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Plants produce phylogenetically and spatially restricted, as well as structurally diverse specialized metabolites via multistep metabolic pathways. Hallmarks of specialized metabolic evolution include enzymatic promiscuity and recruitment of primary metabolic enzymes and examples of genomic clustering of pathway genes. Solanaceae glandular trichomes produce defensive acylsugars, with sidechains that vary in length across the family. We describe a tomato gene cluster on chromosome 7 involved in medium chain acylsugar accumulation due to trichome specific acyl-CoA synthetase and enoyl-CoA hydratase genes. This cluster co-localizes with a tomato steroidal alkaloid gene cluster and is syntenic to a chromosome 12 region containing another acylsugar pathway gene. We reconstructed the evolutionary events leading to this gene cluster and found that its phylogenetic distribution correlates with medium chain acylsugar accumulation across the Solanaceae. This work reveals insights into the dynamics behind gene cluster evolution and cell-type specific metabolite diversity.
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Fruity, sticky, stinky, spicy, bitter, addictive, and deadly: evolutionary signatures of metabolic complexity in the Solanaceae
Plants collectively synthesize a huge repertoire of metabolites. General metabolites, also referred to as primary metabolites, are conserved across the plant kingdom and are required for processes essential to growth and development. These include amino acids, sugars, lipids, and organic acids. In contrast, specialized metabolites, historically termed secondary metabolites, are structurally diverse, exhibit lineage-specific distribution and provide selective advantage to host species to facilitate reproduction and environmental adaptation. Due to their potent bioactivities, plant specialized metabolites attract considerable attention for use as flavorings, fragrances, pharmaceuticals, and bio-pesticides. The Solanaceae (Nightshade family) consists of approximately 2700 species and includes crops of significant economic, cultural, and scientific importance: these include potato, tomato, pepper, eggplant, tobacco, and petunia. The Solanaceae has emerged as a model family for studying the biochemical evolution of plant specialized metabolism and multiple examples exist of lineage-specific metabolites that influence the senses and physiology of commensal and harmful organisms, including humans. These include, alcohols, phenylpropanoids, and carotenoids that contribute to fruit aroma and color in tomato (fruity), glandular trichome-derived terpenoids and acylsugars that contribute to plant defense (stinky & sticky, respectively), capsaicinoids in chilli-peppers that influence seed dispersal (spicy), and steroidal glycoalkaloids (bitter) from Solanum, nicotine (addictive) from tobacco, as well as tropane alkaloids (deadly) from Deadly Nightshade that deter herbivory. Advances in genomics and metabolomics, coupled with the adoption of comparative phylogenetic approaches, resulted in deeper knowledge of the biosynthesis and evolution of these metabolites. This review highlights recent progress in this area and outlines opportunities for – and challenges of-developing a more comprehensive understanding of Solanaceae metabolism.
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- Award ID(s):
- 1714093
- PAR ID:
- 10469465
- Publisher / Repository:
- Royal Society of Chemistry
- Date Published:
- Journal Name:
- Natural Product Reports
- Volume:
- 39
- Issue:
- 7
- ISSN:
- 0265-0568
- Page Range / eLocation ID:
- 1438 to 1464
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract 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 by ACYLSUGAR ACYLTRANSFERASE (ASAT) enzymes from sugars and acyl-coenzyme A esters. Published research has revealed trichome acylsugars composed of glucose and sucrose cores in species across the family. In addition, acylsugars have been analyzed across a small fraction of the >1,200 species in the phenotypically megadiverse Solanum genus, with a handful containing inositol and glycosylated inositol cores. The current study sampled several dozen species across subclades of Solanum to get a more detailed view of acylsugar chemodiversity. In depth characterization of acylsugars from the clade II species brinjal eggplant (Solanum melongena) led to the identification of eight unusual structures with inositol or inositol glycoside cores and hydroxyacyl chains. Liquid chromatography-mass spectrometry analysis of 31 additional species in the Solanum genus revealed striking acylsugar diversity, with some traits restricted to specific clades and species. Acylinositols and inositol-based acyldisaccharides were detected throughout much of the genus. In contrast, acylglucoses and acylsucroses were more restricted in distribution. Analysis of tissue-specific transcriptomes and interspecific acylsugar acetylation differences led to the identification of the brinjal eggplant ASAT 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 appears to be a functionally divergent ASAT3. This study provides a foundation for investigating the evolution and function of diverse Solanum acylsugar structures and harnessing this diversity in breeding and synthetic biology.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1039/D2NP00003B
