  N. Bertin,et al.  Light and temperature dependence of the emission of cyclic and acyclic monoterpenes from holm oak (Quercus ilex L.) leaves , 1998 .

[117]  M. Maffei,et al.  Plasma membrane potential depolarization and cytosolic calcium flux are early events involved in tomato (Solanum lycopersicon) plant-to-plant communication. , 2012, Plant science : an international journal of experimental plant biology.

[118]  E. Shklarman,et al.  Modification of flower color and fragrance by antisense suppression of the flavanone 3-hydroxylase gene , 2002, Molecular Breeding.

[119]  W. Eisenreich,et al.  The deoxyxylulose phosphate pathway of terpenoid biosynthesis in plants and microorganisms. , 1998, Chemistry & biology.

[120]  M. Hossaert-McKey,et al.  The chemical ecology of seed dispersal in monoecious and dioecious figs , 2008 .

[121]  P. Kevan,et al.  The Impact of Greenhouse Tomato (Solanales: Solanaceae) Floral Volatiles on Bumble Bee (Hymenoptera: Apidae) Pollination , 2012 .

[122]  I. Baldwin,et al.  Field Experiments with Transformed Plants Reveal the Sense of Floral Scents , 2008, Science.

[123]  U. Ravid,et al.  Linalool and linalool oxide production in transgenic carnation flowers expressing the Clarkia breweri linalool synthase gene , 2002, Molecular Breeding.

[124]  I. Hiltpold,et al.  Manipulation of Chemically Mediated Interactions in Agricultural Soils to Enhance the Control of Crop Pests and to Improve Crop Yield , 2012, Journal of Chemical Ecology.

[125]  E. Pichersky,et al.  RNAi Suppression of Arogenate Dehydratase1 Reveals That Phenylalanine Is Synthesized Predominantly via the Arogenate Pathway in Petunia Petals[C][W] , 2010, Plant Cell.

[126]  J. Gershenzon,et al.  Subgroup 4 R2R3-MYBs in conifer trees: gene family expansion and contribution to the isoprenoid- and flavonoid-oriented responses , 2010, Journal of experimental botany.

[127]  Natalia Dudareva,et al.  Regulation of Circadian Methyl Benzoate Emission in Diurnally and Nocturnally Emitting Plants , 2001, The Plant Cell Online.

[128]  R. Raguso Wake Up and Smell the Roses: The Ecology and Evolution of Floral Scent , 2008 .

[129]  A. Fürholz,et al.  Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[130]  Roman G. Bayer,et al.  Supporting Information for Proteomics , 2010 .

[131]  L. S. Adler,et al.  Advertising to the enemy: enhanced floral fragrance increases beetle attraction and reduces plant reproduction. , 2012, Ecology.

[132]  P. Thonart,et al.  The lipoxygenase metabolic pathway in plants: potential for industrial production of natural green leaf volatiles , 2010 .

[133]  J. Zapp,et al.  Incorporation of 1-[1-(13)C]Deoxy-D-xylulose in chamomile sesquiterpenes. , 1999, Archives of biochemistry and biophysics.

[134]  W. Schwab,et al.  Expression of Clarkia S-linalool synthase in transgenic petunia plants results in the accumulation of S-linalyl-beta-D-glucopyranoside. , 2001, The Plant journal : for cell and molecular biology.

[135]  Characterisation of the gene family encoding acetoacetyl-CoA thiolase in Arabidopsis. , 2008, Functional plant biology : FPB.

[136]  D. Tholl Terpene synthases and the regulation, diversity and biological roles of terpene metabolism. , 2006, Current opinion in plant biology.

[137]  R. Croteau,et al.  Biosynthesis of mono- and sesquiterpenes in peppermint from mevalonate-2-14C , 1972 .

[138]  J. Gershenzon,et al.  Floral Odor Bouquet Loses its Ant Repellent Properties After Inhibition of Terpene Biosynthesis , 2011, Journal of Chemical Ecology.

[139]  J. Gershenzon,et al.  Restoring a maize root signal that attracts insect-killing nematodes to control a major pest , 2009, Proceedings of the National Academy of Sciences.

[140]  Robert C Schuurink,et al.  The transcription factor EMISSION OF BENZENOIDS II activates the MYB ODORANT1 promoter at a MYB binding site specific for fragrant petunias. , 2011, The Plant journal : for cell and molecular biology.

[141]  A. Hemmerlin,et al.  Cross-talk between the Cytosolic Mevalonate and the Plastidial Methylerythritol Phosphate Pathways in Tobacco Bright Yellow-2 Cells* , 2003, Journal of Biological Chemistry.

[142]  H. C. Beck,et al.  Metabolite production and kinetics of branched-chain aldehyde oxidation in Staphylococcus xylosus , 2002 .

[143]  A. Weber,et al.  A plastidial sodium-dependent pyruvate transporter , 2011, Nature.

[144]  H. E. Dobson Relationship between Floral Fragrance Composition and Type of Pollinator , 2006 .

[145]  L. Wolfe Why Alien Invaders Succeed: Support for the Escape‐from‐Enemy Hypothesis , 2002, The American Naturalist.

[146]  Ying-Bo Mao,et al.  Arabidopsis MYC2 Interacts with DELLA Proteins in Regulating Sesquiterpene Synthase Gene Expression[W][OA] , 2012, Plant Cell.

[147]  S. Aubourg,et al.  Genomic analysis of the terpenoid synthase (AtTPS) gene family of Arabidopsis thaliana , 2002, Molecular Genetics and Genomics.

[148]  I. Baldwin,et al.  Making sense of nectar scents: the effects of nectar secondary metabolites on floral visitors of Nicotiana attenuata. , 2007, The Plant journal : for cell and molecular biology.

[149]  H. Klee,et al.  The tomato carotenoid cleavage dioxygenase 1 genes contribute to the formation of the flavor volatiles beta-ionone, pseudoionone, and geranylacetone. , 2004, The Plant journal : for cell and molecular biology.

[150]  Walter Griffin,et al.  The Tomato , 2011 .

[151]  E. Pichersky,et al.  Chapter eleven The SABATH family of MTS in Arabidopsis Thaliana and other plant species , 2003 .

[152]  G. Reineccius Flavor Chemistry and Technology , 1986 .

[153]  R. Rouseff,et al.  Carotenoid-derived aroma compounds , 2001 .

[154]  U. Flügge,et al.  Transport of isoprenoid intermediates across chloroplast envelope membranes. , 2005, Plant biology.

[155]  A. Aharoni,et al.  Metabolic Engineering of Terpenoid Biosynthesis in Plants , 2006, Phytochemistry Reviews.

[156]  S. K. Boey,et al.  Plasma Membrane , 2005 .

[157]  B. M. Lange,et al.  Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[158]  J. Noel,et al.  Characterization of phenylpropene O-methyltransferases from sweet basil: facile change of substrate specificity and convergent evolution within a plant O-methyltransferase family. , 2002, The Plant cell.

[159]  J. Henning,et al.  Cornbined Gas Chromatography-Electroantennogram Characterization of Alfalfa Floral Volatiles Recognized by Honey Bees (Hymenoptera: Apidae) , 1992 .

[160]  M. Maffei,et al.  Signal Transduction in Plant–Insect Interactions: From Membrane Potential Variations to Metabolomics , 2012 .

[161]  A. Aharoni,et al.  Functional Characterization of Enzymes Forming Volatile Esters from Strawberry and Banana[w] , 2004, Plant Physiology.

[162]  J. Harwood,et al.  A raison d'être for two distinct pathways in the early steps of plant isoprenoid biosynthesis? , 2012, Progress in lipid research.

[163]  O. Vitek,et al.  Developmental Changes in the Metabolic Network of Snapdragon Flowers , 2012, PloS one.

[164]  R. Croteau,et al.  2.05 – Monoterpene Biosynthesis , 1999 .

[165]  J. Gershenzon,et al.  Characterization of a BAHD acyltransferase responsible for producing the green leaf volatile (Z)-3-hexen-1-yl acetate in Arabidopsis thaliana. , 2007, The Plant journal : for cell and molecular biology.

[166]  J. Gershenzon,et al.  Biochemistry of Plant Volatiles1 , 2004, Plant Physiology.

[167]  Nathaniel D Hawkins,et al.  Metabolomic analysis of Arabidopsis reveals hemiterpenoid glycosides as products of a nitrate ion-regulated, carbon flux overflow , 2011, Proceedings of the National Academy of Sciences.

[168]  Jérôme Garin,et al.  Chloroplast proteomics highlights the subcellular compartmentation of lipid metabolism. , 2010, Progress in lipid research.

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

[170]  L. Davin,et al.  Chavicol formation in sweet basil (Ocimum basilicum): cleavage of an esterified C9 hydroxyl group with NAD(P)H-dependent reduction. , 2006, Organic & biomolecular chemistry.

[171]  R. Rouseff,et al.  A comparison of citrus blossom volatiles. , 2009, Phytochemistry.

[172]  M. Bowman,et al.  The multiple phenylpropene synthases in both Clarkia breweri and Petunia hybrida represent two distinct protein lineages. , 2008, The Plant journal : for cell and molecular biology.

[173]  J. Gershenzon,et al.  Developmental regulation of monoterpene biosynthesis in the glandular trichomes of peppermint. , 2000, Plant physiology.

[174]  J. Noel,et al.  Floral benzenoid carboxyl methyltransferases: from in vitro to in planta function. , 2005, Phytochemistry.

[175]  J. Noel,et al.  Biosynthesis of Plant Volatiles: Nature's Diversity and Ingenuity , 2006, Science.

[176]  R. Raguso,et al.  Phenotypic selection to increase floral scent emission, but not flower size or colour in bee-pollinated Penstemon digitalis. , 2012, The New phytologist.

[177]  Y. Kamiya,et al.  The Small Subunit of Snapdragon Geranyl Diphosphate Synthase Modifies the Chain Length Specificity of Tobacco Geranylgeranyl Diphosphate Synthase in Planta[W] , 2009, The Plant Cell Online.

[178]  M. Gijzen,et al.  Phytochemical diversity: The sounds of silent metabolism , 2009 .

[179]  T. Ashman,et al.  The sweet smell of success: floral scent affects pollinator attraction and seed fitness in Hesperis matronalis , 2009 .

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

[181]  U. Grossniklaus,et al.  Stearoyl-acyl carrier protein desaturases are associated with floral isolation in sexually deceptive orchids , 2011, Proceedings of the National Academy of Sciences.

[182]  F. Malcata,et al.  Amino acid catabolism and generation of volatiles by lactic acid bacteria. , 2002, Journal of dairy science.

[183]  E. Woltering,et al.  Physiology and molecular biology of petal senescence. , 2008, Journal of experimental botany.

[184]  Min-Sik Song,et al.  Isolation and characterization of a jasmonic acid carboxyl methyltransferase gene from hot pepper(capsicum annuum L.) , 2005, Journal of Plant Biology.

[185]  J. Gershenzon,et al.  The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)-β-caryophyllene, is a defense against a bacterial pathogen. , 2012, The New phytologist.

[186]  T. Kunz,et al.  Chemical Ecology of Fruit Bat Foraging Behavior in Relation to the Fruit Odors of Two Species of Paleotropical Bat-Dispersed Figs (Ficus hispida and Ficus scortechinii) , 2007, Journal of Chemical Ecology.

[187]  K. Nabeta,et al.  Synthesis of chlorophyll a and β-carotene from 2H- and13C-labelled mevalonates and 13C-labelled glycine incultured cells of liverworts, Heteroscyphus planus andLophocolea heterophylla , 1997 .

[188]  Xinlu Chen,et al.  Understanding in Vivo Benzenoid Metabolism in Petunia Petal Tissue1 , 2004, Plant Physiology.

[189]  J. Gershenzon,et al.  Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. , 2009, Phytochemistry.

[190]  N. Dudareva,et al.  Plant Volatiles: Recent Advances and Future Perspectives , 2006 .

[191]  Gad Galili,et al.  The Biosynthetic Pathways for Shikimate and Aromatic Amino Acids in Arabidopsis thaliana , 2010, The arabidopsis book.

[192]  C. Wilkerson,et al.  Two nearly identical terpene synthases catalyze the formation of nerolidol and linalool in snapdragon flowers. , 2008, The Plant journal : for cell and molecular biology.

[193]  O. von Helversen,et al.  Sulphur-containing “perfumes” attract flower-visiting bats , 2000, Journal of Comparative Physiology A.

[194]  F. Kaplan,et al.  Subterranean, Herbivore-Induced Plant Volatile Increases Biological Control Activity of Multiple Beneficial Nematode Species in Distinct Habitats , 2012, PloS one.

[195]  L. Rieseberg,et al.  Plant Speciation , 2007, Science.

[196]  Jörg Bohlmann,et al.  Induction of Volatile Terpene Biosynthesis and Diurnal Emission by Methyl Jasmonate in Foliage of Norway Spruce1 , 2003, Plant Physiology.

[197]  M. Dicke,et al.  Variation in natural plant products and the attraction of bodyguards involved in indirect plant defense , 2010 .

[198]  Eleni A. Spyropoulou,et al.  RNA-seq discovery, functional characterization, and comparison of sesquiterpene synthases from Solanum lycopersicum and Solanum habrochaites trichomes , 2011, Plant Molecular Biology.