Open access peer-reviewed chapter

Plant Metabolites in Plant Defense Against Pathogens

Written By

Xóchitl S. Ramírez-Gómez, Sandra N. Jiménez-García, Vicente Beltrán Campos and Ma. Lourdes García Campos

Submitted: April 1st, 2019 Reviewed: June 11th, 2019 Published: July 15th, 2019

DOI: 10.5772/intechopen.87958

Chapter metrics overview

1,356 Chapter Downloads

View Full Metrics

Abstract

Medicinal plants are widely used worldwide to treat various diseases. Its widespread use is due in part to the cultural acceptance of traditional medicine in different regions of the world, as well as its effectiveness in treating various diseases. Many of its active substances or secondary metabolites are formed to a response of various situations that generate stress in their habitat, such as sudden changes in environmental temperature, humidity, rain, drought, and infections by phytopathogens (fungi, bacteria, viruses, nematodes, protozoa). The production of these secondary metabolites is a mechanism of defense of plants. In this context, the objective of this chapter is to study the secondary metabolites of medicinal plants that could have a promising application in the control of different phytopathogens in crops of agricultural and economic interest.

Keywords

  • medicinal plants
  • phytopathogens
  • secondary metabolites
  • pesticides
  • biotic and abiotic elicitors

1. Introduction

Phytopathogens generally attack plants during their growth, causing alterations in their cellular metabolism and/or interfering with the absorption of nutrients [1]. The crops of cereals, vegetables, and fruits are affected by these organisms during harvest and postharvest [2]. However, one of the main control measures to eradicate phytopathogens is the use of pesticides. Although they are effective, easy to access, and easy to use, they have several disadvantages, generate resistance, and are considered toxic substances, not only for bacteria, fungi, viruses, protozoa, and nematodes but also for the humans, animals, and the environment [3, 4]. In this context, the pesticides can induce acute and chronic toxicity, to persist in the environment and pollute soil and water. So, they are easily incorporated into the food chain, bioaccumulation, and biomagnification [5]. Regarding their toxicity mechanisms, it has been described that they can act as endocrine disruptors and as reactive species that generate oxidative stress in the cell [6, 7, 8, 9].

On the other hand, the study of medicinal plants as possible natural sources of obtaining active compound (secondary metabolites) against phytopathogens has gained increasing interest in recent years, due to several aspects, mainly that they are obtained from a natural source through the production or synthesis of secondary metabolites considered as nontoxic such as phenols, flavonoids, terpenes, alkaloids, etc. [10, 11, 12, 13]. Another advantage is that phytopathogens still do not develop resistance to the antifungal, antimicrobial, and nematicide effect of the phytochemical compounds produced by some medicinal plants. When carrying out an exhaustive search in the literature, it was found that the potential use of the secondary metabolites obtained from medicinal plant extracts is fungicide [14, 15, 16]. Most of the research in this area focuses on evaluating the effects of these active compounds on fungi such as Fusarium, maybe because it is one of the main phytopathogens that cause economic losses mainly in cereal crops and health problems by their aflatoxins [17, 18]. This chapter shows an overview of the recent research on this topic, emphasizing the effect of biotic and abiotic elicitors on the secondary metabolite production, as well as a brief description of the scientific name of the plant, metabolites with antifungal and antibacterial effect, and their limitations and perspectives of its use in the biological control of phytopathogens.

Advertisement

2. Pesticides in the control of phytopathogens

In the market, there are a variety of pesticides that are used alone or in combination to eradicate, control, or prevent pests [4]. Pesticides can be classified according to the chemical group to which they belong, to their selectivity toward a certain phytopathogen, its mechanism of action, and its use or application. However, the most widely used for their effectiveness and a broad spectrum of activity against various pests and diseases in plants are insecticides, herbicides, and fungicides [4, 19].

Pesticides used in agriculture mainly contaminate the soil by direct application and water by leaching, and it is very easy for them to be present either in trace quantities or high in food and to enter the food chain, which facilitates its accumulation and biomagnification [5, 20]. In general pesticides are considered dangerous substances for living beings since they can produce acute or chronic toxicity; however the magnitude of the poisoning depends on several aspects to be considered such as the physicochemical characteristics of the pesticide, the concentration, the exposure time, the route of entry to organisms, their toxicodynamics and toxicokinetics (absorption, distribution, half-life, metabolism, and elimination), as well as the use of mixtures of different pesticides, the components of their formulation, and the general state of health of the individual [21, 22]. All these aspects influence that pesticides represent a risk or danger for those who use them in the fields of cultivation, as well as for those who consume foods that contain substances in trace quantities in prolonged consumption.

Regarding its toxicity, it has been described that pesticides act as endocrine disruptors and generators of free radicals and enzymatic inhibitors [8, 9]. Unfortunately, the cellular targets to which most of these pesticides are directed coincide with cellular targets that are also present in man, such as the case of the mechanisms of action of organophosphorus insecticides, which inhibit the activity of acetylcholinesterase enzyme present in different insects; unfortunately man and other mammals also have acetylcholinesterase, so their toxicity is not selective toward the pests that they wish to control, but they also affect man, and depending on the magnitude of the poisoning, they can cause death [19, 20, 21, 22]. However, until today an ideal pesticide does not exist, and the correct use of herbicides, fungicides, insecticides, etc. has many benefits to control plagues and increase the yield of the crops [19].

Advertisement

3. Secondary metabolites of medicinal plants as biological control of phytopathogens

There are several methods of biological control against phytopathogens. The use of extracts of medicinal plants to eradicate diseases in crops caused mainly by viruses, bacteria, and fungi is one of them [23]. The above makes sense if we analyze the fact that plants have mechanisms to protect themselves from both biotic and abiotic stress agents. That is, if the phytopathogens (biotic agents) are attacking the plants, why not think what the plant does to defend itself?

In this context, it is interesting to analyze the secondary metabolism of plants know which phytochemical substances are produced and what biological activity they present.

3.1 The bioactive potential of secondary metabolites derived from the medicinal plant

Plants are formed by a primary metabolism that is responsible for the physiological processes and development of the plant, such as lipids, carbohydrates, and proteins [23]. The secondary metabolism is not essential in the basic processes of plants. However, these bioactive compounds play an important role in the defense of plants, and these secondary metabolites can be classified as phenolic compounds, carotenoids, terpenes, alkaloids, and sulfur compounds, among others, as shown in Table 1 [24].

Table 1.

Types of plant secondary metabolites.

Phenolic compounds are aromatic substances formed during the passage of the shikimic acid pathway or mainly the mevalonic pathway. These can be divided into insoluble compounds such as condensed tannins, lignins, and hydroxamic acids bound to the cell walls, and soluble compounds are phenolic acids, flavonoids, and kinases [25]. Carotenoids are lipophilic molecules and are found in plants giving orange tones. The importance of these compounds is the intervention they have in photosynthesis, and they also protect the photosynthetic apparatus from excess energy [25]. The carotenoid contents in plants are affected by various factors, such as plant development, stress conditions, postharvest conditions, or cooking treatments, but the interest of these compounds has been increasing due to their potential antioxidant activity [26]. Terpenes are lipid-soluble compounds that include one- or more five-carbon isoprene units, which are synthesized by all organisms through two pathways, mevalonate and deoxy-D-xylulose [27]. Terpenoids are classified according to the number of isoprene units they contain; terpenes and terpenoids are basic constituents of many types of plant essential oils [28]. Alkaloids are bioactive compounds that generally contain nitrogen derived from an amino acid of great importance because it has physiological and medicinal properties, for example, caffeine, nicotine, morphine, atropine, and quinine [29].

Now well, all these compounds mentioned above help the plants to develop complex defense systems against different types of stress for the survival or the systematic forces in their metabolism for resistance against pests and diseases. Stress provoked in the plant involves several signaling response pathways for pathogens and insects, and some of these response pathways are induced by the microorganisms themselves. Also, the plants have specific recognition and signaling systems allowing them to detect the pathogens and initiate an effective defense response [30, 31]. The defence system broadest have the plants against pathogens are the phenolic compounds (phenylpropanoids and flavonoids). These substances have different mechanisms of action they can dissociate the ions of the phenolic hydroxyl and forming phenolates, ionic and hydrogen bonds with peptides and proteins causing a high astringency and protein denaturation. In the other hand, they interfere with the pathogen's cell signalling compounds and affect their physiological activities through enzymatic inhibition, DNA alkylation and altering their reproductive system [31]. The compounds with allelopathic effects affect positively or negatively on the ecosystem’s structure to remove or eliminate microorganisms from the plants. Some phenolic compounds are allelochemicals that have been shown to have an activity as antibiotics, antifungals, and antipredator [31]. Phenolic acids, such as benzoic, hydroxybenzoic, vanillic, and caffeic, have antimicrobial and antifungal properties produced by the inhibition of enzymes. Caffeic, chlorogenic, sinapic, ferulic, and p-coumaric acids have antioxidant activity by the inhibition of oxidation of lipids and the elimination of reactive oxygen species. These effects are important to the plant defense [32].

3.2 Improving production of plant secondary metabolites through biotic and abiotic stresses

Classification of secondary metabolites related to the defense of plants is commonly used in the form of synthesis and accumulation of phytochemicals with interaction effect of the pathogenic plant against plant insect, virus, fungi, and antibacterial compounds. For example, phytoalexins are produced very quickly after infection of a pathogen producing toxicity to an ambiguous environment of fungi or bacteria [33, 34].

Phenylpropanoids and flavonoids have hydroxyl groups that contain phenolic compounds, which dissociate into phenolate ions, and the phenolic hydroxyl groups form ionic bonds and hydrogen bonds with peptides and protons, producing a high astringency and denaturation that thus show an antifungal effect acting together with cellular signaling compounds and physiological activities or acting on the parts of the pathogen, reproductive system, enzymatic inhibition, etc. [35]. The properties of the proteins change with any change in protein conformation, for example, by changing the three-dimensional structure forming covalent bonds with SH, OH or free amino groups there is inactivation or protein function loss. When polyphenols of the plants bind to some proteins of phytopathogens are less toxic for them but can protect the plant of abiotic elicitors [36]. On the other hand, phytoalexins are induced against the attack of microbes and insects activated by β-glucosidase by the release of biocidal aglycones [37]. In the same way act the benzoxazinoids (BX), these phytochemical compounds are produced and released by tissue damage and hydrolysis by β-glucosidase and act as insect repellents too [38].

At present, several biotechnological strategies have been used to increase the productivity of secondary metabolites, using different inducers of secondary metabolites such as at the cellular, organic, and plant levels, as well as the most effective methods to improve the synthesis of these secondary metabolites in endemic and medicinal plants [39]. These secondary metabolites accumulate in plants when they are prone to various stress types, inducers, or signal molecules. Thus, there are different modulating factors of secondary metabolites, as well as microbial, physical, or chemical effects such as abiotic or biotic elicitors, inducing the biosynthesis of specific compound that plays an important role in the adaptations of plants to stress conditions, and these phenomena cause a greater synthesis and accumulation of secondary metabolites [40]. In Table 2 the authors focus on the abiotic elicitors that are substances of biological origin such as proteins and carbohydrates that are initiator compounds or coupling responses at the cellular level activating several enzymes or signaling canals. There are also microorganisms and chemical compounds with elicitor effect that stress the plant and produce the expression of a greater amount of metabolites or new metabolites which cause physiological changes in the plant against pathogens. As shown in Table 2, glycoprotein-type proteins produce phytoalexins that have been used to identify ion channels in cell membranes and thus transfer signals by external stimuli, as demonstrated by Alami [41] where the Plantanus x acerifoliacultures were applied to an inducer of Ceratocystis fimbriataf. sp. These, in turn, induced the synthesis of phytoalexins (hydroxycoumarin, scopoletin, and umbelliferone), and upon isolating the glycoprotein produced the synthesis of coumarin by 80%. On the other hand, oligogalacturonic acids are found in the cell wall of the plant inducing the biosynthesis of phytoalexins, whereas chitin is found in the cell wall of fungi, generating signaling factors in plants such as Hypericum perforatumproduction stress in the plant and increasing the production of phenolic compounds for their defense against pathogens [39, 42]. Rhizobacteria function as modelers of secondary metabolites with pharmacological activity. Rhizobacteria colonize the rhizospheres of the plants and improve the growth of the plant, being localized in the bark or root nodules acting as inducers of the enzymes that participate in the metabolic pathways of bioactive compounds and jasmonic acid biosynthesis; these act as signal transducers [43, 44]. Other signal inducers are the mycorrhizal fungi that help the plant to absorb more water and show defense against other pathogens such as fungi, bacteria, or parasites that affect the roots of the plant. These mycorrhizal fungi produce secondary metabolites such as phenolic compounds and alkaloids, among others [45, 46, 47, 48]. Elicitors such as salicylic acid, jasmonic acid, hydrogen peroxide, chitosan, etc. act as plant hormones in the expression of genes interacting as target signaling causing a physiological response in the plant which increases the production of phenolic compounds, vitamin C, carotenoids, or defense stimuli against pathogens; there are also synergistic effects between salicylic acid and jasmonic acid providing resistance against pathogens by the induction of the octadecanoic acid pathway [49, 50, 51, 52, 53].

Table 2.

Effect of biotic elicitor on the production of various secondary metabolites in plants [54, 55, 56, 57, 58, 59, 60, 61, 62, 63, 64].

On the other hand, Table 3 shows some research that has the influence of different abiotic elicitors that are considered substance and that are not of biological origin such as salt, drought, light or heavy metals, and temperature, among others. Table 3 shows different perspectives of research on medicinal or aromatic plants in hydroponic crops, outdoors, and the application of elicitors in different stages of growth or postharvest. For example, heavy metals such as Al3+, Cr3+, Co2+, Ni2+, Cu2+, Zn2+, and Cd2+, among others, are considered high toxicity compounds depending on the concentrations applied in the sprinkler system or because they are used as biocontrol since they alter the production of metabolites in plants. Similarly, Zobayed [65] demonstrated that the temperature in high concentrations in Panax quinqufoliusimproves the senescence of the leaves and produces a greater quantity of bioactive compounds in the root of the plant. So the investigations using high or low temperatures demonstrate the production of secondary metabolites, but the temperatures that have been investigated the most are the low producing physiological changes in the plant, increasing the lignification by the production of suberin in the cell wall and the metabolites such as sorbitol, raffinose, proline, melatonin, anthocyanins, etc. However, light by means of ultraviolet radiations generates the production of essential oils and phenolic compounds and decreases the production of toxic compounds in some plants [66]. On the other hand, salinity and drought produce death leading to cellular dehydration or osmotic stress and in certain concentrations can reduce the growth or development of plants but alter many physiological and metabolic processes that stimulate the production of polyphenolic compounds, anthocyanins, terpenes, and alkaloids, among others. Salinity can be produced in plants by ionic or osmotic means and drought by environmental or intentional changes due to water deficit which are always accompanied by temperature or solar radiation [67, 68, 69]. Then we can say that the biotic and abiotic factors are modular secondary metabolites influencing the metabolic level and the production of secondary metabolites. Therefore, the current research focuses on the use of elicitors, for the regulation of metabolic pathways, and target signaling in genes that influence the overproduction of secondary metabolites using various applications but taking care of the production performance of fruits, vegetables, or different plants.

Table 3.

Effect of abiotic elicitor on the production of various secondary metabolites in plants [70, 71, 72, 73, 74, 75, 76, 77, 78, 79, 80, 81].

Recent studies focused on evaluating the secondary metabolites of medicinal plants that are active against phytopathogens show that the potential use that these compounds can have in the future is for the control of phytopathogenic fungi, mainly against different species of Fusarium[14, 15, 16]. In this regard, the most active compounds have been found mainly in the essential oil obtained from the aerial parts of various medicinal plants, which suggests that the bioactive compounds are liposoluble; this may explain why they are active mainly against fungi, because the cell wall of these specimens are composed mainly of ergosterol, the active liposoluble compounds present in the essential oil to easily cross the cell wall of the fungus and in the interior act on their cell target, or they can alter the permeability of the wall of the fungus [82]. It can cause rupture and lysis of the fungal cell; however, it is necessary to study the toxicodynamics of these substances in order for them to know how to act in the fungi cell. On the other hand, the antifungal activity has been evaluated in vitro, by the agar diffusion and microdilution method; in general terms the range of the evaluated IC50 varies in a range that goes from 0.0035 to 8 mg/ml of the extract. It is important to mention that one of the main limitations of these studies is that this activity has only been evaluated at the laboratory level [83, 84, 85]. Table 4 shows different types of extracts made with medicinal plants, and their biological activity reported in vitrotests at the laboratory level.

Table 4.

Secondary metabolites of medicinal plants with biological activity against phytopathogens [86, 87, 88, 89, 90, 91, 92, 93, 94].

Finally, in the realization of a retrospective of the secondary metabolite modulating factors in our workgroup, Garcia-Mier [95] demonstrated that the use of mixtures of elicitors such as jasmonic acid, hydrogen peroxide, and chitosan in different concentrations applied in various stages of plant development of the sweet bell red pepper and in different stages of ripening of the fruit has a positive effect on the increase of polyphenolic and carotenoid compounds, where the results showed that the maturation stage of 95% produces a greater quantity of bioactive compounds. On the other hand, Vargas-Hernández [96] demonstrated that the foliar application of hydrogen peroxide in Capsicum chinenseJacq. has an effect on the antimicrobial activity, where the different concentrations of hydrogen peroxide potentiated the production of secondary metabolites such as flavonoids, capsaicin, and dihydrocapsaicin, where these metabolites had an effect on microorganisms such as Staphylococcus aureus, Escherichia coli, Streptococcus mutant, Salmonella thompson, Listeria monocytogenes, Streptococcus faecalis, and Candida albicans, and the results showed that the application of hydrogen peroxide increases the inhibitory effect against pathogenic microorganisms, showing greater activity against S. aureus, S. Thompson, and C. albicansin the jaguar variety, while the variety Chichen-Itza was more potent against E. faecalisand E. coli. Also, Zunun-Pérez [97] evaluated the effect of modulating factors of secondary metabolites by spray application that is performed in Capsicum annuumL. in weekly applications and 1 day before collection with elicitors such as hydrogen peroxide, salicylic acid, and oligosaccharide of xyloglucan on capsiate concentration and the expression of genes such as phenylalanine ammonia-lyase, aminotransferase, capsaicin synthase, and β-keto acyl synthase where the results showed that hydrogen peroxide in weekly applications significantly increases capsiate concentrations and gene expression and the yields of the production of the plant are not affected by the application of these elicitors.

Advertisement

4. Conclusions

The phytochemicals that produce medicinal plants derived from their secondary metabolism represent a safe and effective alternative to control various phytopathogens that affect various crops of agricultural products of economic and nutritional interest. There are different challenges in the use of biopesticides obtained from medicinal plants, such as evaluating the costs of obtaining these compounds on a large scale or exploring the possibility of them being obtained through chemical synthesis to increase yield and reduce costs. On the other hand, the various studies that exist on the effectiveness of these compounds are only at the laboratory level, which is why it is still necessary to explore and evaluate their effectiveness at the greenhouse and field levels.

Advertisement

Acknowledgments

The authors would like to acknowledge the University of Guanajuato for the grant of this publication.

Advertisement

Conflict of interest

The authors declare no conflict of interest.

References

  1. 1. Jones JDG, Dangl JL. The plant immune system. Nature. 2006;444:323-329. DOI: 10.1038/nature05286
  2. 2. FHIA. Post-Harvest Deterioration of Fresh Fruits and Vegetables by Fungi and Bacteria [Internet]. 2007. Available from:http://www.fhia.org.hn/dowloads/fhia_informa/fhiainfdic2007.pdf[Accessed: 04 January 2019]
  3. 3. Gene SM, Hoekstra PF, Hannam C, White M, Truman C, Hanson ML, et al. The role of vegetated buffers in agriculture and their regulation across Canada and the United States. Journal of Environmental Management. 2019;243:12-21. DOI: 10.1016/j.jenvman.2019.05.003
  4. 4. Sun C, Chen L, Zhai L, Liu H, Jiang Y, Wang K, et al. National assessment of spatiotemporal loss in agricultural pesticides and related potential exposure risks to water quality in China. Science of the Total Environment. 2019;677:98-107. DOI: 10.1016/j.scitotenv.2019.04.34
  5. 5. Katagi T. Bioconcentration, bioaccumulation, and metabolism of pesticides in aquatic organisms. Reviews of Environmental Contamination and Toxicology. 2010;204:1-132. DOI: 10.1007/978-1-4419-1440-8_1
  6. 6. Pelkonen O, Bennekou SH, Crivellente F, Terron A, Hernandez AF. Integration of epidemiological findings with mechanistic evidence in regulatory pesticide risk assessment: EFSA experiences. Archives of Toxicology. 2019:1-10. DOI: 10.1007/s00204-019-02467-w
  7. 7. Panseri S, Chiesa L, Ghisleni G, Marano G, Boracchi P, Ranghieri V, et al. Persistent organic pollutants in fish: Biomonitoring and cocktail effect with implications for food safety. Food Additives & Contaminants. Part A, Chemistry, Analysis, Control, Exposure & Risk Assessment. 2019;36:601-611. DOI: 10.1080/19440049.2019.1579926
  8. 8. Hao Y, Zhang H, Zhang P, Yu S, Ma D, Li L, et al. Chlorothalonil inhibits mouse ovarian development through endocrine disruption. Toxicology Letters. 2019;303:38-47. DOI: 10.1016/j.toxlet.2018.12.011
  9. 9. Abolhassani M, Asadikaram G, Paydar P, Fallah H, Aghaee-Afshar M, Moazed V, et al. Organochlorine and organophosphorus pesticides may induce colorectal cancer; a case-control study. Ecotoxicology and Environmental Safety. 2019;178:168-177. DOI: 10.1016/j.ecoenv.2019.04.030
  10. 10. Żaczek M, Weber-Dąbrowska B, Górski A. Phages in the global fruit and vegetable industry. Journal of Applied Microbiology. 2015;118:537-556. DOI: 10.1111/jam.12700
  11. 11. Pino-Otín MR, Ballestero D, Navarro E, González-Coloma A, Val J, Mainar AM. Ecotoxicity of a novel biopesticide fromArtemisia absinthiumon non-target aquatic organisms. Chemosphere. 2019;216:131-146. DOI: 10.1016/j.chemosphere.2018.09.071
  12. 12. Pino-Otín MR, Val J, Ballestero D, Navarro E, Sánchez E, González-Coloma A, et al. Ecotoxicity of a new biopesticide produced byLavandula luisierion non-target soil organisms from different trophic levels. Science of the Total Environment. 2019;671:83-93. DOI: 10.1016/j.scitotenv.2019.03.293
  13. 13. Yamada T, Hamada M, Floreancig P, Nakabachi A. Diaphorin, a polyketide synthesized by an intracellular symbiont of the Asian citrus psyllid, is potentially harmful for biological control agents. PLoS One. 2019;14:e0216319. DOI: 10.1371/journal.pone.0216319
  14. 14. Mafakheri H, Mirghazanfari SM. Antifungal activity of the essential oils of some medicinal plants against human and plant fungal pathogens. Cellular and Molecular Biology. 2018;64:13-19
  15. 15. Isaac GS, Abu-Tahon MA.In vitroantifugal activity of medicinal plant extract againstFusarium oxysporumF. sp.lycopersicirace 3 the causal agent of tomato wilt. Acta Biologica Hungarica. 2014;65:107-118. DOI: 10.1556/ABiol.65.2014.1.10
  16. 16. Askarne L, Talibi I, Boubaker H, Boudyach EH, Msanda F, Saadi B, et al. Use of Moroccan medicinal plant extracts as botanical fungicide against citrus blue mould. Letters in Applied Microbiology. 2013;56:37-43. DOI: 10.1111/lam.12012
  17. 17. Mohamed EZ. Impact of mycotoxins on humans and animals. Journal of Saudi Chemical Society. 2011;15:129-144. DOI: 10.1016/j.jscs.2010.06.006
  18. 18. Molina A, Chavarría G, Alfaro-Cascante M, Leiva A, Granados-Chinchilla F. Mycotoxins at the start of the food chain in Costa Rica: Analysis of six Fusarium toxins and ochratoxin a between 2013 and 2017 in animal feed and aflatoxin M1 in dairy products. Toxins. 2019;11:E312. DOI: 10.3390/toxins11060312
  19. 19. Thiour-Mauprivez C, Martin-Laurent F, Calvayrac C, Barthelmebs L. Effects of herbicide on non-target microorganisms: Towards a new class of biomarkers? Science of the Total Environment. 2019;684:314-325. DOI: 10.1016/j.scitotenv.2019.05.230
  20. 20. Tahir HM, Basheer T, Ali S, Yaqoob R, Naseem S, Khan SY. Effect of pesticides on biological control potential ofNeoscona theisi(Araneae: Araneidae). Journal of Insect Science. 2019;19:pii:17. DOI: 10.1093/jisesa/iez024
  21. 21. Brunton LL, Chabner BA, Knollman B. Goodman & Gilman’s the Pharmacological Basis of Therapeutics. 12th ed. Vol. 17-39. United States: McGraw-Hill; 2012. pp. 123-143
  22. 22. Katzung BG, Masters SB, Trevor AJ. Basic & Clinical Pharmacology. 12th ed. United States: McGraw-Hill; 2013. pp. 37-68
  23. 23. Jimenez-Garcia SN, Guevara-Gonzalez RG, Miranda-Lopez R, Feregrino-Perez AA, Torres-Pacheco I, Vazquez-Cruz MA. Functional properties and quality characteristics of bioactive compounds in berries: Biochemistry, biotechnology, and genomics. Food Research International. 2013;54:1195-1207. DOI: 10.1016/j.foodres.2012.11.004
  24. 24. Jimenez-Garcia SN, Vazquez-Cruz MA, Guevara-Gonzalez RG, Torres-Pacheco I, Cruz-Hernandez A, Feregrino-Perez AA. Current approaches for enhanced expression of secondary metabolites as bioactive compounds in plants for agronomic and human health purposes—A review. Polish Journal of Food and Nutrition Sciences. 2013;63:67-78. DOI: 10.2478/v10222-012-0072-6
  25. 25. Khalid M, Rahman S-u, Bilal M. Role of flavonoids in plant interactions with the environment and against human pathogens—A review. Journal of Integrative Agriculture. 2019;18:211-230. DOI: 10.1016/s2095-3119(19)62555-4
  26. 26. Zhao C, Liu Y, Lai S, Cao H, Guan Y, San Cheang W, et al. Effects of domestic cooking process on the chemical and biological properties of dietary phytochemicals. Trends in Food Science and Technology. 2019;01:55-66. DOI: 10.1016/j.tifs.2019.01.004
  27. 27. Sahebi M, Hanafi MM, van Wijnen AJ, Akmar ASN, Azizi P, Idris AS, et al. Profiling secondary metabolites of plant defence mechanisms and oil palm in response toGanoderma boninenseattack. International Biodeterioration and Biodegradation. 2017;122:151-164. DOI: 10.1016/j.ibiod.2017.04.016
  28. 28. Valduga AT, Gonçalves IL, Magri E, Delalibera FJR. Chemistry, pharmacology and new trends in traditional functional and medicinal beverages. Food Research International. 2019;120:478-503. DOI: 10.1016/j.foodres.2018.10.091
  29. 29. Chakraborty P. Herbal genomics as tools for dissecting new metabolic pathways of unexplored medicinal plants and drug discovery. Biochime Open. 2018;6:9-16. DOI: 10.1016/j.biopen.2017.12.003
  30. 30. Jamwal K, Bhattacharya S, Puri S. Plant growth regulator mediated consequences of secondary metabolites in medicinal plants. Journal of Applied Research on Medicinal and Aromatic Plants. 2018;9:26-38. DOI: 10.1016/j.jarmap.2017.12.003
  31. 31. Frérot B, Leppik E, Groot AT, Unbehend M, Holopainen JK. Chemical signatures in plant-insect interactions. In: Sauvion N, Thiéry D, Calatayud PA, editors. Insect-Plant Interact a Crop Prot Perspect. 1st ed. London, United Kingdom: Academic Press; 2017. pp. 139-177. Available from:http://www.sciencedirect.com/science/article/pii/S0065229616300982
  32. 32. McCutcheon SC, Jørgensen SE. Phytoremediation. In: Jørgensen SE, Fath BD, editors. Encyclopedia of Ecology. 1st ed. Oxford: Academic Press; 2008. pp. 2751-2766. Available from:http://www.sciencedirect.com/science/article/pii/B9780080454054000690
  33. 33. Hounsome N, Hounsome B, Tomos D, Edwards-Jones G. Plant metabolites and nutritional quality of vegetables. Journal of Food Science. 2008;73:48-65. DOI: 10.1111/j.1750-3841.2008.00716.x
  34. 34. VanEtten HD, Sandrock RW, Wasmann CC, Soby SD, McCluskey K, Wang P. Detoxification of phytoanticipins and phytoalexins by phytopathogenic fungi. Canadian Journal of Botany. 1995;73:518-525. DOI: 10.1139/b95-291
  35. 35. Morrissey J, Lou GM. Iron uptake and transport in plants: The good, the bad, and the ionome. Chemical Reviews. 2009;109:4553-4567. DOI: 10.1021/cr900112r
  36. 36. Zaynab M, Fatima M, Abbas S, Sharif Y, Umair M, Zafar MH, et al. Role of secondary metabolites in plant defense against pathogens. Microbial Pathogenesis. 2018;124:198-202. DOI: 10.1016/j.micpath.2018.08.034
  37. 37. Seppänen SK, Syrjälä L, Von Weissenberg K, Teeri TH, Paajanen L, Pappinen A. Antifungal activity of stilbenes inin vitrobioassays and in transgenicPopulusexpressing a gene encoding pinosylvin synthase. Plant Cell Reports. 2004;22:584-593. DOI: 10.1007/s00299-003-0728-0
  38. 38. Del Cueto J, Møller BL, Dicenta F, Sánchez-Pérez R. β-Glucosidase activity in almond seeds. Plant Physiology and Biochemistry. 2018;126:163-172. DOI: 10.1016/j.plaphy.2017.12.028
  39. 39. Gadzovska Simic S, Tusevski O, Maury S, Delaunay A, Joseph C, Hagège D. Effects of polysaccharide elicitors on secondary metabolite production and antioxidant response inHypericum perforatumL. shoot cultures. Scientific World Journal. 2014;2014:609649. DOI: 10.1155/2014/609649
  40. 40. Sathiyabama M, Bernstein N, Anusuya S. Chitosan elicitation for increased curcumin production and stimulation of defence response in turmeric (Curcuma longaL.). Industrial Crops and Products. 2016;89:87-94. DOI: 10.1016/j.indcrop.2016.05.007
  41. 41. Alami I, Mari S, Clérivet A. A glycoprotein fromCeratocystis fimbriataf. sp.platanitriggers phytoalexin synthesis inPlatanus × acerifoliacell-suspension cultures. Phytochemistry. 1998;48:771-776. DOI: 10.1016/S0031-9422(97)00892-3
  42. 42. Gadzovska Simic S, Tusevski O, Maury S, Delaunay A, Lainé E, Joseph C, et al. Polysaccharide elicitors enhance phenylpropanoid and naphtodianthrone production in cell suspension cultures ofHypericum perforatum. Plant Cell, Tissue and Organ Culture. 2015;122:649-663. DOI: 10.1007/s11240-015-0798-z
  43. 43. Hemashenpagam N, Selvaraj T. Effect of arbuscular mycorrhizal (AM) fungus and plant growth promoting rhizomicroorganisms (PGPR’s) on medicinal plantSolanum viarumseedlings. Journal of Environmental Biology. 2011;32:579-583
  44. 44. Vafadar F, Amooaghaie R, Otroshy M. Effects of plant-growth-promoting rhizobacteria and arbuscular mycorrhizal fungus on plant growth, stevioside, NPK, and chlorophyll content ofStevia rebaudiana. Journal of Plant Interactions. 2013;9:128-136. DOI: 10.1080/17429145.2013.779035
  45. 45. Kurosaki F, Yamashita A, Arisawa M. Involvement of GTP-binding protein in the induction of phytoalexin biosynthesis in cultured carrot cells. Plant Science. 2001;161:273-278. DOI: 10.1016/S0168-9452(01)00407-1
  46. 46. Bais HP, Walker TS, Schweizer HP, Vivanco JM. Root specific elicitation and antimicrobial activity of rosmarinic acid in hairy root cultures ofOcimum basilicum. Plant Physiology and Biochemistry. 2002;40:983-995. DOI: 10.1016/S0981-9428(02)01460-2
  47. 47. Singh G, Gavrieli J, Oakey JS, Curtis WR. Interaction of methyl jasmonate, wounding and fungal elicitation during sesquiterpene induction inHyoscyamus muticusin root cultures. Plant Cell Reports. 1998;17:391-395. DOI: 10.1007/s002990050412
  48. 48. Yang D, Ma P, Liang X, Wei Z, Liang Z, Liu Y, et al. PEG and ABA trigger methyl jasmonate accumulation to induce the MEP pathway and increase tanshinone production inSalvia miltiorrhizahairy roots. Physiologia Plantarum. 2012;146:173-183. DOI: 10.1111/j.1399-3054.2012.01603.x
  49. 49. Xu A, Zhan JC, Huang WD. Effects of ultraviolet C, methyl jasmonate and salicylic acid, alone or in combination, on stilbene biosynthesis in cell suspension cultures ofVitis viniferaL. cv. Cabernet Sauvignon. Plant Cell, Tissue and Organ Culture. 2015;122:197-211. DOI: 10.1007/s11240-015-0761-z
  50. 50. Hao X, Shi M, Cui L, Xu C, Zhang Y, Kai G. Effects of methyl jasmonate and salicylic acid on tanshinone production and biosynthetic gene expression in transgenicSalvia miltiorrhizahairy roots. Biotechnology and Applied Biochemistry. 2015;62:24-31. DOI: 10.1002/bab.1236
  51. 51. Xu YW, Lv SS, Zaho D, Chen JW, Yang WT, Wu W. Effects of salicylic acid on monoterpene production and antioxidant systems inHouttuynia cordata. African Journal of Biotechnology. 2012;11:1364-1372. DOI: 10.5897/AJB11.1524
  52. 52. Chodisetti B, Rao K, Gandi S, Giri A. Gymnemic acid enhancement in the suspension cultures ofGymnema sylvestreby using the signaling molecules—Methyl jasmonate and salicylic acid.In VitroCellular & Developmental Biology—Plant. 2015;51:88-92. DOI: 10.1007/s11627-014-9655-8
  53. 53. Krzyzanowska J, Czubacka A, Pecio L, Przybys M, Doroszewska T, Stochmal A, et al. The effects of jasmonic acid and methyl jasmonate on rosmarinic acid production inMentha piperitacell suspension cultures. Plant Cell, Tissue and Organ Culture. 2012;108:73-81. DOI: 10.1007/s11240-011-0014-8
  54. 54. Hayashi H, Huang P, Inoue K. Up-regulation of soyasaponin biosynthesis by methyl jasmonate in cultured cells ofGlycyrrhiza glabra. Plant & Cell Physiology. 2003;44:404-411. DOI: 10.1093/pcp/pcg054
  55. 55. Hu X, Neill S, Cai W, Tang Z. Hydrogen peroxide and jasmonic acid mediate oligogalacturonic acid-induced saponin accumulation in suspension-cultured cells ofPanax ginseng. Physiologia Plantarum. 2003;118:414-421. DOI: 10.1034/j.1399-3054.2003.00124.x
  56. 56. Taurino M, Ingrosso I, D’amico L, De Domenico S, Nicoletti I, Corradini D, et al. Jasmonates elicit different sets of stilbenes inVitis viniferacv. Negramaro cell cultures. Springerplus. 2015;4:49. DOI: 10.1186/s40064-015-0831-z
  57. 57. Gorelick J, Rosenberg R, Smotrich A, Hanuš L, Bernstein N. Hypoglycemic activity of withanolides and elicitatedWithania somnifera. Phytochemistry. 2015;116:283-289. DOI: 10.1016/j.phytochem.2015.02.029
  58. 58. Ghorbanpour M, Hatami M, Kariman K, Dahaji PA. Phytochemical variations and enhanced efficiency of antioxidant and antimicrobial ingredients inSalvia officinalisas inoculated with different rhizobacteria. Chemistry & Biodiversity. 2016;13:319-330. DOI: 10.1002/cbdv.201500082
  59. 59. Banchio E, Bogino PC, Santoro M, Torres L, Zygadlo J, Giordano W. Systemic induction of monoterpene biosynthesis inOriganum majoricumby soil bacteria. Journal of Agricultural and Food Chemistry. 2010;58:650-654. DOI: 10.1021/jf9030629
  60. 60. Banchio E, Xie X, Zhang H, Paré PW. Soil bacteria elevate essential oil accumulation and emissions in sweet basil. Journal of Agricultural and Food Chemistry. 2009;57:653-657. DOI: 10.1021/jf8020305
  61. 61. del Rosario Cappellari L, Santoro MV, Nievas F, Giordano W, Banchio E. Increase of secondary metabolite content in marigold by inoculation with plant growth-promoting rhizobacteria. Applied Soil Ecology. 2013;70:16-22. DOI: 10.1016/j.apsoil.2013.04.001
  62. 62. Liang Z, Ma Y, Xu T, Cui B, Liu Y, Guo Z, et al. Effects of abscisic acid, gibberellin, ethylene and their interactions on production of phenolic acids inSalvia miltiorrhizabunge hairy roots. PLoS One. 2013;8:e72806. DOI: 10.1371/journal.pone.0072806
  63. 63. McSteen P, Zhao Y. Plant hormones and signaling: Common themes and new developments. Developmental Cell. 2008;14:467-473. DOI: 10.1016/j.devcel.2008.03.013
  64. 64. Abbasi BH, Stiles AR, Saxena PK, Liu CZ. Gibberellic acid increases secondary metabolite production inEchinacea purpureahairy roots. Applied Biochemistry and Biotechnology. 2012;168:2057-2066. DOI: 10.1007/s12010-012-9917-z
  65. 65. Zobayed SMA, Afreen F, Kozai T. Temperature stress can alter the photosynthetic efficiency and secondary metabolite concentrations in St. John’s wort. Plant Physiology and Biochemistry. 2005;43:977-984. DOI: 10.1016/j.plaphy.2005.07.013
  66. 66. Binder BYK, Peebles CAM, Shanks JV, San K-Y. The effects of UV-B stress on the production of terpenoid indole alkaloids inCatharanthus roseushairy roots. Biotechnology Progress. 2009;25:861-865. DOI: 10.1002/btpr.97
  67. 67. Tari I, Kiss G, Deér AK, Csiszár J, Erdei L, Gallé A, et al. Salicylic acid increased aldose reductase activity and sorbitol accumulation in tomato plants under salt stress. Biologia Plantarum. 2010;54:677-683. DOI: 10.1007/s10535-010-0120-1
  68. 68. Liu H, Wang X, Wang D, Zou Z, Liang Z. Effect of drought stress on growth and accumulation of active constituents inSalvia miltiorrhizabunge. Industrial Crops and Products. 2011;33:84-88. DOI: 10.1016/j.indcrop.2010.09.006
  69. 69. Gupta P, Sharma S, Saxena S. Biomass yield and steviol glycoside production in callus and suspension culture ofStevia rebaudianatreated with proline and polyethylene glycol. Applied Biochemistry and Biotechnology. 2015;176:863-874. DOI: 10.1007/s12010-015-1616-0
  70. 70. Threlfall DR, Whitehead IM. The use of biotic and abiotic elicitors to induce the formation of secondary plant products in cell suspension cultures of solanaceous plants. Biochemical Society Transactions. 1988;16:71-75. DOI: 10.1042/bst0160071
  71. 71. Furze JM, Rhodes MJ, Parr AJ, Robins RJ, Withehead IM, Threlfall DR. Abiotic factors elicit sesquiterpenoid phytoalexin production but not alkaloid production in transformed root cultures ofDatura stramonium. Plant Cell Reports Germany. 1991;10:111-114. DOI: 10.1007/BF00232039
  72. 72. Shakeran Z, Keyhanfar M, Asghari G, Ghanadian M. Improvement of atropine production by different biotic and abiotic elicitors in hairy root cultures ofDatura metel. Turkish Journal of Biology. 2015;39:111-118. DOI: 10.3906/biy-1405-25
  73. 73. Cai Z, Kastell A, Speiser C, Smetanska I. Enhanced resveratrol production inVitis viniferacell suspension cultures by heavy metals without loss of cell viability. Applied Biochemistry and Biotechnology. 2013;171:330-340. DOI: 10.1007/s12010-013-0354-4
  74. 74. Savitha BC, Thimmaraju R, Bhagyalakshmi N, Ravishankar GA. Different biotic and abiotic elicitors influence betalain production in hairy root cultures ofBeta vulgarisin shake-flask and bioreactor. Process Biochemistry. 2006;41:50-60. DOI: 10.1016/j.procbio.2005.03.071
  75. 75. Jochum GM, Mudge KW, Thomas RB. Elevated temperatures increase leaf senescence and root secondary metabolite concentrations in the understory herbPanax quinquefolius(Araliaceae). American Journal of Botany. 2007;94:819-826. DOI: 10.3732/ajb.94.5.819
  76. 76. Zhao Y, Qi L-W, Wang W-M, Saxena PK, Liu C-Z. Melatonin improves the survival of cryopreserved callus ofRhodiola crenulata. Journal of Pineal Research. 2011;50:83-88. DOI: 10.1111/j.1600-079X.2010.00817.x
  77. 77. Chan LK, Koay SS, Boey PL, Bhatt A. Effects of abiotic stress on biomass and anthocyanin. Biological Research. 2010;43:127-135. DOI: /S0716-97602010000100014
  78. 78. Liu W, Liu C, Yang C, Wang L, Li S. Effect of grape genotype and tissue type on callus growth and production of resveratrols and their piceids after UV-C irradiation. Food Chemistry. 2010;122:475-481. DOI: 10.1016/j.foodchem.2010.03.055
  79. 79. Bor M, Seckin B, Ozgur R, YIlmaz O, Ozdemir F, Turkan I. Comparative effects of drought, salt, heavy metal and heat stresses on gamma-aminobutyric acid levels of sesame (Sesamum indicumL.). Acta Physiologiae Plantarum. 2009;31:655-659. DOI: 10.1007/s11738-008-0255-2
  80. 80. Chen Y, Guo Q, Liu L, Liao L, Zhu Z. Influence of fertilization and drought stress on the growth and production of secondary metabolites inPrunella vulgarisL. The Journal of Medicinal Plants Research. 2011;5:1749-1755
  81. 81. Pavlík M, Vacek J, Klejdus B, Kubáň V. Hypericin and hyperforin production in St. John’s wortin vitroculture: Influence of saccharose, polyethylene glycol, methyl jasmonate, and agrobacterium tumefaciens. Journal of Agricultural and Food Chemistry. 2007;55:6147-6153. DOI: 10.1021/jf070245w
  82. 82. Butassi E, Svetaz LA, Zhou S, Wolfender JL, Cortés JCG, Ribas JC, et al. The antifungal activity and mechanisms of action of quantified extracts from berries, leaves and roots ofPhytolacca tetramera. Phytomedicine. 2019;16:152884. DOI: 10.1016/j.phymed.2019.152884
  83. 83. Talibi I, Askarne L, Boubaker H, Boudyach EH, Msanda F, Saadi B, et al. Antifungal activity of Moroccan medicinal plants against citrus sour rot agentGeotrichum candidum. Letters in Applied Microbiology. 2012;55:155-161. DOI: 10.1111/j.1472-765X.2012.03273.x
  84. 84. Anaruma ND, Schmidt FL, Duarte MC, Figueira GM, Delarmelina C, Benato LA, et al. Control ofColletotrichum gloeosporioides(penz.) Sacc. In yellow passion fruit usingCymbopogon citratusessential oil. Brazilian Journal of Microbiology. 2010;41:66-73. DOI: 10.1590/S1517-838220100001000012
  85. 85. Zhao W, Xu LL, Zhang X, Gong XW, Zhu DL, Xu XH, et al. Three new phenanthrenes with antimicrobial activities from the aerial parts ofJuncus effusus. Fitoterapia. 2018;130:247-250. DOI: 10.1016/j.fitote.2018.09.007
  86. 86. Rodríguez AT, Morales D, Ramírez MA. Efecto de extractos vegetales sobre el crecimientoin vitrode hongos fitopatógenos. Cultivos Tropicales. 2000;21:79-82
  87. 87. Salhi N, Saghir SAM, Terzi V, Brahmi I, Ghedairi N, Bissati S. Antifungal activity of aqueous extracts of some dominant Algerian medicinal plants. BioMed Research International. 2017;2017:7526291. DOI: 10.1155/2017/7526291
  88. 88. Mongalo NI, Dikhoba PM, Soyingbe SO, Makhafola TJ. Antifungal, anti-oxidant activity and cytotoxicity of south African medicinal plants against mycotoxigenic fungi. Heliyon. 2018;4:e00973. DOI: 10.1016/j.heliyon.2018.e00973
  89. 89. Mahlo SM, Chauke HR, McGaw L, Eloff J. Antioxidant and antifungal activity of selected medicinal plant extracts against phytopathogenic fungi. African Journal of Traditional, Complementary, and Alternative Medicines. 2016;13:216-222. DOI: 10.21010/ajtcam.v13i4.28
  90. 90. Costa E, Silva J, de Sousa Carlos Mourão D, de Oliveira Lima FS, de Almeida Sarmento R, Sunti Dalcin M, et al. The efficiency of noni (Morinda citrifoliaL.) essential oil on the control of leaf spot caused byExserohilum turcicumin maize culture. Medicines. 2017;4:60. DOI: 10.3390/medicines4030060
  91. 91. Nkomo MM, Katerere D, Vismer H, Cruz TT, Stephane S, Balayssac SS, et al. Fusarium inhibition by wild populations of the medicinal plantSalvia africana-lutea L. linked to metabolomic profiling. BMC Complementary and Alternative Medicine. 2014;14(99):2-9. DOI: 10.1186/1472-6882-14-99
  92. 92. Elshafie HS, Grul’ová D, Baranová B, Caputo L, De Martino L, Sedlák V, et al. Antimicrobial activity and chemical composition of essential oil extracted fromSolidago canadensisL. growing wild in Slovakia. Molecules. 2019;24:1206. DOI: 10.3390/molecules24071206
  93. 93. Tabti L, Amine Dib ME, Gaouar N, Samira B, Tabti B. Antioxidant and antifungal activity of extracts of the aerial parts ofThymus capitatus(L.) Hoffmanns against four phytopathogenic fungi ofCitrus sinensis. Jundishapur Journal of Natural Pharmaceutical Products. 2014;9:49-54. DOI: 10.17795/jjnpp-13972
  94. 94. Slazak B, Kapusta M, Strömstedt AA, Słomka A, Krychowiak M, Shariatgorji M, et al. How does the sweet violetViola odorataL. fight pathogens and pests-cyclotides as a comprehensive plant host defense system. Frontiers in Plant Science. 2018;9:1296. DOI: 10.3389/fpls.2018.01296
  95. 95. Garcia-Mier L, Jimenez-Garcia SN, Guevara-González RG, Feregrino-Perez AA, Contreras-Medina LM, Torres-Pacheco I. Elicitor mixtures significantly increase bioactive compounds, antioxidant activity, and quality parameters in sweet bell pepper. Journal of Chemistry. 2015;2015:8. DOI: 10.1155/2015/269296. Article ID: 269296
  96. 96. Vargas-Hernández M, Torres-Pacheco I, Gautier F, Álvarez-Mayorga B, Cruz-Hernández A, García-Mier L, et al. Influence of hydrogen peroxide foliar applications onin vitroantimicrobial activity inCapsicum chinenseJacq. Plant Biosystems. 2017;151:269-275. DOI: 10.1080/11263504.2016.1168494
  97. 97. Zunun-Pérez AY, Guevara-Figueroa T, Jimenez-Garcia SN, Feregrino-Pérez AA, Gautier F, Guevara-González RG. Effect of foliar application of salicylic acid, hydrogen peroxide and a xyloglucan oligosaccharide on capsiate content and gene expression associated with capsinoids synthesis inCapsicum annuumL. Journal of Biosciences. 2017;42:245-250. DOI: 10.1007/s12038-017-9682-9

Written By

Xóchitl S. Ramírez-Gómez, Sandra N. Jiménez-García, Vicente Beltrán Campos and Ma. Lourdes García Campos

Submitted: April 1st, 2019 Reviewed: June 11th, 2019 Published: July 15th, 2019