RESUMEN
Gymnosperms are long-lived, cone-bearing seed plants that include some of the most ancient extant plant species. These relict land plants have evolved to survive in habitats marked by chronic or episodic stress. Their ability to thrive in these environments is partly due to their phenotypic flexibility, and epigenetic regulation likely plays a crucial part in this plasticity. We review the current knowledge on abiotic and biotic stress memory in gymnosperms and the possible epigenetic mechanisms underlying long-term phenotypic adaptations. We also discuss recent technological improvements and new experimental possibilities that likely will advance our understanding of epigenetic regulation in these ancient and hard-to-study plants.
Asunto(s)
Cycadopsida , Epigénesis Genética , Estrés Fisiológico , Cycadopsida/genética , Cycadopsida/fisiología , Estrés Fisiológico/genética , Adaptación Fisiológica/genética , Regulación de la Expresión Génica de las Plantas , FenotipoRESUMEN
BACKGROUND: The order Lepidoptera has an abundance of species, including both agriculturally beneficial and detrimental insects. Molecular data has been used to investigate the phylogenetic relationships of major subdivisions in Lepidoptera, which has enhanced our understanding of the evolutionary relationships at the family and superfamily levels. However, the phylogenetic placement of many superfamilies and/or families in this order is still unknown. In this study, we determine the systematic status of the family Argyresthiidae within Lepidoptera and explore its phylogenetic affinities and implications for the evolution of the order. We describe the first mitochondrial (mt) genome from a member of Argyresthiidae, the apple fruit moth Argyresthia conjugella. The insect is an important pest on apples in Fennoscandia, as it switches hosts when the main host fails to produce crops. RESULTS: The mt genome of A. conjugella contains 16,044 bp and encodes all 37 genes commonly found in insect mt genomes, including 13 protein-coding genes (PCGs), two ribosomal RNAs, 22 transfer RNAs, and a large control region (1101 bp). The nucleotide composition was extremely AT-rich (82%). All detected PCGs (13) began with an ATN codon and terminated with a TAA stop codon, except the start codon in cox1 is ATT. All 22 tRNAs had cloverleaf secondary structures, except trnS1, where one of the dihydrouridine (DHU) arms is missing, reflecting potential differences in gene expression. When compared to the mt genomes of 507 other Lepidoptera representing 18 superfamilies and 42 families, phylogenomic analyses found that A. conjugella had the closest relationship with the Plutellidae family (Yponomeutoidea-super family). We also detected a sister relationship between Yponomeutoidea and the superfamily Tineidae. CONCLUSIONS: Our results underline the potential importance of mt genomes in comparative genomic analyses of Lepidoptera species and provide valuable evolutionary insight across the tree of Lepidoptera species.
Asunto(s)
Genoma Mitocondrial , Lepidópteros , Malus , Mariposas Nocturnas , Humanos , Animales , Mariposas Nocturnas/genética , Malus/genética , Filogenia , Frutas , Lepidópteros/genética , ARN de Transferencia/genética , Codón de TerminaciónRESUMEN
Norway spruce (Picea abies) is an economically and ecologically important tree species that grows across northern and central Europe. Treating Norway spruce with jasmonate has long-lasting beneficial effects on tree resistance to damaging pests, such as the European spruce bark beetle Ips typographus and its fungal associates. The (epi)genetic mechanisms involved in such long-lasting jasmonate induced resistance (IR) have gained much recent interest but remain largely unknown. In this study, we treated 2-year-old spruce seedlings with methyl jasmonate (MeJA) and challenged them with the I. typographus vectored necrotrophic fungus Grosmannia penicillata. MeJA treatment reduced the extent of necrotic lesions in the bark 8 weeks after infection and thus elicited long-term IR against the fungus. The transcriptional response of spruce bark to MeJA treatment was analysed over a 4-week time course using mRNA-seq. This analysis provided evidence that MeJA treatment induced a transient upregulation of jasmonic acid, salicylic acid and ethylene biosynthesis genes and downstream signalling genes. Our data also suggests that defence-related genes are induced while genes related to growth are repressed by methyl jasmonate treatment. These results provide new clues about the potential underpinning mechanisms and costs associated with long-term MeJA-IR in Norway spruce.
Asunto(s)
Picea , Acetatos/farmacología , Ciclopentanos , Oxilipinas , Picea/fisiología , Corteza de la Planta , Transcriptoma/genética , ÁrbolesRESUMEN
Plants can form an immunological memory known as defense priming, whereby exposure to a priming stimulus enables quicker or stronger response to subsequent attack by pests and pathogens. Such priming of inducible defenses provides increased protection and reduces allocation costs of defense. Defense priming has been widely studied for short-lived model plants such as Arabidopsis, but little is known about this phenomenon in long-lived plants like spruce. We compared the effects of pretreatment with sublethal fungal inoculations or application of the phytohormone methyl jasmonate (MeJA) on the resistance of 48-year-old Norway spruce (Picea abies) trees to mass attack by a tree-killing bark beetle beginning 35 days later. Bark beetles heavily infested and killed untreated trees but largely avoided fungus-inoculated trees and MeJA-treated trees. Quantification of defensive terpenes at the time of bark beetle attack showed fungal inoculation induced 91-fold higher terpene concentrations compared with untreated trees, whereas application of MeJA did not significantly increase terpenes. These results indicate that resistance in fungus-inoculated trees is a result of direct induction of defenses, whereas resistance in MeJA-treated trees is due to defense priming. This work extends our knowledge of defense priming from model plants to an ecologically important tree species.
Asunto(s)
Escarabajos , Picea/inmunología , Corteza de la Planta/química , Enfermedades de las Plantas/inmunología , Acetatos/farmacología , Animales , Ciclopentanos/farmacología , Hongos/fisiología , Noruega , Oxilipinas/farmacología , Reguladores del Crecimiento de las Plantas , Terpenos , ÁrbolesRESUMEN
In response to various stimuli, plants acquire resistance against pests and/or pathogens. Such acquired or induced resistance allows plants to rapidly adapt to their environment. Spraying the bark of mature Norway spruce (Picea abies) trees with the phytohormone methyl jasmonate (MeJA) enhances resistance to tree-killing bark beetles and their associated phytopathogenic fungi. Analysis of spruce chemical defenses and beetle colonization success suggests that MeJA treatment both directly induces immune responses and primes inducible defenses for a faster and stronger response to subsequent beetle attack. We used metabolite and transcriptome profiling to explore the mechanisms underlying MeJA-induced resistance in Norway spruce. We demonstrated that MeJA treatment caused substantial changes in the bark transcriptional response to a triggering stress (mechanical wounding). Profiling of mRNA expression showed a suite of spruce inducible defenses are primed following MeJA treatment. Although monoterpenes and diterpene resin acids increased more rapidly after wounding in MeJA-treated than control bark, expression of their biosynthesis genes did not. We suggest that priming of inducible defenses is part of a complex mixture of defense responses that underpins the increased resistance against bark beetle colonization observed in Norway spruce. This study provides the most detailed insights yet into the mechanisms underlying induced resistance in a long-lived gymnosperm.
Asunto(s)
Acetatos/farmacología , Ciclopentanos/farmacología , Oxilipinas/farmacología , Picea/efectos de los fármacos , Picea/fisiología , Animales , Escarabajos/microbiología , Ciclopentanos/metabolismo , Metilación de ADN/efectos de los fármacos , Regulación de la Expresión Génica de las Plantas/efectos de los fármacos , Histonas/metabolismo , Monoterpenos/metabolismo , Oxilipinas/metabolismo , Fenotipo , Corteza de la Planta/efectos de los fármacos , Corteza de la Planta/genética , Reguladores del Crecimiento de las Plantas/metabolismo , Proteínas de Plantas/genética , Proteínas de Plantas/metabolismoRESUMEN
Acetophenones are phenolic compounds involved in the resistance of white spruce (Picea glauca) against spruce budworm (Choristoneura fumiferiana), a major forest pest in North America. The acetophenones pungenol and piceol commonly accumulate in spruce foliage in the form of the corresponding glycosides, pungenin and picein. These glycosides appear to be inactive against the insect but can be cleaved by a spruce ß-glucosidase, PgßGLU-1, which releases the active aglycons. The reverse glycosylation reaction was hypothesized to involve a family 1 UDP-sugar dependent glycosyltransferase (UGT) to facilitate acetophenone accumulation in the plant. Metabolite and transcriptome profiling over a developmental time course of white spruce bud burst and shoot growth revealed two UGTs, PgUGT5 and PgUGT5b, that glycosylate pungenol. Recombinant PgUGT5b enzyme produced mostly pungenin, while PgUGT5 produced mostly isopungenin. Both UGTs also were active in vitro on select flavonoids. However, the context of transcript and metabolite accumulation did not support a biological role in flavonoid metabolism but correlated with the formation of pungenin in growing shoots. Transcript levels of PgUGT5b were higher than those of PgUGT5 in needles across different genotypes of white spruce. These results support a role of PgUGT5b in the biosynthesis of the glycosylated acetophenone pungenin in white spruce.
Asunto(s)
Acetofenonas/metabolismo , Glicosiltransferasas/metabolismo , Insectos/fisiología , Enfermedades de las Plantas/inmunología , Inmunidad de la Planta , Tracheophyta/enzimología , Animales , Glucósidos/metabolismo , Glicósidos/metabolismo , Glicosiltransferasas/genética , Enfermedades de las Plantas/parasitología , Proteínas de Plantas/genética , Proteínas de Plantas/metabolismo , Tracheophyta/genética , Tracheophyta/inmunología , Tracheophyta/parasitología , Azúcares de Uridina Difosfato/metabolismoRESUMEN
Plants are sessile organisms that lack a specialized immune system to cope with biotic and abiotic stress. Instead, plants have complex regulatory networks that determine the appropriate distribution of resources between the developmental and the defense programs. In the last years, epigenetic regulation of repeats and gene expression has evolved as an important player in the transcriptional regulation of stress-related genes. Here, we review the current knowledge about how different stresses interact with different levels of epigenetic control of the genome. Moreover, we analyze the different examples of transgenerational epigenetic inheritance and connect them with the known features of genome epigenetic regulation. Although yet to be explored, the interplay between epigenetics and stress resistance seems to be a relevant and dynamic player of the interaction of plants with their environments.
Asunto(s)
Epigénesis Genética , Regulación de la Expresión Génica de las Plantas , Plantas/genética , Transducción de Señal/genética , Estrés Fisiológico , Sequías , Interacción Gen-Ambiente , Modelos Genéticos , Enfermedades de las Plantas/genética , Enfermedades de las Plantas/microbiología , Enfermedades de las Plantas/virología , Plantas/microbiología , Plantas/virología , SalinidadRESUMEN
Periodic outbreaks of spruce budworm (SBW) affect large areas of ecologically and economically important conifer forests in North America, causing tree mortality and reduced forest productivity. Host resistance against SBW has been linked to growth phenology and the chemical composition of foliage, but the underlying molecular mechanisms and population variation are largely unknown. Using a genomics approach, we discovered a ß-glucosidase gene, Pgßglu-1, whose expression levels and function underpin natural resistance to SBW in mature white spruce (Picea glauca) trees. In phenotypically resistant trees, Pgßglu-1 transcripts were up to 1000 times more abundant than in non-resistant trees and were highly enriched in foliage. The encoded PgßGLU-1 enzyme catalysed the cleavage of acetophenone sugar conjugates to release the aglycons piceol and pungenol. These aglycons were previously shown to be active against SBW. Levels of Pgßglu-1 transcripts and biologically active acetophenone aglycons were substantially different between resistant and non-resistant trees over time, were positively correlated with each other and were highly variable in a natural white spruce population. These results suggest that expression of Pgßglu-1 and accumulation of acetophenone aglycons is a constitutive defence mechanism in white spruce. The progeny of resistant trees had higher Pgßglu-1 gene expression than non-resistant progeny, indicating that the trait is heritable. With reported increases in the intensity of SBW outbreaks, influenced by climate, variation of Pgßglu-1 transcript expression, PgßGLU-1 enzyme activity and acetophenone accumulation may serve as resistance markers to better predict impacts of SBW in both managed and wild spruce populations.
Asunto(s)
Resistencia a la Enfermedad/genética , Picea/fisiología , Proteínas de Plantas/fisiología , beta-Glucosidasa/fisiología , Acetofenonas/metabolismo , Animales , Perfilación de la Expresión Génica , Regulación de la Expresión Génica de las Plantas , Herbivoria , Larva/fisiología , Modelos Moleculares , Datos de Secuencia Molecular , Mariposas Nocturnas/fisiología , Picea/enzimología , Picea/genética , Proteínas de Plantas/química , Proteínas de Plantas/genética , Proteínas de Plantas/metabolismo , Estructura Terciaria de Proteína , beta-Glucosidasa/química , beta-Glucosidasa/genética , beta-Glucosidasa/metabolismoRESUMEN
Tomato flavor is dependent upon a complex mixture of volatiles including multiple acetate esters. Red-fruited species of the tomato clade accumulate a relatively low content of acetate esters in comparison with the green-fruited species. We show that the difference in volatile ester content between the red- and green-fruited species is associated with insertion of a retrotransposon adjacent to the most enzymatically active member of a family of esterases. This insertion causes higher expression of the esterase, resulting in the reduced levels of multiple esters that are negatively correlated with human preferences for tomato. The insertion was evolutionarily fixed in the red-fruited species, suggesting that high expression of the esterase and consequent low ester content may provide an adaptive advantage in the ancestor of the red-fruited species. These results illustrate at a molecular level how closely related species exhibit major differences in volatile production by altering a volatile-associated catabolic activity.
Asunto(s)
Acetatos/metabolismo , Esterasas/metabolismo , Proteínas de Plantas/metabolismo , Solanum lycopersicum/enzimología , Compuestos Orgánicos Volátiles/metabolismo , Secuencia de Bases , Esterasas/genética , Humanos , Solanum lycopersicum/genética , Datos de Secuencia Molecular , Proteínas de Plantas/genética , Plantas Modificadas Genéticamente/enzimología , Plantas Modificadas Genéticamente/genética , Retroelementos/genéticaRESUMEN
O-methyltransferases (OMT) are important enzymes that are responsible for the synthesis of many small molecules, which include lignin monomers, flavonoids, alkaloids, and aroma compounds. One such compound is guaiacol, a small volatile molecule with a smoky aroma that contributes to tomato flavor. Little information is known about the pathway and regulation of synthesis of guaiacol. One possible route for synthesis is via catechol methylation. We identified a tomato O-methyltransferase (CTOMT1) with homology to a Nicotiana tabacum catechol OMT. CTOMT1 was cloned from Solanum lycopersicum cv. M82 and expressed in Escherichia coli. Recombinant CTOMT1 enzyme preferentially methylated catechol, producing guaiacol. To validate the in vivo function of CTOMT1, gene expression was either decreased or increased in transgenic S. lycopersicum plants. Knockdown of CTOMT1 resulted in significantly reduced fruit guaiacol emissions. CTOMT1 overexpression resulted in slightly increased fruit guaiacol emission, which suggested that catechol availability might limit guaiacol production. To test this hypothesis, wild type (WT) and CTOMT1 that overexpress tomato pericarp discs were supplied with exogenously applied catechol. Guaiacol production increased in both WT and transgenic fruit discs, although to a much greater extent in CTOMT1 overexpressing discs. Finally, we identified S. pennellii introgression lines with increased guaiacol content and higher expression of CTOMT1. These lines also showed a trend toward lower catechol levels. Taken together, we concluded that CTOMT1 is a catechol-O-methyltransferase that produces guaiacol in tomato fruit.
Asunto(s)
Catecol O-Metiltransferasa/metabolismo , Aromatizantes/metabolismo , Guayacol/metabolismo , Proteínas de Plantas/metabolismo , Solanum lycopersicum/enzimología , Catecol O-Metiltransferasa/genética , Catecoles/metabolismo , Clonación Molecular , Activación Enzimática , Escherichia coli/genética , Escherichia coli/metabolismo , Frutas/metabolismo , Regulación Enzimológica de la Expresión Génica , Regulación de la Expresión Génica de las Plantas , Técnicas de Silenciamiento del Gen , Solanum lycopersicum/genética , Solanum lycopersicum/metabolismo , Metilación , Filogenia , Proteínas de Plantas/genética , Plantas Modificadas Genéticamente/enzimología , Plantas Modificadas Genéticamente/genética , Plantas Modificadas Genéticamente/metabolismo , Sitios de Carácter Cuantitativo , Ácido Salicílico/metabolismo , Especificidad por SustratoRESUMEN
Genetic studies have shown the effects of various photoreceptors on early photomorphogenic processes, defining the precise time course of red (RL), far-red (FrL) and blue light (BL) action. In this study, the effect of green wavebands in conjunction with these responses is examined. Longer-term (end point; 24-96 h) analysis of hypocotyl elongation in enriched green environments shows an increase in growth compared to seedlings under blue, red or both together. The effect was only observed at lower fluence rates (<10 µmol/m² s). Genetic analyses demonstrate that cryptochromes are required for this GL effect, consistent with earlier findings, and that the phy receptors have no influence. However, analysis of early (minutes to hours) stem growth kinetics indicates that GL cannot reverse the cryptochrome-mediated BL effect during early stem growth inhibition, and instead acts additively with BL to drive cryptochrome-mediated inhibition. Green light (GL) treatments antagonize RL and FrL-mediated hypocotyl inhibition. The GL opposition of RL responses persists in phyA, phyB, cry1cry2 and phot2 mutants. The response requires phot1 and NPH3, suggesting that this is not a GL response, but instead a response to extremely low-fluence rate BL. Tests with dim BL (<0.1 µmol/m² s) confirm a previously uncharacterized phot1-dependent promotion of stem growth, opposing the effects of RL. These findings demonstrate how enriched green environments may adjust RL and BL photomorphogenic responses through both the crys and phot1 receptors, and define a new role for phot1 in stem growth promotion.
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Criptocromos/genética , Hipocótilo/efectos de la radiación , Luz , Mutación , Fototropinas/genética , Arabidopsis/genética , Arabidopsis/crecimiento & desarrollo , Arabidopsis/efectos de la radiación , Proteínas de Arabidopsis/genética , Factores de Transcripción con Cremalleras de Leucina de Carácter Básico/genética , Proteínas de Ciclo Celular/genética , Regulación del Desarrollo de la Expresión Génica/efectos de la radiación , Regulación de la Expresión Génica de las Plantas/efectos de la radiación , Hipocótilo/genética , Hipocótilo/crecimiento & desarrollo , Péptidos y Proteínas de Señalización Intracelular/genética , Cinética , Proteínas de la Membrana , Proteínas Nucleares/genética , Fosfoproteínas/genética , Fitocromo A/genética , Fitocromo B/genética , Tallos de la Planta/genética , Tallos de la Planta/crecimiento & desarrollo , Tallos de la Planta/efectos de la radiación , Proteínas Serina-Treonina Quinasas , Reacción en Cadena de la Polimerasa de Transcriptasa Inversa , Plantones/genética , Plantones/crecimiento & desarrollo , Plantones/efectos de la radiación , Factores de TiempoRESUMEN
The large pine weevil (Hylobius abietis) is a major regeneration pest in commercial forestry. Pesticide application has historically been the preferred control method, but pesticides are now being phased out in several countries for environmental reasons. There is, thus, a need for alternative plant protection strategies. We applied methyl jasmonate (MeJA), salicylic acid (SA) or oxalic acid (OxA) on the stem of 2-year-old Norway spruce (Picea abies) plants to determine effects on inducible defenses and plant growth. Anatomical examination of stem cross-sections 9 weeks after application of 100 mM MeJA revealed massive formation of traumatic resin ducts and greatly reduced sapwood growth. Application of high concentrations of SA or OxA (500 and 200 mM, respectively) induced much weaker physiological responses than 100 mM MeJA. All three treatments reduced plant height growth significantly, but the reduction was larger for MeJA (~55%) than for SA and OxA (34-35%). Lower MeJA concentrations (5-50 mM) induced comparable traumatic resin duct formation as the high MeJA concentration but caused moderate (and non-significant) reductions in plant growth. Two-year-old spruce plants treated with 100 mM MeJA showed reduced mortality after exposure to pine weevils in the field, and this enhanced resistance-effect was statistically significant for three years after treatment.
RESUMEN
The Chernobyl Nuclear Power Plant (ChNPP) accident in 1986 resulted in extremely high levels of acute ionising radiation, that killed or damaged Scots pine (Pinus sylvestris) trees in the surrounding areas. Dead trees were cleared and buried, and new plantations established a few years later. Today, more than three decades later, gamma and beta-radiation near the ChNPP is still elevated compared with ambient levels but have decreased by a factor of 300 and 100, respectively. In the present work, Scots pine-trees growing at High (220 µGy h-1), Medium (11 µGy h-1), and Low (0.2 µGy h-1) total (internal + external) dose rates of chronically elevated ionising radiation in the Chernobyl Exclusion zone were investigated with respect to possible damage to DNA, cells and organelles, as well as potentially increased levels of phenolic and terpenoid antioxidants. Scots pine from the High and Medium radiation sites had elevated levels of DNA damage in shoot tips and needles as shown by the COMET assay, as well as increased numbers of resin ducts and subcellular abnormalities in needles. Needles from the High radiation site showed elevated levels of monoterpenes and condensed tannins compared with those from the other sites. In conclusion, more than three decades after the ChNPP accident substantial DNA damage and (sub)cellular effects, but also mobilisation of stress-protective substances possessing antioxidant activity were observed in Scots pine trees growing at elevated levels of ionising radiation. This demonstrates that the radiation levels in the Red Forest still significantly impact the plant community.
Asunto(s)
Accidente Nuclear de Chernóbil , Pinus sylvestris , Pinus , Monitoreo de Radiación , Radiación Ionizante , Árboles , BosquesRESUMEN
To be protected from biological threats, plants have evolved an immune system comprising constitutive and inducible defenses. For example, upon perception of certain stimuli, plants can develop a conditioned state of enhanced defensive capacity against upcoming pathogens and pests, resulting in a phenotype called 'induced resistance' (IR). To tackle the confusing lexicon currently used in the IR field, we propose a widely applicable code of practice concerning the terminology and description of IR phenotypes using two main phenotypical aspects: local versus systemic resistance, and direct versus primed defense responses. Our general framework aims to improve uniformity and consistency in future scientific communication, which should help to avoid further misinterpretations and facilitate the accessibility and impact of this research field.
RESUMEN
We review a recently discovered white spruce (Picea glauca) chemical defense against spruce budworm (Choristoneura fumiferana) involving hydroxyacetophenones. These defense metabolites detected in the foliage accumulate variably as the aglycons, piceol and pungenol, or the corresponding glucosides, picein and pungenin. We summarize current knowledge of the genetic, genomic, molecular, and biochemical underpinnings of this defense and its effects on C. fumiferana. We present an update with new results on the ontogenic variation and the phenological window of this defense, including analysis of transcript responses in P. glauca to C. fumiferana herbivory. We also discuss this chemical defense from an evolutionary and a breeding context.
RESUMEN
As primary producers, plants are under constant pressure to defend themselves against potentially deadly pathogens and herbivores. In this review, we describe short- and long-term strategies that enable plants to cope with these stresses. Apart from internal immunological strategies that involve physiological and (epi)genetic modifications at the cellular level, plants also employ external strategies that rely on recruitment of beneficial organisms. We discuss these strategies along a gradient of increasing timescales, ranging from rapid immune responses that are initiated within seconds to (epi)genetic adaptations that occur over multiple plant generations. We cover the latest insights into the mechanistic and evolutionary underpinnings of these strategies and present explanatory models. Finally, we discuss how knowledge from short-lived model species can be translated to economically and ecologically important perennials to exploit adaptive plant strategies and mitigate future impacts of pests and diseases in an increasingly interconnected and changing world.
Asunto(s)
Herbivoria , Plantas , Adaptación Fisiológica , Evolución Biológica , Enfermedades de las PlantasRESUMEN
Eastern spruce budworm (Choristoneura fumiferiana Clemens) (ESBW) is a major forest pest which feeds on young shoots of white spruce (Picea glauca) and can cause landscape level economic and ecological losses. Release of acetophenone metabolites, piceol and pungenol, from their corresponding glycosides, picein and pungenin, can confer natural resistance of spruce to ESBW. A beta-glucosidase gene, Pgßglu-1, was recently discovered and the encoded enzyme was characterized in vitro to function in the release of the defensive acetophenone aglycons. Here we describe overexpression of Pgßglu-1 in a white spruce genotype whose metabolome contains the glucosylated acetophenones, but no detectable amounts of the aglycons. Transgenic overexpression of Pgßglu-1 resulted in release of the acetophenone aglycons in planta. This work provides in vivo evidence for the function of Pgßglu-1.
RESUMEN
Although human perception of food flavors involves integration of multiple sensory inputs, the most salient sensations are taste and olfaction. Ortho- and retronasal olfaction are particularly crucial to flavor because they provide the qualitative diversity so important to identify safe versus dangerous foods. Historically, flavor research has prioritized aroma volatiles present at levels exceeding the orthonasally measured odor threshold, ignoring the variation in the rate at which odor intensities grow above threshold. Furthermore, the chemical composition of a food in itself tells us very little about whether or not that food will be liked. Clearly, alternative approaches are needed to elucidate flavor chemistry. Here we use targeted metabolomics and natural variation in flavor-associated sugars, acids, and aroma volatiles to evaluate the chemistry of tomato fruits, creating a predictive and testable model of liking. This nontraditional approach provides novel insights into flavor chemistry, the interactions between taste and retronasal olfaction, and a paradigm for enhancing liking of natural products. Some of the most abundant volatiles do not contribute to consumer liking, whereas other less abundant ones do. Aroma volatiles make contributions to perceived sweetness independent of sugar concentration, suggesting a novel way to increase perception of sweetness without adding sugar.