Encyclopedia
Please note this is a comparison between Version 1 by Pratap Adinath Divekar and Version 3 by Bruce Ren.
Plants have evolved several adaptive strategies through physiological changes in response to herbivore attacks. Plant secondary metabolites (PSMs) are synthesized to provide defensive functions and regulate defense signaling pathways to safeguard plants against herbivores. Herbivore injury initiates complex reactions which ultimately lead to synthesis and accumulation of PSMs. The biosynthesis of these metabolites is regulated by the interplay of signaling molecules comprising phytohormones. Plant volatile metabolites are released upon herbivore attack and are capable of directly inducing or priming hormonal defense signaling pathways. Secondary metabolites enable plants to quickly detect herbivore attacks and respond in a timely way in a rapidly changing scenario of pest and environment.Several studies have suggested that the potential for adaptation and/or resistance by insect herbivores to secondary metabolites is limited. These metabolites cause direct toxicity to insect pests, stimulate antixenosis mechanisms in plants to insect herbivores, and, by recruiting herbivore natural enemies, indirectly protect the plants. Herbivores adapt to secondary metabolites by the up/down regulation of sensory genes, and sequestration or detoxification of toxic metabolites. PSMs modulate multi-trophic interactions involving host plants, herbivores, natural enemies and pollinators. Although the role of secondary metabolites in plant-pollinator interplay has been little explored, several reports suggest that both plants and pollinators are mutually benefited. Molecular insights into the regulatory proteins and genes involved in the biosynthesis of secondary metabolites will pave the way for the metabolic engineering of biosynthetic pathway intermediates for improving plant tolerance to herbivores. This review throws light on the role of PSMs in modulating multi-trophic interactions, contributing to the knowledge of plant-herbivore interactions to enable their management in an eco-friendly and sustainable manner.
- secondary metabolites
- insect herbivores
- defense regulation
- phytohormones
- insect adaptations
- natural enemy
- pollinators
- sustainable protection
1. Introduction
All living organisms have to face environmental and biotic challenges during their lifetime. According to Darwin’s evolutionary theory, “survival of the fittest” or “natural selection” enables the fittest organism to compete, survive and reproduce. The fittest organisms have the diverse genetic potential to defend themselves, or resist or avoid stress consequences which hamper their physiological functions, permitting them to grow, develop and survive. This adaptive evolution ensures the ecological specialization of a species for a specific niche [1] and ultimately results in speciation [2]. Being sessile organisms, plants are continuously exposed to various biotic and abiotic stresses, such as herbivore or pathogen attack, drought, salinity, UV-irradiation, extreme temperatures, and nutritional imbalances in natural environments [3][4][5][3,4,5]. Phytophagous herbivores are said to be responsible for destroying one-fifth of the world’s total crop production annually [6].
Plants have evolved several types of secondary metabolites as a defensive shield to protect themselves from phytophagous herbivores [7]. Nearly 200,000 PSMs have been isolated and characterized which is a small number relative to the 391,000 described plant species [8]. Upon exposure to herbivores, secondary metabolites accumulate at an increased level and act as signaling molecules to upregulate the defense response genes. PSMs ensure the competitiveness and survival of plants under stress conditions. Recently, the signaling role of these metabolites in defending plants has received more attention [5]. PSMs include alkaloids, terpenes, amines, glucosinolates, cyanogenic glucosides, quinones, phenolics, peptides and polyacetylenes [9]. PSMs have no role in the basic life processes of plants, but they play a vital role in adaptation and defense against herbivores. PSMs are synthesized through several metabolites and intermediates that are engaged in plant defense. These pathways start from primary metabolic pathways, which are the ultimate precursors of PSMs. Primary metabolites are actively engaged in the regulation of the normal growth and development of plants. However, secondary metabolites are only involved in plant defense against herbivores. Although the role of these plant metabolites is different, they are interlinked, as primary metabolites act as precursors for the synthesis of secondary metabolites [10]. Primary and secondary metabolites are different in their structure, function and distribution in different tissues of plants.
Plants have devised a sophisticated recognition and signaling system which ensures early recognition of herbivore attacks and triggers a powerful defense response [11]. Recent genetic and chemical investigations have demonstrated the multifunctional nature of PSMs, which act as potent regulators of plant growth, defense and primary metabolism. Induced plant defenses are driven by the phytohormones jasmonic acid (JA) and salicylic acid (SA), and the associated pathways interact in a complicated fashion at the transcript and protein level. Adverse effects on the survival of chewing insects (Heliothis virescens) and sucking insects (Myzus persicae) were reported after JA and SA application [12]. Secondary metabolites may also have hormone-like properties by binding to specific receptor proteins [13]. There is a synergistic effect of PSMs operating together to tackle herbivore damage [14]. A combination of these secondary metabolites is likely to prevent or delay the development of resistance by insect herbivores [15]. However, insects have been found to show different adaptive responses, including detoxification, excretion or sequestration of plant secondary metabolites [10]. Although the role of secondary metabolites in plant defense is well established, in addition some metabolites are used to attract insect pollinators and parasitoids [16][17][16,17]. Secondary metabolites are seen as not only a cost-effective and ecologically friendly means to sustain agriculture, but they also compete with agrochemicals in terms of plant growth and protection [18].
2. Secondary Metabolite Functional Role in the Regulation of Plant Defense and Early Detection of Herbivore Attack
Plants generally increase their resistance and decrease their growth in response to herbivore attacks. A phytohormonal signaling network enables this prioritization. The rice transcription factor WRKY70, which is activated by herbivore-induced mitogen-activated protein kinase signaling, plays a critical role in prioritizing defense over growth by positively regulating jasmonic acid (JA) and negatively regulating gibberellin (GA) levels in response to attack by the chewing herbivore Chilo suppressalis. Proteinase inhibitors are activated and resistance to C. suppressalis is achieved through WRKY70-dependent JA biosynthesis. WRKY70 induction, on the other hand, makes rice plants more susceptible to the rice brown planthopper, Nilaparvata lugens. Studies with GA-deficient rice lines demonstrated that WRKY70-dependent GA signaling is responsible for susceptibility to N. lugens. Thus, prioritizing defense over growth results in a resistance trade-off, which has significant consequences for plant defense regulation [19][39]. Plants regulate defense activation to save metabolic energy and avoid self-damage. Feedback regulation, which includes both positive and negative feedback loops embedded into early defense signals, is often used to titrate defense investment [19][39] and hormonal networks [20][40]. These feedback loops have the drawback of not providing direct information on the final level of defensive activation (i.e., the production of defense metabolites per se). Herbivores can interfere with the synthesis of defense chemicals at many levels, including the last steps of biosynthesis [21][41], so incorporating them directly into regulatory feedback loops should help plants effectively monitor and regulate defense. Secondary metabolites, as defense activation readouts, may also assist plants in maximizing synergy between several defenses and compensating for failures in the defense pathway.
Because many secondary metabolites are compartmentalized and/or retained in inactive forms, decompartmentalization and/or activation may aid plants in detecting herbivore tissue damage [22][31]. Plants that have been damaged perceive a range of endogenous chemicals as danger signals, which are referred to as damage-associated molecular patterns (DAMPs). Secondary metabolites would be employed as DAMPs. Secondary metabolites that are also DAMPs include green-leaf volatiles [23][42].
Plant defenses can also be regulated by volatile compounds, such as terpenoids, green-leaf volatiles, and aromatic chemicals, in addition to glucosinolates and benzoxazinoids [24][43]. Most of these volatiles are generated in response to herbivore attacks, and they can directly induce or prime hormonal defense signaling pathways and resistance. In maize, mutants that cannot synthesize volatile indole are unable to condition their systemic tissues to release terpenes quickly in response to herbivore attacks. Adding indole to the headspace of maize plants restores this priming phenotype [25][44]. Rice (Oryza sativa) plants also respond to indole through priming of early defense signaling elements, such as the map kinase OsMPK3. Transgenic plants lacking the OsMPK3 gene are no longer responsive to indole, implying that indole functions by activating early defensive signaling [26][45]. Five types of secondary metabolites (i.e., glucosinolates, benzoxazinoids, terpenes, aromatics, and green-leaf volatiles) have now been demonstrated to serve as potential plant defense regulators. It is exciting to think that there are potentially several other secondary metabolites with similar regulatory functions.
Plants have evolved efficient defense systems to protect themselves from herbivores. They can recognize and respond to invaders by activating defense-related signaling pathways, such as mitogen-activated protein kinase (MAPK) and hormonal signaling, which results in the expression of several defense-related genes and phytochemicals [27][46]. Induced resistance to herbivores is mediated primarily through jasmonic acid (JA), salicylic acid (SA), and ethylene (ET)-mediated signaling [28][47]. Herbivore-plant interaction is a two-way process, i.e., plants activate a specific defense response after insect injury to protect themselves. Plants must be able to distinguish between physical injury and insect feeding to activate an insect-specific defense. The oral secretion or oviposition fluid of insects has been found to contain specific active substances known as elicitors. These are recognized by plants and are important in the formation of defense-related downstream signaling cascades [29][48]. Oral secretions have also been observed to suppress plant defense mechanisms [30][49]. Elicitors are divided into six categories based on their chemical structure and composition: enzymes, fatty acid amino acid conjugates (FACs), fatty acids, peptides, esters, and benzyl cyanide [31][50]. Enzymes, fatty acids, FACs, and peptides are secreted in oral secretions, while esters and benzyl cyanide are released in oviposition fluids during egg-laying [29][32][33][48,51,52]. Different types of elicitors may have different effects and modes of action.
An enzyme elicitor, β-glucosidase, from Pieris brassicae regurgitates was the first insect elicitor to be recognized and reported [34][53]. The plant defense is activated and a series of volatiles are released by β-glucosidase in cabbage, lima beans, and corn plants [35][36][26,54]. These released volatiles attract the parasitoid Cotesia glomerata. Thus, the β-glucosidase in P. brassicae induces indirect plant defense [34][53]. Sucking insects also express this type of elicitor, in addition to chewing herbivores. β-glucosidase is predominantly present in Nilaparvata lugens, which raises the concentrations of jasmonic acid (JA), hydrogen peroxide (H2O2), and ethylene [37][55]. This leads to multiple downstream signaling cascades and the release of volatiles, such as dodecenal and tetradecane, which in turn attracts the parasite Anagrus nilaparvatae [37][55]. β-glucosidases are compartmentalized away from the inactive, glucosidically bound volatiles, i.e., glucosinolates. A mixture of these two elements leads to β-glucosidase activity, releasing volatiles, such as isothiocyanate, thiocyanate, and nitriles, as a result of insect feeding [30][38][49,56].
Plants recognize certain elicitors from insect oral secretions (OS) which enter through wounds during insect feeding in plant tissue and trigger a chain of interlinked signaling pathways involved in the synthesis of defensive metabolites. Mitogen-activated protein kinases (MAPKs) are ubiquitously present in all eukaryotic organisms and are actively engaged in many cellular processes of normal growth and stress responses. Insect OS activates the two types of MAPKs, salicylic acid-induced protein kinase (SIPK) and wound-induced protein kinase (WIPK) in plants. MAPKs are important in active regulation of the insect herbivore-induced dynamics of phytohormones, jasmonic acid, ethylene, and salicylic acid. MAPKs are also required for transcriptional activation of herbivore defense-related genes and accumulation of defensive metabolites [11]. Induced defense is maintained by signaling processes that regulate the downstream responses to insect-herbivore specific cues, including transcriptional activation of genes that encode enzymes involved in the synthesis of defense metabolites [39][57]. The activation of MAPKs, which modulate phytohormone levels and restructure the transcriptome and proteome in preparing for plant defense, is the most crucial process in signaling after insect attack.
Herbivore-associated molecular patterns (HAMPs) include all herbivore-induced signaling metabolites recognized by the host plants and, thus, elicit defense responses [40][58]. Insect OS-containing elicitors are the most explored HAMPs in understanding herbivore-plant interactions [28][47]. These elicitors activate insect-specific responses when they enter into plant tissue during insect feeding. The first elicitor identified in the armyworm Spodoptera exigua oral secretions was N-(17-hydroxy linolenoyl)-l-glutamine (volicitin). Volicitin can induce volatiles in maize to attract parasitoids of S. exigua [41][59]. Fatty acid-amino acid conjugates (FACs), structurally similar to volicitin, were reported from OS Manduca sexta larvae [42][60]. Application of FACs to wounds, mimicking caterpillar feeding, activates insect-specific responses in plants, including the enhanced concentration of jasmonic acid (JA), ethylene (ET) and salicylic acid (SA) and reshaping of the transcriptome [43][61]. FACs are elicitors that activate MAPK signaling [39][57]. Focused research is needed to understand how elicitors activate defense signaling (e.g., MAPKs) and downregulate defense reactions in plants. In view of the complexity of insect-herbivore interactions, there is potential for the existence of several insect-derived elicitors, which may trigger insect-specific defense response in a particular plant species.
