Role of Elicitors in Inducing Resistance in Plants against Pathogen Infection: A Review

1Plants are challenged by a variety of biotic stresses like fungal, bacterial, or viral infections. This lead to a great loss to plant yield. There are various options available for the farmers to protect their crop from the disease. Some options include development of resistant cultivars, biological control, crop rotation, tillage, and chemical pesticides. Nearly all chemical pesticides or fungicides have a direct antibiotic principle. But their use at commercial level is uneconomical, application is cumbersome, and some are proved to be carcinogenic. Therefore, considerable efforts have been accomplished to devise environmental-friendly strategies for the check of plant diseases and thus to save mankind from health hazard.

2Plants can activate separate defense pathways depending on the type of pathogen encountered. Jasmonic acid (JA) and ethylene dependent responses seem to be initiated by necrotrophs, whereas salicylic acid (SA) dependent response is activated by biotrophic pathogens. The mechanisms responsible for this differential recognition and response may involve crosstalk among these three different signal transduction pathways: JA, ethylene, and SA.

3The better understanding of plant signalling pathways has led to the discovery of natural and synthetic compounds called elicitors that induce similar defense responses in plants as induced by the pathogen infection. Different types of elicitors have been characterized, including carbohydrate polymers, lipids, glycopeptides, and glycoproteins. In plants, a complex array of defense response is induced after detection of microorganism via recognition of elicitor molecules released during plant-pathogen interaction. Following elicitor perception, the activation of signal transduction pathways generally lead to the production of active oxygen species (AOS), phytoalexin biosynthesis, reinforcement of plant cell wall associated with phenyl propanoid compounds, deposition of callose, synthesis of defense enzymes, and the accumulation of pathogenesis-related (PR) proteins, some of which possess antimicrobial properties. AOS lead to hypersensitive response (HR) in plants which is a localized or rapid death of one or few cells at the infection site to delimit the pathogen growth. Following the activation of HR, uninfected distal parts of the plant may develop resistance to further infection, by a phenomenon known as systemic acquired resistance (SAR), which is effective against diverse pathogens, including viruses, bacteria, and fungi.

4Resistance in plant species is often divided into host- or nonhost-specific resistance. Host-specific resistance involves interactions between specific host and pathogen genotypes, which give a pathogen race-specific resistance. Nonhost resistance, shown by a whole plant species against a specific parasite or pathogen, is the most common form of resistance in plants towards the majority of potential pathogens. The biochemical changes that occur during infection are very similar in host and nonhost resistant plants. Disease spreads only in susceptible plants (compatible interactions) which are unable to recognize the pathogen or respond too slowly.

5The hypersensitive response is triggered by the plant when it recognizes a pathogen. The identification of a pathogen typically occurs when avirulence (Avr) gene products, secreted by pathogen, bind to or indirectly interact with the product of a plant resistance (R) gene (gene for gene model). When both the R gene and corresponding Avr genes are present, recognition occur, which lead to active resistance of the plant and avirulence of the pathogen. If either Avr gene in the pathogen or R gene in the host is absent or is mutated, no recognition will occur and outcome will be a compatible reaction and disease. As a result of putative binding of these two partners, a signal transduction cascade is activated and lead to the activation of a variety of plant defense responses. The defense responses are associated with restriction of pathogen growth. R gene products are highly polymorphic and many plants produce several different types of R gene products, enabling them to act as a receptor of Avr proteins produced by many different pathogens.

6Direct physiological contact between the host and infecting parasite is obviously necessary for the activation of HR. The HR was first described by Stakman to describe rapid host cell death in resistant wheat plants upon infection by rust fungi. Hypersensitivity is a rapidly developing defense reaction induced in incompatible host by a plant pathogen, which results in the death of a limited number of host cells and a concomitant localization of the pathogen. Some investigators have described the HR as resembling the process of apoptosis, the principal manifestation of programmed cell death in many animal cell types. This definition has now expanded to include defense gene expression in addition to cell death. The HR is analogous to the innate immune response found in animals. HR provides resistance to biotrophic pathogens that obtain their energy from living cells.

7The first report on the rapid generation of ROS during plant-pathogen interactions was by Doke in Phytophthora infestans—potato interaction. In studies involving bacteria and cell suspensions in the incompatible interaction, there are two phases of ROS production, termed as “oxidative burst”. Phase 1 is rapid, transient, and nonspecific, whereas phase 2 occurs later and yields a much higher concentration of ROS. This specific, biphasic response is proposed to be an important component of plant defense because in compatible interactions only the first phase is induced. The two distinct phases of the oxidative burst are seen only when an R gene and an Avr gene are both present, for example, with transgenic tomato plants differing only in the presence or absence of the R gene, Pto, and the bacterial pathogen, Pseudomonas syringae pv. tomato, with the avr gene, avrPto. This confirms that the second phase of the oxidative burst is associated with disease resistance. The earlier defense responses are the opening of specific ion channels across the plasma membranes, the rapid production of AOS, such as O2 − and H2O2, known as the oxidative burst or phosphorylation or dephosphorylation of specific proteins. These initial reactions are the prerequisite for initiation of the signalling network that will trigger the overall defense response.

8ROS are toxic intermediates that are generated through the sequential one electron reduction steps of molecular oxygen. Various enzyme systems have been proposed as the source of ROS in plants. An NADPH oxidase system similar to that of mammalian systems or a pH-dependent cell wall peroxidase may be two sources of oxidative burst. If NADPH oxidase activity is a ROS generating system, O2 − should be the initial product produced, however the O2 − generated is usually rapidly dismutated to H2O2 via SOD. Therefore, in most systems H2O2 appears to be the major ROS that accumulates. Under physiological conditions, the first reduction of O2 forms the superoxide anion (O2 −) and hydroperoxyl radical (HO2 •), the second step forms hydrogen peroxide (H2O2), and the third step produces hydroxyl radical (OH•). OH• and O2 − possess very short half lives. Uncharged H2O2 is more stable, whereas OH• cannot migrate in solution and instead reacts locally, notably with molecular targets by modifying their structure and activity. H2O2 as well as OH• can react with polyunsaturated lipids in membranes forming lipid peroxides, which can lead to biological membrane destruction.

9ROS species such as O2 −, OH•, and H2O2 are commonly produced under stress conditions and are strong oxidizing species that can rapidly attack all types of biomolecules and damage. For the protection from oxidative damage, plant cells contain both oxygen radical detoxifying enzymes such as catalase, peroxidase, and superoxide dismutase, and nonenzymatic antioxidants such as ascorbate peroxidase and glutathione-S-transferase. These enzymes play a crucial role in the protection of plant cells from oxidative damage at the sites of enhanced ROS generation. The cooperative function of these antioxidants plays an important role in scavenging ROS and maintaining the physiological redox status of organisms.

10Host plants can be protected against further pathogen attack if they have survived earlier infection by phytopathogenic viruses, bacteria, or fungi. It appears that the first infecting pathogen immunizes the plant against further infections by homologous pathogens, even though the plant may not carry gene determining cultivar-specific resistance. The readiness of the plant to repel subsequent pathogen attacks spread throughout the whole plant. This response is called systemic acquired resistance (SAR). The development of SAR is often associated with various cellular defense responses, such as synthesis of PR proteins, phytoalexins and accumulation of AOS, rapid alterations in cell wall, and enhanced activity of various defense related enzymes.

11The onset of SAR in noninfected plant organs is triggered by the phloem mobile signal which is released following pathogen infection. The signal travels throughout the plant and transduced in target tissues. Following signal transduction, resistance is maintained for several days and weeks and this is likely due to de novo gene expression. The biochemical changes that occur during SAR can be divided into two phases, that is, initiation and maintenance. Physiological changes during initiation phase may be transient and short lived, but during maintenance a quasisteady state should exist.

12Originally the term elicitor was used for molecules capable of inducing the production of phytoalexins, but it is now commonly used for compounds stimulating any type of plant defense. Eventually, the induction of defense responses may lead to enhanced resistance. This broader definition of elicitors includes both substances of pathogen origin (exogenous elicitors) and compounds released from plants by the action of the pathogen (endogenous elicitors). Elicitors are classified as physical or chemical, biotic or abiotic, and complex or defined depending on their origin and molecular structure (Table 1).

13Elicitors may be divided into two groups, “general elicitors” and “race specific elicitors”. While general elicitors are able to trigger defense both in host and nonhost plants, race specific elicitors induce defense responses leading to disease resistance only in specific host cultivars. A complementary pair of genes in a particular pathogen race and a host cultivar determines this cultivar specific (gene-for-gene) resistance. Thus, a race specific elicitor encoded by or produced by the action of an avirulence gene present in a particular race of a pathogen will elicit resistance only in a host plant variety carrying the corresponding resistance gene. The absence of either gene product will often result in disease. In contrast, general elicitors signal the presence of potential pathogens to both host and nonhost plants. The nonspecific nature of general elicitors is relative, however, and some of these are only recognized by a restricted number of plants.

14Recent studies have indicated remarkable similarities between the defense mechanisms triggered by general elicitors and the innate immunity of animals, and it is tempting to speculate that the recognition of general elicitors subsequently leads to plant innate immunity. Elicitors act as signal compounds at low concentrations, providing information for the plant to trigger defense, distinguishing elicitors from toxins, which may act only at higher concentrations and/or affect the plant detrimentally without active plant metabolism. Elicitor signal transduction mechanism which activates plant primary immune response is shown in Figure 1.

15Alternatives to fungicides in plant protection have arisen with the discovery of disease resistance inducers of biotic and abiotic origins that induce a localized or systemic resistance in susceptible plants, which become resistant to subsequent infections. Depending on their efficacy, these compounds can be used in fields either alone or in combination with fungicides.

16Many compounds have been commercially released in some countries as a plant health promoter of annual crops under the name Bion or Actigard. The SA-dependent defense pathway can be activated by treatment of plants with chemical inducers such as benzo (1,2,3)-thiadiazole-7-carbothioic acid-S-methyl ester (acibenzolar-S-methyl, ASM or BTH, Bion) developed as a potent SAR activators which do not only possess antimicrobial properties, but instead increase the crop resistance to diseases by activating SAR signal transduction pathways in several plant species. BTH is a chemical analogue of SA and has been used successfully to induce resistance to a wide range of diseases on field crops. The nonprotein amino acid β-aminobutyric acid (BABA) protects numerous plants against various pathogens. Several products have also been used as inducers of resistance in plants against pathogens, including chitosan, salicylic acid analogues, living or processed fungal products, and seaweed extracts. Certain synthetic compounds with no direct antimicrobial effect such as 2,6-dichloroisonicotinic acid (INA) and potassium salts has been reported to induce SAR in plants. Table 2 shows the list of various elicitors used and their effects on different plant species.

17The use of elicitors in crop protection and pest management is still in the very early stages of use as a new control method, and thus the current experiences come from experimental trials, and not yet from large scale agricultural use. At least the following advantages of using elicitor treatments have been reported or can be expected:reduced damage from insects, fungi, pests, and herbivores,reduced environmental hazards as elicitors affect directly the crop plant, and their acute toxicity to other organisms is lower than that of pesticides,as protective agrochemicals, elicitors can be applied with the current spraying technology,elicitor treatments could be an alternative to genetically modified (GM) plants for better attraction of natural enemies of pest organisms on cultivated plants,elicitor-treated plants bear lower ecological risks than GM plants.

18reduced damage from insects, fungi, pests, and herbivores,

19reduced environmental hazards as elicitors affect directly the crop plant, and their acute toxicity to other organisms is lower than that of pesticides,

20as protective agrochemicals, elicitors can be applied with the current spraying technology,

21elicitor treatments could be an alternative to genetically modified (GM) plants for better attraction of natural enemies of pest organisms on cultivated plants,

22elicitor-treated plants bear lower ecological risks than GM plants.