Abstract
Glandular trichomes, the epidermal projections over aerial plant parts primarily function in defense against stresses including protection from insects and microbes. These structures are characterized by dedicated genetic machinery for overproduction of structurally diverse secondary metabolites. Certain secondary metabolites of trichome origin display interesting pharmacological activities, and therefore are of immense economical interest as drug, aroma and allelochemicals. For obvious reasons, glandular trichomes have been focus of ‘omics’ studies, particularly for elucidating molecular basis of such a large scale production of secondary metabolites. In the last decade, next generation sequencing has fueled the development of transcriptome landscapes of glandular trichomes of several medicinal and aromatic plants. Taken together, these studies have started to unravel gene and metabolic networks operating in glandular trichomes, and therefore are potentially useful for identification of novel molecular targets for strategic metabolic engineering of economically important secondary metabolites as well as for development of stress tolerant plant varieties. The present book chapter will update our current knowledge about aspects of glandular trichome biology including its applied value in plant biology.
Authors Maridul Kundan, Umar Gani, and Abhishek Kumar Nautiyal are equally contributed.
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17.1 Introduction
A vast number of Angiosperms possess hair-like epidermal structures which are termed as trichomes. Sometimes, similar structures have also been reported in gymnosperms, bryophytes (Uphof 1962), lichens and algae (Engene et al. 2012). Trichomes are primarily present on surface of leaves and stem, but they are also found on petals, petioles, peduncles and seeds, depending upon the species. Trichomes display tremendous diversity in terms of cellular organization, structure and chemistry. These structures can be broadly divided into two categories—glandular and non glandular, depending upon their morphology and secretion ability (Fahn 2000; Kolb and Muller 2004). Irrespective of the types, all the trichomes originate from epidermal cells. Some of the epidermal cells elongate and modify into unicellular trichomes or may undergo division and specialization to develop into multicellular trichomes. Glandular trichomes, characterized by presence of gland cell(s) or secretory cell(s) have been reported in approximately 30% of all vascular plant species (Fahn 2000) and in a single plant species several types of trichomes (both glandular and non-glandular) have been reported to be present together. Owing to their remarkable ability to biosynthesize, store and secrete a range of secondary metabolites, the glandular trichomes are often referred to as biofactories of specialized metabolites. They secrete a mixture of chemicals that often offer a vast array of uses in the pharmaceutical, pesticides and flavour & fragrance industries, besides playing important role in plant biology. These structures are regarded as suitable systems for studying molecular basis of cellular differentiation and biosynthesis of specialized plant metabolites. For obvious reasons, there have been emerging interests to study the gene expression and metabolism in these structures with main focus on identification of genes involved in biosynthesis of trichome specific natural products. Thus, due to their wide occurrence, usage as development model and many other important functions, glandular trichomes have been of academic and applied significance.
17.2 Morphology and Classification of Glandular Trichomes
Glandular trichomes have a multicellular structure, consisting of a stalk, which is terminated by a glandular head (Turner et al. 2000). They are developed from a single protodermal cell, which following vertical enlargement and multiple divisions develop into a trichome structure. On the basis of structure and cellular organization, glandular trichomes can be subdivided into two major classes, namely peltate and capitate trichomes (Fig. 17.1) (Werker 2000). The peltate trichomes are generally characterized by presence of a short stalk, composed of one or two cells, and large head, comprising of four to eight secretory cells, having a large sub-cuticular space (Turner et al. 2000; Werker 2000). The secretory cells are remarkably active in biosynthesizing metabolites that along with other molecules are transported out and stored in a prominent sub-cuticular space. Capitate trichomes are characterized by presence of a single basal cell, which is embedded within the epidermal layer, one or two stalk cells and one or two spherical secretory heads (Werker 2000; Bisio et al. 1999). The Solanum sp., for example are characterized by presence of eight types of trichomes. Out of them, four (i.e., type I, IV, VI and VII) are glandular capitate trichomes and the rest (i.e., type II, III, V and VIII) are non-glandular (Glas et al. 2012). The type I and IV glandular trichomes are capitate, whereas type VI and VII appear to display a peltate structure. These types differ in number of stalk and secretory cells. In S. lycopersicum, Type I and Type VI are the two abundant types of glandular trichomes (McDowell et al. 2011). Type I trichomes consist of a multicellular stalk with a single, small gland cell at the tip where as Type VI trichomes have a unicellular stalk with a four-cell glandular head. The glandular trichomes of Nicotiana tabacum, N. sylvestris and N. rustica exhibit very similar features, characterized by presence of 4 to 6 stalk cells and 1 to 6 head cells. In N. tabacum, usually, two types of capitate glandular trichomes are found (Shepherd et al. 2005); the larger ones with a long stalk and a chlorophyllous head due to presence of chloroplast, and the smaller ones with a short stalk and non- chlorophyllous head. In contrast to the long trichomes, short trichomes do not possess chloroplasts in their head cells. In the members of Lamiaceae, for example, Ocimum sp. and Mentha piperita (mint), both types of glandular trichomes are present together. The Mentha species has non-glandular trichomes, peltate glandular trichomes and capitate glandular trichomes, present on abaxial and adaxial surfaces of the leaf.
Types of glandular trichomes. a and c Schematic diagrams showing peltate and capiate trichomes, respectively. b Scanning electron microscopic view of leaf surface of a member of family lamiaceae showing peltate trichome (Author’s own lab, unpublished picture). d Light microscopic view of leaf surface of N. tabacum showing glandular trichomes
17.3 Glandular Trichomes as Source of Economically Important Natural Products
The glandular trichomes have the ability to synthesise, store and secrete diverse secondary metabolites such as terpenoids (Gershenzon and Dudareva 2007), flavonoids (Treutter 2006), phenylpropenes (Gang et al. 2002), methyl ketones (Fridman et al. 2005) and acyl sugars (Kroumova and Wagner 2003). Many of these secondary metabolites are of human interest and utilized as pharmaceuticals and neutraceuticals (Table 17.1) (Mahmoud and Croteau 2002; Schilmiller et al. 2008). For instance, Lamiaceae, an important aromatic plant family with species such as Basil (Ocimum basilicum), lavender (Lavandula spica), mint (Mentha × piperita), oregano (Origanum vulgare) and thyme (Thymus vulgaris), is renowned for its essential oil, which is produced exclusively in glandular trichomes (Schilmiller et al. 2008). Artemisinin, a sesquiterpene lactone, produced in the glandular trichomes of Artemisia annua (a member of Asteraceae family), is used as an effective drug for the treatment of malaria (Duke et al. 1994; Weathers et al. 2011). The glandular trichomes of Cannabis sativa are source of unique terpeno-phenolic compounds, known as cannabinoids. The Tetrahydrocannabinol (THC)-a psychoactive cannabinoid displays anti-nausea and anti-cancer activities (Sirikantaramas et al. 2005; Pellati et al. 2008) whereas Cannabidiol (CBD)—a non psychoactive cannabinoid has been found to be effective in prevention of neurodegenerative and cardiovascular diseases (Pellati et al. 2008; Taura et al. 2007). Gossypol and other related disesquiterpene produced by the trichomes of Gossypium hirsutum (cotton), possessing anti-fungal activities are potential natural pesticides (Mellon et al. 2014; Dayan and Duke 2003). The labdane-type diterpenes, produced in trichomes of Cistus creticus (Pink Rock-Rose) trichomes exhibit gastric antiulcer (Attaguile et al. 1995), antifungal, antibacterial and anti-inflammatory activities (Demetzos et al. 1997; Demetzos et al. 2001). M. piperita trichomes produce monoterpenes including menthone and menthol (Lange et al. 2000) where as M. spicata (spearmint) produces carvone, that gives attribute like odour and taste to the plant and have been used as flavouring agent in food and pharmaceutical preparations (Chauhan et al. 2009). Several species from Solanaceae family like Solanum lycopersicum, S. habrochaites and S. pennellii contain diverse metabolites in their glandular trichomes such as monoterpenes, sesquiterpenes, methylketones, diterpenes and acyl sugars (Antonious 2001; Besser et al. 2009); The glandular trichomes of Ocimum basilicum (Basil) secrete phenylpropanoids (Gang et al. 2002); gland exudates of Medicago sativa (alfa alfa) contain lipophilic amides (Ranger et al. 2005) and accumulate flavonoids that contributes to the plant’s antioxidant properties (Aziz et al. 2005). The glandular trichomes of Salvia sclarea (clary sage) trichomes accumulates sclareol—a labdane diterpene, that is used as precursor for Ambrox or Ambroxane, which finds application in flavour and fragrance industry (Moulines et al. 2004; Frija et al. 2011).
17.4 Role of Glandular Trichomes in Plant Biology
Trichomes cover the outermost layer of plant organs such as leaf and stem and thereby are directly exposed to the surroundings to encounter prevailing, changing and often challenging growth conditions. In this regard, these structures can act as a component of physical defense system of plants against insects, pathogens and some abiotic stresses (Fig. 17.2). In addition, owing to the appreciable biosynthetic capabilities for producing secondary metabolites, the glandular trichomes are involved in ecological interactions, including chemical defense against invading pathogens and insects (Runyon et al. 2010; Tian et al. 2012).
Schematic representation summarizing role of trichomes in stress
17.4.1 Role in Abiotic Stress Tolerance
Abiotic stress conditions trigger an array of morphological, physiological, molecular and biochemical changes that drastically affect plant growth and development and remains the major constraint to crop yield. In the recent past, several studies have demonstrated that trichomes under adverse abiotic environmental conditions play a vital role in the plant survival.
17.4.1.1 Role in Heavy Metal Detoxification and Homeostasis
The extensive and burgeoning accumulation of heavy metals (HMs) in the biosphere due to anthropogenic disturbances has become a predicament condition for all forms of life including both plants and animals. HMs are non-biodegradable, inorganic chemical constituents which inflict detrimental effects on plants and animals including humans (Cirlakova 2009). HMs at elevated levels can hamper the functions of several important cellular biomolecules such as DNA, nuclear proteins, enzymes and pigments which can lead to excessive generation of reactive oxygen species (ROS) (Zengin and Munzuroglu 2005; Ali et al. 2013). The increased generation of ROS such as superoxide free radicals (O2⋅−), hydroxyl free radicals (OH⋅−) or non-free radical species such as singlet oxygen (1O2) and hydrogen peroxide (H2O2) due to disturbance of cellular homeostasis cause an imbalance between ROS generation and scavenging, results in oxidative stress (Sytar et al. 2013). This stress condition implicates serious deteriorative anomalies within plant cells such as DNA damage, protein degradation, redox imbalance, leakage of ions, and disruption of cell components and membranes which ultimately can lead to cell death via programmed cell death (PCD) pathways (Sharma et al. 2012).
Plants have evolved a repertoire of defense strategies to cope with heavy metal stress (Kupper and Kroneck 2005). Trichomes have been implicated in ion homeostasis and heavy metal detoxification process either by serving as storage sites for HMs or as secretion sites of a wide array of secondary metabolites that counteract perilous effects of heavy metal contamination (Hauser 2014). The HMs have been found to be accumulated in the trichomes of both hyper (Sarret et al. 2006; Broadhurst et al. 2004) and non-hyper accumulating (Lavid et al. 2001; Dominguez-Solis et al. 2004) plants. The role of trichomes in heavy metal sequestration and detoxification has been studied in details in N. tabacum. On exposure of tobacco plant to the toxic level of cadmium (Cd), trichomes were reported to be the primary sites on the leaf surface, which are engaged in exudation of Cd crystals. Also cysteine synthase overexpressing tobacco lines showed Cd tolerance with 20% less endogenous Cd concentration as compared to wild-type plants and its trichome density has been reported to be 25% higher than the wild-type control plants (Harada and Choi 2008). The sequencing of cDNA libraries corresponding to the trichomes of tobacco, with or without Cd treatment revealed that trichomes are the primary sites of expression of genes encoding for stress related proteins such as antipathogenic T-phylloplanin-like proteins, glutathione peroxidase and many other classes of pathogenesis-related (PR) proteins. Furthermore, the glutathione levels were found to be elevated in the tip cells of trichomes as compared to other cells, reflecting the existence of a well developed sulfur-dependent protective system for heavy metal detoxification. Higher expression of genes encoding metallothionins, functioning in metal tolerance has been documented in trichomes of some plants species such as Vicia faba (Foley and Singh 1994). These observations clearly indicate that trichomes have well developed molecular machinery for accumulation, sequestration and exudation of heavy metals.
17.4.1.2 Role in Ozone Stress
During the past century, average tropospheric global ozone (O3) concentration has drastically elevated and is expectedly increasing further (Hartmann et al. 2014; Oltmans et al. 2013). Several reports suggest that elevated level of atmospheric O3 inhibits plant growth and development and results in decrease in productivity (Ainsworth et al. 2012; Fares et al. 2013). Certain plants show more tolerance to ozone stress than others but the underlying mechanism is still not well understood (Ainsworth 2017; Feng et al. 2017). In plants O3 enters mainly via the stomata and reacts with organic molecules in the apoplast and resulting in excessive generation of ROS and ultimately leading to cell damage and cell death (Ainsworth 2017; Cho et al. 2011; Kanagendran et al. 2017). Studies were conducted to investigate the role of glandular and non-glandular trichomes in response to ozone stress. In order to cover a broad range of trichome characteristics, such as trichome density, trichome type etc. twenty-three herbaceous plant species were selected for this study and it was reported that peltate and capitate glandular trichomes showed significant level of tolerance against ozone stress whereas no such resistance was observed in non-glandular trichomes. Also species with lower glandular trichomes on their leaf surface were found to be more vulnerable to ozone stress as compared to those with higher density of glandular trichomes. These results shed light on the possible role of glandular trichome in the reduction of ozone toxicity and may function as chemical barricades that play a key role in neutralizing the toxic O3 before entering into the apoplast (Li et al. 2017).
Apart from this, there are several reports from many species which proposed that glandular trichomes might play role in tolerance to drought stress. For example, a study in tomato found that overexpression of SIMX1, a MIXTA like MYB transcription factor, led to enhanced trichome density including both glandular and non-glandular trichomes accompanied with increased drought tolerance but yet there are no concrete evidences of the role of glandular trichomes specifically involved in imparting the drought tolerance (Ewas et al. 2016).
17.4.2 Role in Biotic Stress Tolerance
Various biotic factors are the major threats to the productivity of large number of important plant species. Several studies demonstrated that trichomes act as chemical defense barrier against insects, pests, herbivores, fungal infections, and even plants of parasitic behaviour (Tian et al. 2012; Peiffer et al. 2009). Apart from non-glandular trichomes, glandular trichomes synthesize and/or accumulate highly interesting secondary metabolites such as terpenoids, phenylpropenes, methyl ketones (Fridman et al. 2005; Ben-Israel et al. 2009), proteinase inhibitors (Tian et al. 2012) and acyl sugars (Schilmiller et al. 2012; Stout et al. 2012; Xu et al. 2013) and contribute substantially to chemical arsenal of plant defense strategies and thus play a fundamental role in both structural and chemical defense strategy against several herbivory and pathogen attacks and are interesting targets for breeding (Glas et al. 2012; Gruber et al. 2006).
17.4.2.1 Insect Resistance
Recent studies in many tomato wild relatives have reported the correlation of the presence, longevity, density, and size of the type I and the shorter multicellular type IV glandular trichomes with resistance against the whitefly (Firdaus et al. 2013). Previously, studies found that suppression of a glandular trichome specific P450 hydroxylase gene in tobacco led to resistance against aphids. The analysis of P450 suppressed transgenic tobacco plants displayed elevated concentration of cembratriene-ol (CBT-ol) which displayed potent aphidicidal activity (Wang et al. 2001). NtLTP1, a glandular-specific lipid transfer protein from tobacco has been implicated in secretion of lipid compounds from trichome heads. The transgenic tobacco lines overexpressing NtLTP1 displayed enhanced tolerance to aphids (Choi et al. 2012). The investigation of the effect of the hairless (hl) mutation on trichome density, chemical composition and herbivory resistance in tomato suggested that leaf surface extracts have low levels of sesquiterpene and polyphenolic compound and hl mutation causes structural distortion of trichomes in leaf tissue and leads to decreased tolerance against insect herbivory (Kang et al. 2010).
17.4.2.2 Resistance Against Pathogens
Glandular trichomes are often capable of secreting exudates displaying antifungal activities. In a wild potato species (S. berthaultii), a trichome exudate was reported to confer resistance to Phytophthora infestans (Lai et al. 2000). The disease incidence has shown negative correlation with the density and polyphenol-oxidase activity of short type A trichome bearing a four-lobed membrane-bound gland at their tips. In chickpea (Cicer arietinum) the concentration of a highly acidic trichome exudate is critical in response to infection by Ascochyta rabiei. Low concentrations of exudates promote germination of Ascochyta rabiei conidia whereas high concentrations inhibit its germination (Armstrong-Cho and Gossen 2005). The damaged trichomes have been observed as entry sites for the infection and colonialization of several different fungal pathogens such as Phoma clematidina on clematis (Van De Graaf et al. 2002), powdery mildew (Erysiphe necator) on grapevine buds (Rumbolz and Gubler 2005), Botrytis cinerea on harvested tomato (Charles et al. 2008), and Beauveria bassiana on poppy (Landa et al. 2013). A trichome specific glycoprotein known as T-phylloplanin in tobacco was reported to be a potent inhibitor of oomycete Peronospora tabacina germination (Kroumova et al. 2007). Also tobacco plants with low expression of phylloplanin are more susceptible to pathogen attacks. Altogether the above mentioned examples clearly provide ample evidences of the active role of trichomes in imparting stress tolerance to several biotic stresses and mediating ecological interactions.
17.5 Omics Approaches for Studying Gene Expression and Function in the Context of Glandular Trichome Biology
Apart from being sources of economically important natural products, trichomes function as physical and chemical defense structures. These structures therefore are interesting systems to understand the molecular basis of secondary metabolism and plant defense. The “Omics” approaches such as transcriptomics, proteomics and metabolomics can provide detailed information about the metabolic and gene regulatory networks operating in trichomes to favour secondary metabolism and defense responses. Initial studies based on Sanger sequencing of cDNA libraries of trichomes provided limited but useful information about the transcriptome landscape of trichomes. Later on, application of next generation sequencing (NGS) revolutionized the area of trichome biology by providing comprehensive information about genes expressing in trichomes (Table 17.2). A dedicated database, TrichOme hosting transcriptomics (ESTs/unigene sequences) and metabolomics (mass-spectrometry-based trichome metabolite profiles) resources of trichomes of a number of plant species is available (Dai et al. 2010) (http://www.planttrichome.org/). The “Omics” approaches have revealed that genes involved in secondary metabolism, defense response, and lipid biosynthesis are enriched in transcriptomes of glandular trichomes. Several medicinal and aromatic plants have been studied for identification and characterization of genes expressing in glandular trichomes (Table 17.3). These studies have been vital for elucidation of molecular basis of biosynthesis of several important natural products as well as for functional attributes of trichomes (Huchelmann et al. 2017; Tissier 2018). In the following heads, the features of gene expression in glandular trichomes have been summarized.
17.5.1 Genes Encoding Enzymes of Secondary Metabolism
Sanger sequencing of cDNA libraries corresponding to the glandular trichomes of N. tabacum and N. sylvestris, for example, provided platform for identification of genes involved in the trichome specific secondary metabolism leading to cembrenoid and labdanoid diterpenoid biosynthesis (Wang et al. 2001, 2002; Wang and Wagner 2003; Ennajdaoui et al. 2010; Sallaud et al. 2012). A terpene synthase named as cembratriene-ol synthase (CBTS) and CYP71D16, a CYP450 enzyme have been shown to be involved in cembrenoid biosynthesis. The labdanoid biosynthesis, on the other hand is driven by enzymes namely copalyl diphosphate synthase 2 (CPS2) and abienol synthase (ABS). The expression of the genes encoding CBTS, CYP71D16, CPS2 and ABS was reported to be trichome specific and therefore their promoter regions can be used for driving trichome specific gene expression. In addition, the characterization of genes expressing primarily in glandular trichomes led to the discovery of metabolic pathways involved in natural product biosynthesis in several medicinal and aromatic plants. C. sativa, for example, biosynthesize bioactive cannabinoids, primarily in the glandular trichomes of female flower. The genes involved in the cannabinoid biosynthesis have been identified using transcriptome resource of glandular trichomes of C. sativa, which in turn helped in elucidation of the pathway at molecular level (Sirikantaramas et al. 2005; Taura et al. 2007, 2009; Page and Boubakir 2011).
The terpenoid biosynthesis necessitates substrate supply in the form of isoprene units. Two pathways, namely mevalonate (MVA) and 2-C-methyl-D-erythritol-4-phosphate (MEP) pathway, localized in cytoplasm and plastids, respectively are responsible for generation of isoprene pool. As the glandular trichomes are often enriched in terpenoid class of secondary metabolites, for example, those having monoterpene, diterpene and sesquiterpene backbones, the key genes involved in the MVA and MEP pathways such as DXS and HMGR, respectively are upregulated in glandular trichome as compared to trichome free leaf sample (Glas et al. 2012; Huchelmann et al. 2017; Balcke et al. 2017; Wang et al. 2009). Likewise, genes involved in the biosynthesis of flavonoid and phenylpropanoid class of secondary metabolites have been reported to display higher transcript levels in glandular trichomes.
17.5.2 Gene Involved in Primary Metabolism
The impressively active metabolism requires sufficient primary Carbon flux and energy to support excessive production of secondary metabolites in glandular trichomes. In this regard, transcriptomic and proteomic studies on glandular trichomes suggested modulation of genes involved in primary metabolism as compared to trichome-free leaf. The long glandular trichomes of tobacco contains chlorophyllous head cell and can photosynthesize. Using proteomics approach, a novel Rubisco small subunit (NtRbcS-T), preferentially expressing in head cells of long glandular trichomes of tobacco was identified. NtRbcS-T was implicated in carbon fixation in gland cell having a cellular environment overproducing specialized metabolites along with CO2 evolution (Laterre et al. 2017). A systems approach involving proteomics, metabolomics and transcriptomics in type VI glandular trichomes and leaves from a cultivated tomato variety (Solanum lycopersicum LA4024) provided important insights into carbon flux regulation, source of reducing power and energy to support intensified metabolism in these trichomes (Balcke et al. 2017). It was demonstrated that although type VI glandular trichomes are photosynthetically active, the major carbon flux to support trichome specific metabolism comes from leaf tissue. However, the reducing power and energy generated during photosynthesis can be utilized in driving secondary metabolism (Balcke et al. 2017).
The “Omics” studies on N. tabacum and tomato revealed that the genes involved in the metabolism of branched chain amino acids e.g. valine, leucine, isoleucine are upregulated in the glandular trichomes as compared to the trichome-free leaf (Balcke et al. 2017; Jin et al. 2014). These observations are consistent with the role of branched chain amino acids as precursors of acyl-sugars, which are enriched in the glandular trichomes of N. tabacum and tomato. The glandular trichomes, in addition, were reported to display higher expression of genes involved in lipid metabolism, especially those concerning with the biosynthesis of polyunsaturated fatty acids and wax (Balcke et al. 2017; Jin et al. 2014; Sallets et al. 2014).
17.5.3 Transporter Genes
Gene expression analysis revealed that the genes encoding transporter proteins belonging to ABC family transporters and Lipid transporter protein (LTP) are preferentially expressed in glandular trichomes. By now, however, only limited number of transporter genes expressing in glandular trichomes have been functionally characterized. An ABCG subfamily transporter gene, named as NtPDR1, displaying higher expression in the gland cells of long glandular trichomes of N.tabacum has been implicated in transportation of terpenoid compounds such as diterpenoids and sesquiterpenoids (Pierman et al. 2017). In A. annua, another ABCG sub-family transporter, namely AaPDR3, whose expression is primarily restricted to the glandular trichomes, has been shown to be involved in transportation of β-caryophyllene (Fu et al. 2017). In N. tabacum, NtLTP1, a gene encoding lipid transporter protein is involved in secretion of lipids from glandular trichomes (Choi et al. 2012).
17.5.4 Genes Involved in Abiotic and Biotic Stresses
The glandular trichomes have been reported to express genes involved in abiotic and biotic stress responses. For example, genes belonging to these functional classes putatively encode PR protein, metallothionein, T-phylloplanin RD22-like BURP domain-containing proteins, and thaumatin-like protein, ascorbate peroxidise, glutathione peroxidase, Fe- superoxide dismutase etc. (Sallets et al. 2014; Marks et al. 2009; Cui et al. 2011). The T-phyllopanin gene, displaying glandular trichome specific expression in N. tabacum has been demonstrated to confer defense against pathogens (Shepherd et al. 2005).
17.6 Transcription Factor Genes Involved in the Regulation of Secondary Metabolism in Glandular Trichomes
Transcription factors play central role in regulation of gene expression associated with metabolic pathways. Limited information pertaining to the transcription factors regulating glandular trichome localized metabolism is currently available. Their identification and characterization is, however, crucial for unveiling molecular mechanism involved in the trichome specific expression of structural genes of secondary metabolism. A number of transcription factors belonging to diverse families have been identified with respect to transcriptional regulation of structural genes of artemisinin biosynthesis in A. annua. The transcription factors namely AaWRKY1, AaERF1/2, AaORA, AaMYC2, AabZIP1, AaNAC1 and AaSPL2 positively regulate the expression of genes involved in artemisinin biosynthesis (Yu et al. 2012; Lu et al. 2013; Zhang et al. 2015; Jiang et al. 2016; Shen et al. 2016; Lv et al. 2016; 2019). These transcription factors often regulate multiple structural genes simultaneously and therefore play crucial role in fine-tuning of the secondary metabolism under spatial and temporal cues including hormone signaling. In Mentha spicata, transcription factor genes namely MsYABBY5 and MsMYB displaying preferential expression in peltate glandular trichomes have been implicated in the regulation of monoterpene production (Wang et al. 2016; Reddy et al. 2017). Another glandular trichome specific transcription factor gene, Expression of terpenoid 1 (EOT1), belonging to SHI transcription factor family has been demonstrated to regulate terpenoid biosynthesis in S. lycopersicum (Spyropoulou et al. 2014).
17.7 Regulatory Genes Involved in Development of Glandular Trichomes
The studies on Arabidopsis have provided detailed information about the molecular players involved in the initiation, development and patterning of non-glandular trichomes (Serna and Martin 2006; Pattanaik et al. 2014). It was established that a complex of three regulatory proteins, viz. MYB, bHLH and WD40 proteins (MBW) plays a central role in the regulation of trichome development in Arabidopsis. In general, the understanding of molecular mechanism of regulation of glandular trichome development is comparatively very limited and it is not clear whether a MBW like regulatory complex is involved in the regulation of glandular trichome development. The studies, conducted so far, have however revealed that transcription factors, mostly belonging to Homeodomain Zipper (HD-Zip), C2H2 Zinc Finger, bHLH and MYB familes are involved in the regulation of glandular trichome development. With the current information, it is also apparent that these regulators might be functionally conserved. Overexpression of AmMIXTA, an R2-R3 MYB family transcription factor gene resulted in enhanced density of glandular trichome in N. tabacum. Similarly, MIXTA like transcription factors, SlMIXTA1 and AaMIXTA positively regulate glandular trichome development in tomato and A. annua, respectively (Ewas et al. 2016; Shi et al. 2018). A HD-Zip transcription factor gene, named as Wooly (Wo) has been implicated in the regulation of glandular trichome development in tomato (Yang et al. 2011). The overexpression of mutant allele of tomato Wo gene resulted in modified glandular trichome development in N. tabacum, suggesting that orthologs of Wo gene could be functionally conserved regulators in Solanaceae (Yang et al. 2015). Recently, a C2H2 Zinc finger transcription factor gene, namely Hair (H) has been identified as positive regulator of glandular trichome development in S. lycopersicum. It was also demonstrated that H interacts with Wo and thereby they might regulate trichome development in a combinatorial manner (Chang et al. 2018). Members of HD-Zip transcription factor families have also been shown to regulate glandular trichome development in A. annua (Yan et al. 2017) and Cucumis sativus (Liu et al. 2016). Recently, a bHLH transcription factor, SlMYC1 has been identified as regulator of the development of type VI glandular trichomes as well as terpenoid biosynthesis in tomato (Xu et al. 2018).
17.8 Conclusions and Future Outlook
Glandular trichomes belong to defense repertoire of plants against invading pest and pathogens. These structures have also been implicated in conferring tolerance against abiotic stresses such as drought, UV and heavy metal challenge. The impressively active metabolic and genetic machinery enable them to overproduce, accumulate and secrete secondary metabolites that include some economically important natural products. For obvious reasons, glandular trichomes have potential to be developed as production system for economically important secondary metabolites through strategic metabolic engineering involving tools of genome engineering. This approach appears to be attractive to fuel the attempts towards development of alternate production system for those secondary metabolites, which are biosynthesized by rare and endangered plant species. The next generation transcriptome sequencing and other related approaches have been instrumental in identification of genes involved in the trichome specific natural product biosynthesis. However, a detailed understanding of metabolic and gene regulatory networks leading to the biosynthesis and accumulation of metabolites in glandular trichomes awaits further investigations. There is also a need of isolation and characterization of novel and highly active trichome specific promoters. Another important area of research is to understand molecular basis of glandular trichome development, which, as of now, remains poorly understood. The knowledge about molecular regulators of glandular trichome development will be useful in enhancing trichome density and thereby the yield of trichome localized metabolites. Further, glandular trichomes can serve as a rich pool of useful genes which could be potential targets for systematic transgenesis towards development of plants tolerant to environmental stresses. However, by now, only a limited number of genes, particularly those involved in secondary metabolism in trichomes have been characterized. It is therefore desirable to carry out investigations pertaining to the elucidation of functions of other trichome specific genes. Altogether the comprehensive and detailed knowledge of fundamental aspects of trichome biology will provide new leads to plant biologists to exploit the untapped biotechnological potential of trichomes to engineer plants that would exhibit increased resistance to pests and tolerance to many abiotic stresses and also would produce specialized natural compounds of valuable industrial/pharmaceutical potential.
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Acknowledgements
PM acknowledges funding support by CSIR, New Delhi and Science and Engineering Research Board (SERB), Department of Science and Technology (DST), Government of India for the project under “Scheme for Young Scientists” (SB/YS/LS-305/2013). MK, UG and AKN acknowledge CSIR, DST-INSPIRE and UGC, India respectively for Junior and senior research fellowships. This represents institutional communication number CSIR-IIIM/IPR/0068.
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Kundan, M., Gani, U., Nautiyal, A.K., Misra, P. (2019). Molecular Biology of Glandular Trichomes and Their Functions in Environmental Stresses. In: Singh, S., Upadhyay, S., Pandey, A., Kumar, S. (eds) Molecular Approaches in Plant Biology and Environmental Challenges. Energy, Environment, and Sustainability. Springer, Singapore. https://doi.org/10.1007/978-981-15-0690-1_17
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