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Several commercially important secondary metabolites are produced and accumulated in high amounts by glandular trichomes, giving the prospect of using them as metabolic cell factories. Due to extremely high metabolic fluxes through glandular trichomes, previous research focused on how such flows are achieved. The question regarding their bioenergetics became even more interesting with the discovery of photosynthetic activity in some glandular trichomes. Despite recent advances, how primary metabolism contributes to the high metabolic fluxes in glandular trichomes is still not fully elucidated. Using computational methods and available multi-omics data, we first developed a quantitative framework to investigate the possible role of photosynthetic energy supply in terpenoid production and next tested experimentally the simulation-driven hypothesis. With this work, we provide the first reconstruction of specialised metabolism in Type-VI photosynthetic glandular trichomes of Solanum lycopersicum. Our model predicted that increasing light intensities results in a shift of carbon partitioning from catabolic to anabolic reactions driven by the energy availability of the cell. Moreover, we show the benefit of shifting between isoprenoid pathways under different light regimes, leading to a production of different classes of terpenes. Our computational predictions were confirmed in vivo, demonstrating a significant increase in production of monoterpenoids while the sesquiterpenes remained unchanged under higher light intensities. The outcomes of this research provide quantitative measures to assess the beneficial role of chloroplast in glandular trichomes for enhanced production of secondary metabolites and can guide the design of new experiments that aim at modulating terpenoid production., (© 2023 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.)

Plant specialized metabolites are often synthesized and stored in dedicated morphological structures such as glandular trichomes, resin ducts, or laticifers where they accumulate in large concentrations. How this high productivity is achieved is still elusive, in particular, with respect to the interface between primary and specialized metabolism. Here, we focus on glandular trichomes to survey recent progress in understanding how plant metabolic cell factories manage to balance homeostasis of essential central metabolites while producing large quantities of compounds that constitute a metabolic sink. In particular, we review the role of gene duplications, transcription factors and photosynthesis., Competing Interests: Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Copyright © 2022 Elsevier Ltd. All rights reserved.)

Tomato (Solanum lycopersicum L.) type VI glandular trichomes that occur on the surface of leaves, stems, young fruits and flowers produce and store a blend of volatile monoterpenes and sesquiterpenes. These compounds play important roles in the interaction with pathogens and herbivorous insects. Although the function of terpene synthases in the biosynthesis of volatile terpenes in tomato has been comprehensively investigated, the deciphering of their transcriptional regulation is only just emerging. We selected transcription factors that are over-expressed in trichomes based on existing transcriptome data and silenced them individually by virus-induced gene silencing. Of these, SlSCL3, a scarecrow-like (SCL) subfamily transcription factor, led to a significant decrease in volatile terpene content and expression of the corresponding terpene synthase genes when its transcription level was downregulated. Overexpression of SlSCL3 dramatically increased both the volatile terpene content and glandular trichome size, whereas its homozygous mutants showed reduced terpene biosynthesis. However, its heterozygous mutants also showed a significantly elevated volatile terpene content and enlarged glandular trichomes, similar to the overexpression plants. SlSCL3 modulates the expression of terpene biosynthetic pathway genes by transcriptional activation, but neither direct protein-DNA binding nor interaction with known regulators was observed. Moreover, transcript levels of the endogenous copy of SlSCL3 were decreased in the overexpression plants but increased in the heterozygous and homozygous mutants, suggesting feedback repression of its own promoter. Taken together, our results provide new insights into the role of SlSCL3 in the complex regulation of volatile terpene biosynthesis and glandular trichome development in tomato., (© 2021 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.)

Glandular trichomes are epidermal outgrowths that are the site of biosynthesis and storage of large quantities of specialized metabolites. Besides their role in the protection of plants against biotic and abiotic stresses, they have attracted interest owing to the importance of the compounds they produce for human use; for example, as pharmaceuticals, flavor and fragrance ingredients, or pesticides. Here, we review what novel concepts investigations on glandular trichomes have brought to the field of specialized metabolism, particularly with respect to chemical and enzymatic diversity. Furthermore, the next challenges in the field are understanding the metabolic network underlying the high productivity of glandular trichomes and the transport and storage of metabolites. Another emerging area is the development of glandular trichomes. Studies in some model species, essentially tomato, tobacco, and Artemisia, are now providing the first molecular clues, but many open questions remain: How is the distribution and density of different trichome types on the leaf surface controlled? When is the decision for an epidermal cell to differentiate into one type of trichome or another taken? Recent advances in gene editing make it now possible to address these questions and promise exciting discoveries in the near future., (© 2019 The Authors. New Phytologist © 2019 New Phytologist Trust.)

Plant glandular trichomes are able to secrete and store large amounts of volatile organic compounds (VOCs). VOCs typically accumulate in dedicated extracellular spaces, which can be either subcuticular, as in the Lamiaceae or Asteraceae, or intercellular, as in the Solanaceae. Volatiles are retained at high concentrations in these storage cavities with limited release into the atmosphere and without re-entering the secretory cells, where they would be toxic. This implies the existence of mechanisms allowing transport of VOCs to the cavity but preventing their diffusion out once they have been delivered. The cuticle and cell wall lining the cavity are likely to have key roles in retaining volatiles, but their exact composition and the potential molecular players involved are largely unknown., (Copyright © 2017 Elsevier Ltd. All rights reserved.)

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., (© 2017 American Society of Plant Biologists. All rights reserved.)

Background: Type VI glandular trichomes represent the most abundant trichome type on leaves and stems of tomato plants and significantly contribute to herbivore resistance, particularly in the wild species. Despite this, their development has been poorly studied so far. The goal of this study is to fill this gap. Using a variety of cell imaging techniques, a detailed record of the anatomy and developmental stages of type VI trichomes in the cultivated tomato (Solanum lycopersicum) and in a related wild species (S. habrochaites) is provided., Results: In both species, the development of these structures follows a highly reproducible cell division pattern. The two species differ in the shape of the trichome head which is round in S. habrochaites and like a four-leaf clover in S. lycopersicum, correlating with the presence of a large intercellular cavity in S. habrochaites where the produced metabolites accumulate. In both species, the junction between the intermediate cell and the four glandular cells constitute a breaking point facilitating the decapitation of the trichome and thereby the quick release of the metabolites. A strongly auto-fluorescent compound transiently accumulates in the early stages of development suggesting a potential role in the differentiation process. Finally, immuno-labelling with antibodies recognizing specific cell wall components indicate a key role of pectin and arabinogalactan components in the differentiation of type VI trichomes., Conclusions: Our observations explain the adaptive morphologies of type VI trichomes for metabolite storage and release and provide a framework for further studies of these important metabolic cellular factories. This is required to better exploit their potential, in particular for the breeding of pest resistance in tomato.

Rosemary (Rosmarinus officinalis) produces the phenolic diterpenes carnosic acid and carnosol, which, in addition to their general antioxidant activities, have recently been suggested as potential ingredients for the prevention and treatment of neurodegenerative diseases. Little is known about the biosynthesis of these diterpenes. Here we show that the biosynthesis of phenolic diterpenes in rosemary predominantly takes place in the glandular trichomes of young leaves, and used this feature to identify the first committed steps. Thus, a copalyl diphosphate synthase (RoCPS1) and two kaurene synthase-like (RoKSL1 and RoKSL2) encoding genes were identified and characterized. Expression in yeast (Saccharomyces cerevisiae) and Nicotiana benthamiana demonstrate that RoCPS1 converts geranylgeranyl diphosphate (GGDP) to copalyl diphosphate (CDP) of normal stereochemistry and that both RoKSL1 and RoKSL2 use normal CDP to produce an abietane diterpene. Comparison to the already characterized diterpene synthase from Salvia miltiorrhiza (SmKSL) demonstrates that the product of RoKSL1 and RoKSL2 is miltiradiene. Expression analysis supports a major contributing role for RoKSL2. Like SmKSL and the sclareol synthase from Salvia sclarea, RoKSL1/2 are diterpene synthases of the TPS-e group which have lost the internal gamma-domain. Furthermore, phylogenetic analysis indicates that RoKSL1 and RoKSL2 belong to a distinct group of KSL enzymes involved in specialized metabolism which most likely emerged before the dicot-monocot split., (Copyright © 2014 Elsevier Ltd. All rights reserved.)

Plant glandular trichomes are specialized secretory structures located on the surface of the aerial parts of plants with large biosynthetic capacity, often with terpenoids as output molecules. The collection of plant trichomes requires a method to separate trichomes from leaf epidermal tissues. For metabolite profiling, trichome tissue needs to be rapidly quenched in order to maintain the indigenous state of intracellular intermediates. Appropriate extraction and chromatographic separation methods must be available, which address the wide-ranging polarity of metabolites. In this chapter, a protocol for trichome harvest using a frozen paint brush is presented. A work flow for broad-range metabolite profiling using LC-MS(2) analysis is described, which is applicable to assess very hydrophilic isoprenoid precursors as well as more hydrophobic metabolites from trichomes and other plant tissues.

Sesquiterpene lactones (STLs) are bitter tasting plant specialized metabolites derived from farnesyl pyrophosphate (FPP) that contain a characteristic lactone ring. STLs can be found in many plant families that are distantly related to each other and outside the plant kingdom. They are especially prevalent in the plant families Apiaceae and Asteraceae, the latter being one of the largest plant families besides the Orchidaceae. The STL diversity is especially large in the Asteraceae, which made them an ideal object for chemosystematic studies in these species. Many STLs show a high bioactivity, for example as protective compounds against herbivory. STLs are also relevant for pharmaceutical applications, such as the treatment of malaria with artemisinin. Recent findings have dramatically changed our knowledge about the biosynthesis of STLs, as well as their developmental, spatial, and environmental regulation. This review intents to update the currently achieved progress in these aspects. With the advancement of genome editing tools such as CRISPR/Cas and the rapid acceleration of the speed of genome sequencing, even deeper insights into the biosynthesis, regulation, and enzyme evolution of STL can be expected in the future. Apart from their role as protective compounds, there may be a more subtle role of STL in regulatory processes of plants that will be discussed as well. [ABSTRACT FROM AUTHOR]

The leaves of the wild tomato Solanum galapagense harbor type-IV glandular trichomes (GT) that produce high levels of acylsugars (AS), conferring insect resistance. Conversely, domesticated tomatoes (S. lycopersicum) lack type-IV trichomes on the leaves of mature plants, preventing high AS production, thus rendering the plants more vulnerable to insect predation. We hypothesized that cultivated tomatoes engineered to harbor type-IV trichomes on the leaves of adult plants could be insect-resistant. We introgressed the genetic determinants controlling type-IV trichome development from S. galapagense into cv. Micro-Tom (MT) and created a line named "Galapagos-enhanced trichomes" (MT-Get). Mapping-by-sequencing revealed that five chromosomal regions of S. galapagense were present in MT-Get. Further genetic mapping showed that S. galapagense alleles in chromosomes 1, 2, and 3 were sufficient for the presence of type-IV trichomes on adult organs but at lower densities. Metabolic and gene expression analyses demonstrated that type-IV trichome density was not accompanied by the AS production and exudation in MT-Get. Although the plants produce a significant amount of acylsugars, those are still not enough to make them resistant to whiteflies. We demonstrate that type-IV glandular trichome development is insufficient for high AS accumulation. The results from our study provided additional insights into the steps necessary for breeding an insect-resistant tomato. [ABSTRACT FROM AUTHOR]

Glandular trichomes contribute to the high resistance of wild tomato species against insect pests not only thanks to the metabolites they produce but also because of morphological and developmental features which support the high production of these defense compounds. In Solanum habrochaites , type VI trichomes have a distinct spherical shape and a large intercellular storage cavity where metabolites can accumulate and are released upon breaking off of the glandular cells. In contrast, the type VI trichomes of S. lycopersicum have a four-leaf clover shape corresponding to the four glandular cells and a small internal cavity with limited capacity for storage of compounds. To better characterize the genetic factors underlying these trichome morphological differences we created a back-cross population of 116 individuals between S. habrochaites LA1777 and S. lycopersicum var. cerasiforme WVa106. A trichome score that reflects the shape of the type VI trichomes allowing the quantification of this trait was designed. The scores were distributed normally across the population, which was mapped with a total of 192 markers. This resulted in the identification of six quantitative trait locus (QTLs) on chromosomes I, VII, VII, and XI. The QTL on chromosome I with the highest LOD score was confirmed and narrowed down to a 500 gene interval in an advanced population derived from one of the back-cross lines. Our results provide the foundation for the genetic dissection of type VI trichome morphology and the introgression of these trichome traits into cultivated tomato lines for increased insect resistance. Key Message: This work shows that the shape of type VI glandular trichomes in tomato is a genetically defined trait controlled by multiple QTLs with one on chromosome I being the major contributor. [ABSTRACT FROM AUTHOR]

Plants have a remarkable capacity for the production of a wide range of metabolites. Much has been reported and reviewed on the diversity of these metabolites and how it is achieved, for example through the evolution of enzyme families. In comparison, relatively little is known on the extraordinary metabolic productivity of dedicated organs where many of these metabolites are synthesized and accumulate. Plant glandular trichomes are such specialized metabolite factories, for which recent omics analyses have shed new light on the adaptive metabolic strategies that support high metabolic fluxes. In photosynthetic trichomes such as those of the Solanaceae, these include CO 2 refixation and possibly C4-like metabolism which contribute to the high productivity of these sink organs. [ABSTRACT FROM AUTHOR]

The industrial relevance of a number of metabolites produced in plant glandular trichomes (GTs) has spurred research on these specialized organs for a number of years. Most of the research, however, has focused on the elucidation of secondary metabolite pathways and comparatively little has been undertaken on the development and differentiation of GTs. One way to gain insight into these developmental processes is to generate stage-specific transcriptome and metabolome data. The difficulty for this resides in the isolation of early stages of development of the GTs. Here we describe a method for the separation and isolation of intact young and mature type VI trichomes from the wild tomato species Solanum habrochaites. The final and key step of the method uses cell sorting based on distinct autofluorescence signals of the young and mature trichomes. We demonstrate that sorting by flow cytometry allows recovering pure fractions of young and mature trichomes. Furthermore, we show that the sorted trichomes can be used for transcript and metabolite analyses. Because many plant tissues or cells have distinct autofluorescence components, the principles of this method can be generally applicable for the isolation of specific cell types without prior labeling. [ABSTRACT FROM AUTHOR]

Leaves of tobacco ( Nicotiana tabacum) are covered with glandular trichomes that produce sucrose esters and diterpenoids in varying quantities, depending on cultivar type. The bicyclic diterpene Z-abienol is the major labdanoid present in some oriental tobacco cultivars, where it constitutes a precursor of important flavours and aromas. We describe here the identification and characterization of two genes governing the biosynthesis of Z-abienol in N. tabacum. As for other angiosperm labdanoid diterpenes, the biosynthesis of Z-abienol proceeds in two steps. NtCPS2 encodes a class-II terpene synthase that synthesizes 8-hydroxy-copalyl diphosphate, and NtABS encodes a kaurene synthase-like (KSL) protein that uses 8-hydroxy-copalyl diphosphate to produce Z-abienol. Phylogenetic analysis indicates that NtABS belongs to a distinct clade of KSL proteins that comprises the recently identified tomato ( Solanum habrochaites) santalene and bergamotene synthase. RT-PCR results show that both genes are preferentially expressed in trichomes. Moreover, microscopy of NtCPS2 promoter-GUS fusion transgenics demonstrated a high specificity of expression to trichome glandular cells. Ectopic expression of both genes, but not of either one alone, driven by a trichome-specific promoter in transgenic Nicotiana sylvestris conferred Z-abienol formation to this species, which does not normally produce it. Furthermore, sequence analysis of over 100 tobacco cultivars revealed polymorphisms in NtCPS2 that lead to a prematurely truncated protein in cultivars lacking Z-abienol, thus establishing NtCPS2 as a major gene controlling Z-abienol biosynthesis in tobacco. These results offer new perspectives for tobacco breeding and the metabolic engineering of labdanoid diterpenes, as well as for structure-function relationship studies of terpene synthases. [ABSTRACT FROM AUTHOR]

Summary Glandular trichomes cover the surface of many plant species. They exhibit tremendous diversity, be it in their shape or the compounds they secrete. This diversity is expressed between species but also within species or even individual plants. The industrial uses of some trichome secretions and their potential as a defense barrier, for example against arthropod pests, has spurred research into the biosynthesis pathways that lead to these specialized metabolites. Because complete biosynthesis pathways take place in the secretory cells, the establishment of trichome-specific expressed sequence tag libraries has greatly accelerated their elucidation. Glandular trichomes also have an important metabolic capacity and may be considered as true cell factories. To fully exploit the potential of glandular trichomes as breeding or engineering objects, several research areas will have to be further investigated, such as development, patterning, metabolic fluxes and transcription regulation. The purpose of this review is to provide an update on the methods and technologies which have been used to investigate glandular trichomes and to propose new avenues of research to deepen our understanding of these specialized structures. [ABSTRACT FROM AUTHOR]