Fruity, sticky, stinky, spicy, bitter, addictive, and deadly: evolutionary signatures of metabolic complexity in the Solanaceae

Fiesel, Paul D.; Parks, Hannah M.; Last, Robert L.; Barry, Cornelius S.

doi:10.1039/d2np00003b

Cited by 23 publications

(14 citation statements)

References 187 publications

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“…show that conversion of acylsucroses to acylglucoses arose at least twice in Solanum because S. (Fiesel et al, 2022). In contrast, no acylsucroses were detected in any species screened.…”

Section: Sticky Fruits Accumulate Acylinositolsmentioning

confidence: 80%

“…Until recently, it appeared that acylsucroses dominate acylsugar profiles of Solanaceae species with a small number of documented examples of acylglucose-and acylinositol-producing Solanum species (Fiesel et al, 2022;Fobes et al, 1985;Herrera-Salgado et al, 2005;Hurney, 2018;King and Calhoun, 1988;Leong et al, 2020;Liu et al, 2017;Lou et al, 2021;Moghe et al, 2017;Schenck et al, 2022). Our chemotaxonomic survey of nearly three dozen Solanum analyses together cover <3% of Solanum species, this presumably is only a subset of trichome acylsugar diversity within this large genus.…”

Section: Natural Variation Potentiates Novel Activities and Usesmentioning

confidence: 87%

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Trading acyls and swapping sugars: metabolic innovations inSolanumtrichomes

Fiesel

Kerwin

Jones

et al. 2023

Preprint

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Solanaceae (nightshade family) species synthesize a remarkable array of clade- and tissue-specific specialized metabolites. Protective acylsugars, one such class of structurally diverse metabolites, are produced from sugars and acyl-Coenzyme A esters by acylsugar acyltransferases in glandular trichomes. We characterized trichome acylsugars of the Clade II species Solanum melongena (brinjal eggplant) using liquid chromatography-mass spectrometry (LC-MS), gas chromatography-MS and nuclear magnetic resonance (NMR) spectroscopy. This led to the identification of eight unusual structures with inositol cores, inositol glycoside cores, and hydroxyacyl chains. LC-MS analysis of 31 species in the megadiverse Solanum genus revealed striking acylsugar diversity with some traits restricted to specific clades and species. The Acylinositols were found throughout each clade while acylglucoses were restricted to DulMo and VANAns species. Medium length hydroxyacyl chains were found in many species. Analysis of tissue-specific transcriptomes and interspecific acylsugar acetylation differences led to characterization of the S. melongena Acylsugar AcylTransferase 3-Like 1 (SmASAT3-L1; SMEL4.1_12g015780) enzyme. This enzyme is distinct from previously characterized acylsugar acetyltransferases, which are in the ASAT4 clade, and is a functionally divergent ASAT3. This study provides a foundation for investigating the evolution of diverse Solanum acylsugar structures and harnessing this diversity in breeding and synthetic biology.

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“…show that conversion of acylsucroses to acylglucoses arose at least twice in Solanum because S. (Fiesel et al, 2022). In contrast, no acylsucroses were detected in any species screened.…”

Section: Sticky Fruits Accumulate Acylinositolsmentioning

confidence: 80%

Section: Natural Variation Potentiates Novel Activities and Usesmentioning

confidence: 87%

Trading acyls and swapping sugars: metabolic innovations inSolanumtrichomes

Fiesel

Kerwin

Jones

et al. 2023

Preprint

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“…Type-IV trichomes produce AS, a structurally diverse class of compounds resulting from the acylation of a sugar core (Mutschler et al, 1996; Schilmiller et al, 2008; Leckie et al, 2012; Vosman et al, 2019; Feng et al, 2021; Fiesel et al, 2022). AS are especially effective against arthropod herbivory, including Lepidoptera ( Helicoverpa amigera , Spodoptera exigua , Phthorimeae operculella ), Acarina ( Tetranychus urticae ), and Hemiptera ( Myzus persicae ) (Goffreda et al, 1990; Hawthorne et al, 1992; Liedl et al, 1995; Simmons and Gurr, 2005; Maluf et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Woollymutation withGet02locus overcomes the polygenic nature of trichome-based pest resistance in tomato

Vendemiatti,

Hernández-De Lira,

Snijders

et al. 2023

Preprint

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Type-IV glandular trichomes, which only occur in the juvenile phase of tomato development, produce acylsugars (AS) that broadly protect against arthropod herbivory. Previously, we introgressed the capacity to retain type-IV trichomes in the adult phase fromSolanum galapagenseinto the cv. Micro-Tom (MT). The resulting MT-Getline contained five loci associated with enhancing the density of type-IV trichomes in adult plants. We genetically dissected MT-Getand obtained a sub-line containing only the locus on chromosome 2 (MT-Get02). This genotype displayed about half the density of type-IV trichomes compared to the wild progenitor. However, when we stacked the gain-of-function allele ofWOOLLY, which codes for a HD-ZIP IV transcription factor, MT-Get02/Woexhibited double the number of type-IV trichomes compared toS. galapagense. This discovery corroborates previous reports positioningWOOLLYas a master regulator of trichome development. AS levels in MT-Get02/Wowere comparable to the wild progenitor, although the composition of AS types differed, especially regarding less AS with medium-length acyl chains. Agronomical parameters of MT-Get02/Wo, including yield, were comparable to MT. Pest resistance assays showed enhanced protection against whitefly, caterpillar, and the fungusSeptoria lycopersici. However, resistance levels did not reach that of the wild progenitor, suggesting the specificity of particulars AS types in the pest resistance mechanism. Our findings in trichome-mediated resistance advance the development of robust, naturally resistant tomato varieties, harnessing the potential of natural genetic variation. Moreover, by manipulating only two loci, we achieved exceptional results for a highly complex, polygenic trait, such as herbivory resistance in tomato.

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“…Plants synthesize complex mixtures of specialized metabolites of various chemical classes that facilitate reproduction and adaptation to abiotic and biotic challenges (Tewksbury & Nabhan, 2001 ; Weinhold & Baldwin, 2011 ; A. C. Huang et al ., 2019 ; Voges et al ., 2019 ; Fiesel et al ., 2022 ; Roy et al ., 2022 ). The bioactive properties of plant‐specialized metabolites have led to the cooption of plants and their chemical components for use as pharmaceuticals, flavorings, fragrances, and agrochemicals.…”

Section: Introductionmentioning

confidence: 99%

“…The bioactive properties of plant‐specialized metabolites have led to the cooption of plants and their chemical components for use as pharmaceuticals, flavorings, fragrances, and agrochemicals. In turn, this has driven intense interest toward purifying bioactive components from plant extracts, elucidating their structures, resolving their underlying mechanisms of biosynthesis, and developing metabolic engineering strategies for sustainable or increased production (Westfall et al ., 2012 ; Galanie et al ., 2015 ; Srinivasan & Smolke, 2020 ; Mitreiter & Gigolashvili, 2021 ; Fiesel et al ., 2022 ).…”

Section: Introductionmentioning

confidence: 99%

Redirecting tropane alkaloid metabolism reveals pyrrolidine alkaloid diversity in Atropa belladonna

et al. 2022

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Summary Plant‐specialized metabolism is complex, with frequent examples of highly branched biosynthetic pathways, and shared chemical intermediates. As such, many plant‐specialized metabolic networks are poorly characterized. The N‐methyl Δ1‐pyrrolinium cation is a simple pyrrolidine alkaloid and precursor of pharmacologically important tropane alkaloids. Silencing of pyrrolidine ketide synthase (AbPyKS) in the roots of Atropa belladonna (Deadly Nightshade) reduces tropane alkaloid abundance and causes high N‐methyl Δ1‐pyrrolinium cation accumulation. The consequences of this metabolic shift on alkaloid metabolism are unknown. In this study, we utilized discovery metabolomics coupled with AbPyKS silencing to reveal major changes in the root alkaloid metabolome of A. belladonna. We discovered and annotated almost 40 pyrrolidine alkaloids that increase when AbPyKS activity is reduced. Suppression of phenyllactate biosynthesis, combined with metabolic engineering in planta, and chemical synthesis indicates several of these pyrrolidines share a core structure formed through the nonenzymatic Mannich‐like decarboxylative condensation of the N‐methyl Δ1‐pyrrolinium cation with 2‐O‐malonylphenyllactate. Decoration of this core scaffold through hydroxylation and glycosylation leads to mono‐ and dipyrrolidine alkaloid diversity. This study reveals the previously unknown complexity of the A. belladonna root metabolome and creates a foundation for future investigation into the biosynthesis, function, and potential utility of these novel alkaloids.

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Fruity, sticky, stinky, spicy, bitter, addictive, and deadly: evolutionary signatures of metabolic complexity in the Solanaceae

Abstract: This review focuses on the biosynthesis and evolution of specialized metabolism in the Solanaceae (Nightshade) family.

Cited by 23 publications

References 187 publications

Trading acyls and swapping sugars: metabolic innovations inSolanumtrichomes

Trading acyls and swapping sugars: metabolic innovations inSolanumtrichomes

Woollymutation withGet02locus overcomes the polygenic nature of trichome-based pest resistance in tomato

Redirecting tropane alkaloid metabolism reveals pyrrolidine alkaloid diversity in Atropa belladonna

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