| Received | : | Dec 26, 2018 |
| Accepted | : | Feb 25, 2018 |
| Published Online | : | Mar 07, 2018 |
| Journal | : | Journal of Plant Biology and Crop Research |
| Publisher | : | MedDocs Publishers LLC |
| Online edition | : | http://meddocsonline.org |
Cite this article: Cna’ani A , Seifan M, Tzin V. Indole is an essential molecule for plant interactions with herbivores and pollinators. J Plant Biol Crop Res. 2018; 1(1): 1003.
Indole is a well-characterized molecule that is used as a building block for a multitude of natural compounds. It can be utilized directly as a free indole or it can serve as a substrate for indole-derived metabolites. Besides serving as a substrate for the essential amino acid tryptophan, it is also involved in a variety of plant functions. One of the most important processes in which involving indole is the chemical interaction between plants and insects. These insects are classified into two groups: i) herbivores, which feed on plant tissue (e.g. caterpillars) or consume nutrients from the phloem (e.g. aphids), and ii) pollinators, which feed on plant nectar and pollen and serve as vectors fortransferring male gametes between flowers. The nature of indole and indole-derived metabolite usage may differ based on the type of interactions. While indole is a volatile compound emitted to the plant’s surrounding, functioning as a remotesignal, indole-derived metabolites are mainly non-volatile and mostly function asdeterrents that harm herbivores by “direct contact”. In this review, we discuss the major role of indole in determining plant fitness by attracting pollinators and repelling herbivores.
Keywords: Defense; Emission; Floral scent; Insect; Tryptophan; Metabolite; Volatile
Indole is an aromatic heterocyclic organic compound, consisting of a six-membered benzene ring fused to a five-membered nitrogen-containing pyrrole ring [1]. In plants, indole is produced via the shikimate pathway, resulting in tryptophan (Trp) biosynthesis (Figure 1). The biosynthesis of Trp is catalyzed by the two enzymatic steps: Trp synthase-alpha subunit, which converts indole-3-glycerol into indole, and channels it directly to the Trp synthase-beta subunit for further conversion into Trp (existing as a α2β2 tetramer complex; [2]). During Trp biosynthesis, indole-3-glycerol phosphate is produced and directed into different pathways leading to the biosynthesis of both volatile and non-volatile compounds (Figure 2). The indole moleculeis embedded in many biological systems including the neurotransmitter serotonin, the hormone melatonin, or scent compounds in human’s sweat and flowers [1,3]. In plants, this molecule plays a role in many functions, ranging from Trp production to the coloring of yellow petals (terpenoidindole alkaloid), and the biosynthesis of defense and scent metabolites [4-7]. Indole is also known as a substrate for the phytohormone auxin (indole-3-acetic acid), which is fundamental in regulating many aspects of plant growth and development [8,9]. Auxin can be synthesized through the Trp-dependent auxin biosynthetic pathway or the Trp-independent pathway as recently reported [5,10]. In monocots that produce non-volatile defense metabolites such as benzoxazinoids, free indole can be produced by the indole-3-glycerol phosphate lyase enzyme, named Bx1 [11-13]. In addition, indole is probably catalyzed by the enzyme indole-synthase (INS) in Arabdiopsis thaliana and indole-3- glycerol phosphate lyase (IGL) in maize (Zea mays; [6,14,15]). In relation to plant-insect chemical interactions, indole serves as a precursor for deterrence metabolites that are involved in plant defense against herbivores (e.g. benzoxazinoids, gramine, glucosinolates,and serotonin); in addition indole is emitted as a scent (to attract pollinators or predators) or as an aerial priming agent to non-attacked plant tissues. Because indole is involved in a wide range of plant functions, it is considered to be a major factor in determining plant fitness.
Figure 1: An overview ofindole biosynthesis (grey box), several major classes of specialized metabolites (orange box) and phytohormones biosynthesis (blue box).
Figure 2: Schematic representation of indole and Trp biosynthesis. In blue are the enzymatic reactions.
Floral signals are an important component of plant-pollinator interactions, and are composed of two major traits: visual (e.g. color and shape) and olfactory scents volatile compounds; [16]. Although visual cues are important in attracting pollinators, they often elicit fewer specific responses than odors [17-19]. One major scent compound that plays a role in these interactions is indole. It is the most prolific nitrogen-containing volatile found in the petals of flowering plants and it is biosynthesized and emitted from the flowers of over 30 distinct plant families [20]. In some plant species, indole accumulation and/or emission is restricted to floral tissues, which highlights its role in scent formation [21]. In several classes of insects, such as the grey-backed mining bee ( Andrena vaga ), hummingbird moth ( Hyles lineata ) and the housefly ( Musca domestica ), indole was reported to elicit substantial antennal responses, indicating that these species can detect and react to this signal when foraging and subsequently during pollination [22,23].
Indole is occasionally a constituent of floral scent bouquets in nocturnal, moth-pollinated plants [24,25]. For example, in a reproduction isolation experiment, Bischoff et al. (2014) showed that indole contributed to the promotion of hawkmoth visits to Ipomopsis flowers [26]. The author’s showed that, overall, hawkmoths preferred to visit I. tenuituba , which is light-pink and naturally emitting indole, regardless of the artificial addition of the metabolite. In the case of I. aggregate, which has red petals and does not emit indole, the hawkmoth visitation rate was increased when indole was added. Indole is also involved in the attraction of insects to the flowers of “sapromyiophilous” plants, which mimic carrion and dung odors to attract flies for pollination services. These plants typically do not produce nectar and rely heavily on sensory cues to ensure pollination [27]. Flowers of such plants (e.g. Periploca laevigata, Stemona species and Satyrium pumilum ) usually emit a blend of sweet and putrid volatiles that are associated with both ovipositional/mating sites and potential food sources [23,28,29]. Indole, being present in animal waste (Cosse and Baker, 1996) and carrions, is regarded as a signal leading the insects to the aforementioned, sites as well as to the flowers of dung and carrion-mimicking plants [22,25].
In response to mechanical and herbivore damage, plants release a specific blend of volatile compounds. These volatiles can affect herbivores in different manners by: i) attracting natural enemies that feed on herbivores (i.e., predators and parasitic wasps) to locate their prey or host [31], ii) signalling to other herbivores that the plant has initiated the production of deterrent compounds; iii) signalling that herbivores are already present on the plant and its nutritional value is reduced, therefore helping to reduce additional herbivore damage [32], and iv) function as anaerial priming agent to non-attacked neighboring plants, which will allow them to induce their defense mechanisms in preparation for future attacks [33]. An example of aerial priming was recently reported by Erb et al (2015). This research revealed that herbivore-infested maize leaves emit indole to enhance the induction of defensive mechanisms in systemic leaves and neighboring maize plants in a species-specific manner. Indole emission increased the biosynthesis of mono and homo-terpenes in the systemic leaves of attacked plants as well as the production of the stress phytohormones, such as jasmonic acid conjugate and abscisic acid in neighboring plants [33].
In plants, Trp and its substrate indole, serve as precursors for various classes of toxic, deterrent metabolites that play a defensive role against insects and pathogen by interfering with their life cycle [2,34,35], as depicted in Figure 3. These classes of metabolites differ between monocots and dicots and among the plant species in each group. In monocots, for example, the two millet species, foxtail millet ( Setaria italica ) and Japanese barnyard millet ( Echinochloa esculenta ), as well as rice plants ( Oryza sativa ) accumulate serotonin in response to pathogen or herbivore infestations [37,38]. For example, rice leaves were fed on by rice striped stem borer ( Chilo suppressalis ) larvae for either 24 h or 48 h which induced of four Trp-derived metabolites including serotonin, tryptamine, feruloyl tryptamine (FerTry) and p-coumaroylserotonin [38]. High concentrations of tryptamine in Catharanthus roseus plants have also been shown to express anti-oviposition activity toward whiteflies ( Bemisia tabaci ; [39]) and anti-feeding activities in tobacco and poplar toward Malacosoma disstria and Manduca sexta caterpillars [40]. Other monocots such as maize, wheat ( Triticum genus ), rye ( Secale cereale ), and wild barley ( Hordeum genus ) produce benzoxazinoids [11,41-43] while the cultivated barley species (Hordeum vulgare) produces gramine, an indolic defense compound, against aphids and pathogens [44,45]. Benzoxazinoids were shown to cause negative effects against awide range of pests, including insects (aphids andcaterpillars), bacteria, fungi and nematodes [13,46-48,50-52]. The mode of action of these specialized metabolites is to deter insects by antibiosis properties caused by inhibition the digestive proteases responsible for detoxification and pest salivation and therefore, to affect the insect’s fitness [53]. For example, feeding experiments of cereal aphids on an artificial diet containing benzoxazinoid conjugates showed increased aphid mortality which supports a toxic function for these metabolites [48,52].
Figure 3: A summary of the major functions of indole and indole-derived metabolites. In blue are the functions of indole and indole-derived volatile metabolites, in red are the classes of non-volatile deterrent metabolites; in green are the indication of the roles of indole and Trp in plant growth and development.
Dicot plants that belong to the Brassicaceae family, produce one or more indole glucosinolates which are among the most widely distributed glucosinolates in nature [54]. Glucosinolatesremain compartmentalized and come in contact with the pest only upon tissue damage, followed by myrosinases (β-thioglucoside glucohydrolase) activity and release of defensive hydrolysis products including isothiocyantes, nitriles, and epithionitriles which are toxic compounds [55,56]. The glucosinolates levels increase and their composition can change in response to herbivory and pathogen attack in several Brassicaceae species [57,58]. For example, a defensive role for indole glucosinolates was observed in the case of the A. thaliana atr1D mutant plant, which over produces indole glucosinolates. This in turn confers resistance to Brassicaceae-generalist herbivore, Myzus persicae aphids. Conversely, the Arabidopsis cyp79B2/ cyp79B3 double mutant, which possess low levels of indole glucosinolates, responded to M. persicae more rapidly [59,60]. Interestingly, the cyp79B2/cyp79B3 double mutant was tested for Brassicaceae-specialist herbivores, Pieris rapae , oviposition and received fewer P. repae eggs than the wild-type [61]. It was suggested that the role of indole glucosinolates and their breakdown products in plant-herbivore interactions, remains complex due to their differential influence on generalist and specialist herbivores [62].
Indole is an essential metabolite that often determines the outcome of plant and insect interaction. On the one hand, indole is involved in positive plant-insect interactions by serving as part of the volatile signals emitted by plants to attract their pollinators. On the other hand, indole is involved in negative plant-insect interaction by serving as a substrate for several classes of specialized metabolites that are function in repelling herbivores. Therefore, we suggest that further study the biosynthesis and catabolism of indole under insect infestations should be further studied. Additionally, it would be prudent to explore the indole flux during visits of co-occurring insects from different guilds at different plant developmental stages.
This research was funded by the Koshland Foundation for Support of Interdisciplinary Research in Combating Desertification to AC, MS, and VT, and by the Jacob Blaustein Center for Scientific Cooperation and the Bona Terra Foundation Fund for Promoting Sustainable Agriculture in Drylands to AC. This is publication 958 of the Mitrani Department of Desert Ecology .
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