Evolutionary routes to biochemical innovation revealed by integrative analysis of a plant-defense related specialized metabolic pathway

Moghe, Gaurav D.; Leong, Bryan J.; Hurney, Steven M.; Jones, A. Daniel

doi:10.7554/elife.28468

Cited by 98 publications

(280 citation statements)

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“…RNAseq analysis was done essentially according to Moghe et al (2017). Total RNA was extracted from leaf and flower parts at different stages of development using the Total RNA Isolation Kit from Omega.…”

Section: Rnaseq Analysismentioning

confidence: 99%

Coexpression Analysis Identifies Two Oxidoreductases Involved in the Biosynthesis of the Monoterpene Acid Moiety of Natural Pyrethrin Insecticides in Tanacetum cinerariifolium

Moghe

Schilmiller

et al. 2017

Plant Physiol.

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Flowers of Tanacetum cinerariifolium produce a set of compounds known collectively as pyrethrins, which are commercially important pesticides that are strongly toxic to flying insects but not to most vertebrates. A pyrethrin molecule is an ester consisting of either trans-chrysanthemic acid or its modified form, pyrethric acid, and one of three alcohols, jasmolone, pyrethrolone, and cinerolone, that appear to be derived from jasmonic acid. Chrysanthemyl diphosphate synthase (CDS), the first enzyme involved in the synthesis of trans-chrysanthemic acid, was characterized previously and its gene isolated. TcCDS produces free trans-chrysanthemol in addition to trans-chrysanthemyl diphosphate, but the enzymes responsible for the conversion of trans-chrysanthemol to the corresponding aldehyde and then to the acid have not been reported. We used an RNA sequencingbased approach and coexpression correlation analysis to identify several candidate genes encoding putative trans-chrysanthemol and trans-chrysanthemal dehydrogenases. We functionally characterized the proteins encoded by these genes using a combination of in vitro biochemical assays and heterologous expression in planta to demonstrate that TcADH2 encodes an enzyme that oxidizes trans-chrysanthemol to trans-chrysanthemal, while TcALDH1 encodes an enzyme that oxidizes trans-chrysanthemal into transchrysanthemic acid. Transient coexpression of TcADH2 and TcALDH1 together with TcCDS in Nicotiana benthamiana leaves results in the production of trans-chrysanthemic acid as well as several other side products. The majority (58%) of trans-chrysanthemic acid was glycosylated or otherwise modified. Overall, these data identify key steps in the biosynthesis of pyrethrins and demonstrate the feasibility of metabolic engineering to produce components of these defense compounds in a heterologous host.

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Section: Rnaseq Analysismentioning

confidence: 99%

Coexpression Analysis Identifies Two Oxidoreductases Involved in the Biosynthesis of the Monoterpene Acid Moiety of Natural Pyrethrin Insecticides in Tanacetum cinerariifolium

Moghe

Schilmiller

et al. 2017

Plant Physiol.

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“…The acyl chains are branched or straight and are proposed to be derived from amino acid or fatty acid metabolism, respectively (Walters and Steffens, 1990; Kroumova and Wagner, 2009; Ning et al, 2015). Acylsugar cores from Solanaceae species are primarily sucrose or sometimes glucose (King et al, 1986; King and Calhoun, 1988; Maldonado et al, 2006; Ghosh et al, 2014; Liu et al, 2017; Moghe et al, 2017; Leong et al, 2019). Solanum lanceolatum is a published exception, accumulating acylated disaccharide cores that contain myo -inositol bound to glucose or xylose (Herrera-Salgado et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

“…Solanum lanceolatum is a published exception, accumulating acylated disaccharide cores that contain myo -inositol bound to glucose or xylose (Herrera-Salgado et al, 2005). Moghe and colleagues screened acylsugars in plants across the Solanaceae family (Moghe et al, 2017). One species – the South American fruit crop Solanum quitoense – produced unusual acylsugars that yielded lower signals of fragment ions generated in a mass spectrometer than acylsucroses or acylglucoses from other members of the Solanaceae (Hurney, 2018).…”

Section: Introductionmentioning

confidence: 99%

“…Acylsugar acyltransferases (ASATs) are clade III BAHD (BEAT, AHCT, HCT, and DAT) acyltransferase family enzymes (D’Auria, 2006; Moghe et al, 2017), which catalyze the core acylation reactions of characterized acylsugar biosynthetic pathways (Schilmiller et al, 2012a; Schilmiller et al, 2015; Fan et al, 2016; Moghe et al, 2017; Nadakuduti et al, 2017; Fan et al, 2019). ASATs sequentially transfer acyl chains from acyl-CoAs to generate acylsucroses in plants as phylogenetically divergent as Solanum lycopersicum, Solanum pennellii, Petunia axillaris , and Salpiglossis sinuata (Schilmiller et al, 2012a; Schilmiller et al, 2015; Fan et al, 2016; Fan et al, 2017; Moghe et al, 2017; Nadakuduti et al, 2017). Expression of characterized ASATs is enriched in glandular trichomes relative to non-acylsugar producing tissues (Ning et al, 2015; Moghe et al, 2017; Nadakuduti et al, 2017; Leong et al, 2019; Mandal et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

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Solanaceae specialized metabolism in a non-model plant: trichome acylinositol biosynthesis

Leong

Hurney

Fiesel

et al. 2020

Preprint

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One sentence summary: Evidence that the final step in Solanum quitoense acylinositol biosynthesis evolved from an acylsucrose acetyltransferase enzyme. AbstractPlants make hundreds of thousands of biologically active specialized metabolites varying widely in structure, biosynthesis and the processes that they influence. An increasing number of these compounds are documented to protect plants from harmful insects, pathogens, or herbivores, or mediate interactions with beneficial organisms including pollinators and nitrogen fixing microbes. Acylsugars -one class of protective compounds -are made in glandular trichomes of plants across the Solanaceae family. While most described acylsugars are acylsucroses, published examples also include acylsugars with hexose cores. The South American fruit crop Solanum quitoense (Naranjilla) produces acylsugars that contain a myoinositol core. We identified an enzyme that acetylates triacylinositols, a function homologous to the last step in the Solanum lycopersicum acylsucrose biosynthetic pathway. Our analysis reveals parallels between S. lycopersicum acylsucrose and S. quitoense acylinositol biosynthesis, suggesting a common evolutionary origin.

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“…The second challenge involves identifying the thousands of metabolites observed in MS data from highly sensitive MS instruments. A recent study found evidence for >300 compounds of a single metabolite class (acylsugars) in a single leaf surface extract (Moghe et al, 2017). …”

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confidence: 99%

The study of plant specialized metabolism: Challenges and prospects in the genomics era

Moghe

Kruse

2018

American J of Botany

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Plants produce a diverse array of compounds through an extensive, evolutionarily malleable network of metabolic pathways. These metabolites are typically classified into two types-primary and specialized-with most of the diversity occurring among specialized metabolites (Fig. 1A). Metabolite presence-absence and types vary dynamically in an individual plant (within/between tissues/organs, developmental stages, across the circadian cycle), between populations, and also between species. Conservatively, it was estimated that each species harbors ~4.7 unique metabolites, and over a million metabolites were predicted to exist across the plant kingdom (Afendi et al., 2012).The scale of metabolite diversity raises multiple challenges for the study of plant specialized metabolism. First, it creates the challenge of identifying these compounds. While genomic and transcriptomic technologies have advanced significantly in the last decade, the complexity of metabolite structures and their chemical properties hinders adoption of standardized protocols for their detection. Second, the lineage-specific nature of specialized metabolism (Fig. 1A) creates the challenge of identifying biosynthetic enzymes and studying their evolution in non-reference species. Finally, there is still much to be understood about the ecological importance of chemical structural diversity in a single plant and across populations. In this article, we discuss these challenges and potential opportunities in more detail. CHARACTERIZING THE VAST DIVERSITY OF PLANT METABOLITESPlant metabolites are typically detected using gas or liquid chromatography, coupled with mass spectrometry (GC-MS or LC-MS). GC-MS is appropriate for compounds that can be readily converted to gas phase, such as some terpenoids, sterols, fatty acids, and aromatic volatiles. It is typically used for low molecular weight compounds that are stable at high temperatures, either in their native form or after some chemical derivatization. LC-MS, on the other hand, is applicable for a much broader array of compounds and generally does not require any derivatization.Despite significant advances in MS technologies, several challenges remain for characterizing plant metabolite diversity. First, because of the large diversity of chemical structures, a variety of different protocols must be used to characterize the true "metabolome", i.e., the entire metabolite repertoire, of a plant, unlike the relative uniformity of experimental designs in transcriptomics or genomics. Various factors at the sample preparation, liquid chromatography, mass spectrometry (MS), and data analysis steps can influence which and how well metabolite peaks are detected. The second challenge involves identifying the thousands of metabolites observed in MS data from highly sensitive MS instruments. A recent study found evidence for >300 compounds of a single metabolite class (acylsugars) in a single leaf surface extract (Moghe et al., 2017).

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Evolutionary routes to biochemical innovation revealed by integrative analysis of a plant-defense related specialized metabolic pathway

Cited by 98 publications

References 98 publications

Coexpression Analysis Identifies Two Oxidoreductases Involved in the Biosynthesis of the Monoterpene Acid Moiety of Natural Pyrethrin Insecticides in Tanacetum cinerariifolium

Coexpression Analysis Identifies Two Oxidoreductases Involved in the Biosynthesis of the Monoterpene Acid Moiety of Natural Pyrethrin Insecticides in Tanacetum cinerariifolium

Solanaceae specialized metabolism in a non-model plant: trichome acylinositol biosynthesis

The study of plant specialized metabolism: Challenges and prospects in the genomics era

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