Sesquiterpenoid glycosides from glandular trichomes of the wild tomato relative Solanum habrochaites

Ekanayaka, E.A. Prabodha; Li, Chao; Jones, A. Daniel

doi:10.1016/j.phytochem.2013.11.011

Cited by 13 publications

(17 citation statements)

References 33 publications

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“…In trichomes, the total ion chromatograms of LA4024 were dominated by monoterpenes (GC-MS) and conjugated flavonols (mainly rutin; LC-MS), while sesquiterpenes (GC-MS), short branched-chain (C2-C12) acyl sugars, and sesquiterpene carboxylic acids are prevalent in LC-MS-based chromatograms of LA1777 (Supplemental Figure 2). These results confirm previous metabolite analyses of tomato trichomes and underline that trichomes of these species produce different terpenoid secondary metabolites (Slocombe et al, 2008;Besser et al, 2009;Schilmiller et al, 2010;McDowell et al, 2011;Ekanayaka et al, 2014;Ghosh et al, 2014;Li et al, 2014). When quantified, rutin alone contributed to 25% 6 3% of the corresponding trichome dry weight in LA4024, whereas the sum of two major sesquiterpene carboxylic acids [(+)-(E)-a-santalene-12-oic acid and (+)-(E)-endo-bergamotene-12-oic acid] added up to 23% 6 2% of the GT dry weight in LA1777.…”

Section: The Trichomes Of Wild and Cultivated Tomato Produce Differensupporting

confidence: 90%

Multi-Omics of Tomato Glandular Trichomes Reveals Distinct Features of Central Carbon Metabolism Supporting High Productivity of Specialized Metabolites

et al. 2017

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Glandular trichomes are metabolic cell factories with the capacity to produce large quantities of secondary metabolites. Little is known about the connection between central carbon metabolism and metabolic productivity for secondary metabolites in glandular trichomes. To address this gap in our knowledge, we performed comparative metabolomics, transcriptomics, proteomics, and 13 C-labeling of type VI glandular trichomes and leaves from a cultivated (Solanum lycopersicum LA4024) and a wild (Solanum habrochaites LA1777) tomato accession. Specific features of glandular trichomes that drive the formation of secondary metabolites could be identified. Tomato type VI trichomes are photosynthetic but acquire their carbon essentially from leaf sucrose. The energy and reducing power from photosynthesis are used to support the biosynthesis of secondary metabolites, while the comparatively reduced Calvin-Benson-Bassham cycle activity may be involved in recycling metabolic CO 2 . Glandular trichomes cope with oxidative stress by producing high levels of polyunsaturated fatty acids, oxylipins, and glutathione. Finally, distinct mechanisms are present in glandular trichomes to increase the supply of precursors for the isoprenoid pathways. Particularly, the citrate-malate shuttle supplies cytosolic acetyl-CoA and plastidic glycolysis and malic enzyme support the formation of plastidic pyruvate. A model is proposed on how glandular trichomes achieve high metabolic productivity.

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Section: The Trichomes Of Wild and Cultivated Tomato Produce Differensupporting

confidence: 90%

Multi-Omics of Tomato Glandular Trichomes Reveals Distinct Features of Central Carbon Metabolism Supporting High Productivity of Specialized Metabolites

et al. 2017

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“…Further characterization of this compound required purification and structure determination using one-dimensional and two-dimensional NMR, since further fragmentation of the core was not observed in negative ion mode and the mass spectra were not consistent with previously known metabolites. The NMR spectra confirmed the structure as the sesquiterpenoid glycoside campherenane diol diglucoside, as we reported earlier (Ekanayaka et al, 2014).…”

Section: Annotation Of Sesquiterpene Diol Glycosides From S Habrochasupporting

confidence: 87%

“…Our recent discovery of a few glycosylated sesquiterpenoids in this accession suggested the metabolic capacity to form such metabolites in the genus (Ekanayaka et al, 2014). It is the intent of this report to present a framework for the accelerated discovery of terpenoid glycosides from mass spectra generated using common instruments such as time-of-flight mass spectrometers that provide intermediate mass resolution and low-ppm mass accuracy using S. habrochaites LA1777 as an example.…”

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confidence: 99%

Relative Mass Defect Filtering of Mass Spectra: A Path to Discovery of Plant Specialized Metabolites

2015

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The rapid identification of novel plant metabolites and assignments of newly discovered substances to natural product classes present the main bottlenecks to defining plant specialized phenotypes. Although mass spectrometry provides powerful support for metabolite discovery by measuring molecular masses, ambiguities in elemental formulas often fail to reveal the biosynthetic origins of specialized metabolites detected using liquid chromatography-mass spectrometry. A promising approach for mining liquid chromatography-mass spectrometry metabolite profiling data for specific metabolite classes is achieved by calculating relative mass defects (RMDs) from molecular and fragment ions. This strategy enabled the rapid recognition of an extensive range of terpenoid metabolites in complex plant tissue extracts and is independent of retention time, abundance, and elemental formula. Using RMD filtering and tandem mass spectrometry data analysis, 24 novel elemental formulas corresponding to glycosylated sesquiterpenoid metabolites were identified in extracts of the wild tomato Solanum habrochaites LA1777 trichomes. Extensive isomerism was revealed by ultra-high-performance liquid chromatography, leading to evidence of more than 200 distinct sesquiterpenoid metabolites. RMD filtering led to the recognition of the presence of glycosides of two unusual sesquiterpenoid cores that bear limited similarity to known sesquiterpenes in the genus Solanum. In addition, RMD filtering is readily applied to existing metabolomics databases and correctly classified the annotated terpenoid metabolites in the public metabolome database for Catharanthus roseus.Plant metabolic networks generate amazing chemical diversity, but our understanding of the genetic factors responsible for plant chemistry remains primitive. The discovery and identification of metabolites has posed the greatest bottleneck in recent efforts to exploit metabolomics to address questions about the basis for biosynthetic diversity in the plant kingdom (Ji et al., 2009;Zhou et al., 2012). Since the specialized metabolism of nonmodel plants is taxonomically restricted, metabolite databases offer a poor representation of plant chemical diversity, and de novo recognition and discovery of metabolite chemistry is necessary. A common strategy for metabolite discovery has often started with the generation of tandem mass spectrometry (MS/MS) spectra, usually beginning with the most abundant metabolites, and uses characteristic fragment ions to assign metabolites to a particular class of compounds. Flavonoid identification from MS/MS spectra is often successful because most flavonoids yield MS/MS fragment ions characteristic of their flavonoid cores (Ma et al., 1997;Li et al., 2013). However, when MS/MS spectra fail to display classcharacteristic fragment ions, the recognition of a metabolite's structural class is less obvious.Specialized plant metabolites are often grouped as polyphenolic, terpenoid, alkaloid, polyketide, or fatty acid metabolites based upon the biosynthesis of their...

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“…This fragmentation pattern allows inferences to be drawn regarding the number of sugars and malonyl groups connected to the aglycone. Typical neutral loss sequences have been characterized for various secondary metabolites such as sesquiterpene glycosides (Ekanayaka et al, 2014(Ekanayaka et al, , 2015, steroidal glycoalkaloids (Itkin et al, 2013;Schwahn et al, 2014), steviol glycosides (Zimmermann, 2011), iridoid glycosides (Es-Safi et al, 2007), cyclic glycolipids (Asai et al, 2012) and flavonoids (Kite and Veitch, 2011). This existing knowledge on the neutral loss sequences of the before mentioned metabolite classes is highly beneficial for devising annotation workflows as described in the second part of this study.…”

Section: Structural Classification Of Hgl-dtgs Based On Diagnostic Msmentioning

confidence: 99%

Using the knowns to discover the unknowns: MS‐based dereplication uncovers structural diversity in 17‐hydroxygeranyllinalool diterpene glycoside production in the Solanaceae

et al. 2016

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SUMMARYExploring the diversity of plant secondary metabolism requires efficient methods to obtain sufficient structural insights to discriminate previously known from unknown metabolites. De novo structure elucidation and confirmation of known metabolites (dereplication) remain a major bottleneck for mass spectrometrybased metabolomic workflows, and few systematic dereplication strategies have been developed for the analysis of entire compound classes across plant families, partly due to the complexity of plant metabolic profiles that complicates cross-species comparisons. 17-hydroxygeranyllinalool diterpene glycosides (HGLDTGs) are abundant defensive secondary metabolites whose malonyl and glycosyl decorations are induced by jasmonate signaling in the ecological model plant Nicotiana attenuata. The multiple labile glycosidic bonds of HGL-DTGs result in extensive in-source fragmentation (IS-CID) during ionization. To reconstruct these IS-CID clusters from profiling data and identify precursor ions, we applied a deconvolution algorithm and created an MS/MS library from positive-ion spectra of purified HGL-DTGs. From this library, 251 nonredundant fragments were annotated, and a workflow to characterize leaf, flower and fruit extracts of 35 solanaceous species was established. These analyses predicted 105 novel HGL-DTGs that were restricted to Nicotiana, Capsicum and Lycium species. Interestingly, malonylation is a highly conserved step in HGL-DTG metabolism, but is differentially affected by jasmonate signaling among Nicotiana species. This MS-based workflow is readily applicable for cross-species re-identification/annotation of other compound classes with sufficient fragmentation knowledge, and therefore has the potential to support hypotheses regarding secondary metabolism diversification.

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Sesquiterpenoid glycosides from glandular trichomes of the wild tomato relative Solanum habrochaites

Cited by 13 publications

References 33 publications

Multi-Omics of Tomato Glandular Trichomes Reveals Distinct Features of Central Carbon Metabolism Supporting High Productivity of Specialized Metabolites

Multi-Omics of Tomato Glandular Trichomes Reveals Distinct Features of Central Carbon Metabolism Supporting High Productivity of Specialized Metabolites

Relative Mass Defect Filtering of Mass Spectra: A Path to Discovery of Plant Specialized Metabolites

Using the knowns to discover the unknowns: MS‐based dereplication uncovers structural diversity in 17‐hydroxygeranyllinalool diterpene glycoside production in the Solanaceae

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