Production of Secondary Metabolites in Plants under Abiotic Stress: An Overview

Now a day, plants, a source of natural antioxidants are facing various kinds of environmental stress during their growth and development. Under stress, plants have potential to synthesize several secondary metabolites to cope with the adverse effects of stress. In the present review paper, the information on the effects of different abiotic stresses on the levels of secondary metabolites in plants is summarised. The production of secondary metabolites in plants can be enhanced by modifying their environmental conditions.


Introduction
Plants possess two types of metabolism called primary metabolism and secondary metabolism. Primary metabolism is related with the production of metabolites such as carbohydrates, amino acids, lipids etc., utilized by the plants for their growth and development. On other hand secondary metabolism is associated with the production of compounds involved in the protection of plants against various abiotic and biotic stresses. Secondary products are synthesized from primary metabolites. Secondary metabolites are important compounds for the human beings as they are sources for food additives, flavours, pharmaceuticals and industrially important pharmaceuticals [1,2], cosmetics, nutraceuticals, etc. Plant secondary metabolites such as morphine, codeine, cocaine, quinine etc., are commonly used in medicine. Alkaloids like, atropine, colchicine, phytostigminine, pilocarpine, reserpine and steroids like diosgenin, digoxin and digitoxin, flavonoids, phenolic, etc., are also the sources of different types of medicines [3].
Environmental stresses affect the metabolism of plants. Plants challenged with different types of abiotic and biotic stresses results into the reduction of different morphological characters such as height, leaf number, leaf area, number of branches, root volume, etc. [4] which ultimately leads to reduction of biomass production. There are different types of abiotic stress such as drought, low and high temperatures, salinity, alkalinity, ultraviolet radiation, ozone, metal ions, etc., which affect the metabolism of the plants. In normal metabolic conditions the synthesis of secondary plant products is often low as plant do not have any defence strategies due to lack of any stress. The synthesis of secondary metabolites is generally increasing when plants suffer with biotic and abiotic stresses. Accumulation of phenylpropenoids and phenolic compounds were found higher during stress condition in plants [5,6]. The concentrations of various secondary plant products are strongly dependent on the growing conditions and physiology through altering the metabolic pathways responsible for the accumulation of the related natural products [4]. The expression levels of certain genes governing the production of such compounds have also been shown to be increased in response to various abiotic stresses [7]. In this review, we have summarized the information about the effects of different abiotic stresses on the synthesis of secondary metabolites in plants.

Responses of Plants to Abiotic Stresses
Plant have potential to adopt some strategies to neutralize the effects of various abiotic stresses such as high and low temperature, salinity, alkalinity, UV, heavy metals, drought etc. The normal metabolism of plants got disturbed under stressed into decreased in growth and productivity and triggered a series of molecular, biochemical, physiological and morphological changes in plants. A stress response is induced when plants recognized the stress at the cellular level. During drought, plants might have tended to decrease the leaf area, to reduce the water loss through respiration, promote the leaf abscission, extend their root, etc., which is regulated by a combination of plant hormones. When plant suffer with oxidative stress, they synthesize the various secondary compounds and increases the level of different endogenous enzymes such as superoxide dismutase (SOD), catalase, (CAT), ascorbate peroxidase (APX), guaiacol peroxidase (GPX), and glutathione reductase (GR) and non-enzymatic antioxidants like ascorbate (AsA), glutathione (GSH), to reduce the effect of reactive oxygen species (ROS) produced in various stresses. Secondary metabolites are involved in protective functions in response to both biotic and abiotic stress conditions. Formation of phenyl amides and dramatic accumulation of polyamines in bean and tobacco under the influence of abiotic stresses were reported and suggested antioxidant role of these secondary metabolites by Edreva et al. [8]. Similarly, anthocyanin accumulation is stimulated by various environmental stresses, such as UV, blue light, high intensity light, wounding, pathogen attack, drought, sugar and nutrient deficiency [9]. Under the stress condition, the primary metabolisms of plant get decline due to unfavourable condition created by different environmental factors. Plants under stress reduce the effect of different abiotic as well as biotic stresses by the synthesizing the more secondary metabolites than normal conditions. These secondary products are biosynthesized from the products of primary metabolisms such as carbohydrates, lipid, and amino acids ( Figure 1).

Effect of Drought
Drought is one of the most significant abiotic stresses which have adverse effect on growth and development of plants [10]. Drought stress occurs when the available water in the soil is low to some critical levels for the plants. Drought causes huge damage to the physiological machinery of the plants resulting in degradation of morphological topology, anatomical structure and biochemical activity i.e. enzyme activity, protein content, sugar content, etc. Drought often causes oxidative stress and was reported to show increase in the amounts of flavonoids and phenolic acids in willow leaves [11]. Morphine content in Papaver somniferum [12], glucocides content in [13] was found increased under water deficit condition as compared to normal. Total phenolic, total flavonoid, anthocyanin and polyphenolic compounds, which promoted the antioxidant capacities of Chrysanthemum sp was found increasing during drought condition [14]. The content of anthocyanin, flavonoid increases during the water stress and these compounds have protective role during drought condition in Pisum sativum [15]. In drought condition saponin content was found to be lower in Chenopodium quinoa [16] (Table 1).

Effects of Heavy Metal
Heavy metals are important to the plants as they are the major unit of various enzymes such as Zn in carbonic anhydrase, Mo and Fe in nitrogenase, Cu in superoxide dismutase, etc. Metals such as Cr, Cu, Mn, and Fe can also directly generate oxidative injury via undergoing Haber-Weiss and Fenton reactions, which leads to the formation of ROS or oxygen free radicals' species in plants, resulting in cell homeostasis disruption, DNA strand breakage, defragmentation of proteins, or cell membrane and damage to photosynthetic pigments, which may trigger cell death. Plant adopts different mechanisms and synthesizes different secondary products to copup with the problems associated with heavy metals. It was noticed that the anthocyanin content in the leaf of lettuce (Lactuca sativa L.) was decline due to Ni stress [33]. According to Singh & Sinha [29], cumulative accumulation of Cr, Fe, Zn and Mn increased oil production upto 35% in Brassica juncea L plant. Betalains content in Beta vulgaris L. plant is stimulated by Cu 2+ [34]. According to Sharma et al. [32], thiol, proline, total phenolics, ascorbic acid content and peroxidase activity were found to be increased in Lady's Finger (Abelmoschus esculentus L.) with increasing in Cd concentration in soil (Table 1). To reduce the effect of oxidative stress, plants have defensive strategies to scavenge the free radicals. Plant cells have developed antioxidant defense mechanism which is comprises of different endogenous enzymatic antioxidants (SOD, CAT, APX, GPX, and GR) and non-enzymatic antioxidants ascorbate (AsA), glutathione (GSH), carotenoids, alkaloids, tocopherols, proline, and phenolic compounds i.e. flavonoids, tannins, and lignin) act as the scavengers of free radicals [35,36].

Effects of Salinity Stress
Salinity is one of the important abiotic factors which reduce the growth and developments of the plants. Salinity in the plant cells causes ionic, osmotic, and oxidative stresses [3]. Synthesis of different osmolites like glycine betain, proline, sorbitol, mannitol, pinitol, and sucrose etc., is one of the important ways to resist in saline condition in plant. Golkar & Taghizadeh [20] found that the secondary plant products i.e. proline, glycine betain, carotenoids, total phenolic contents, total flavonoids were increasing when salinity increases upto 200mM NaCl concentration in Carthamus tinctorius L. plant. During salt stress, different secondary metabolite products such as sorbitol and jasmonic acid in Lycopersicon esculentum L. plant [21], sucrose and starch in Cenchrus pennisetiformis L. plant [37], polyamines in Oryza sativa L. plant [22] were reported to be increased ( Table 1).

Effects of Temperature
Temperature regulates the growth and developmental processes of plants. Plant faces generally two types of stress with reference to temperature; high and low temperature. High temperature in plants adversely affects the normal metabolic processes which can induce premature leaf senescence, reduce the rate of photosynthesis and biomass production in plants. Low temperature in plants causes a series of abiotic stresses including osmotic injury, desiccation, oxidative stresses, etc [3]. Low and high temperature affect the biosynthetic process of different secondary metabolites to resist with that stress. In low temperature environment, plant metabolism leads to synthesis of cryoprotectant compounds like sugar alcohols (sorbitol, ribitol, inositol), soluble sugars (saccharose, raffinose, stachyose, trehalose), and low-molecular weight nitrogenous compounds (proline, glycine betaine) [38] to cop up with adverse effects of the low temperature stress. Cold stresses enhance the production of phenolic compounds (Table 1) [39]. Molmann et al.
[24] reported that the concentrations of quercetin and kaempferol in Medicago sativa L. plant were higher at the warmer temperature and more putrescine content was observed under low temperature environment [40]. Hummel et al. [23] investigated that in low temperature there was an increase in levels of polyamines (agmatine and putrescine) and their levels could be a significant marker of chilling tolerance in seedlings of Pringlea antiscorbutica. Carotenoids contents in Brassicaceae family, including β-carotene, were found to be slightly decreased at high temperature [25].

Effects of Light
In plant metabolism, light play a significant role in production of secondary plant products. Light intensity can promote photosynthesis and enhance dry matter accumulation, whereas excessive irradiation will evoke photo-damage in plants and markedly influenced the plant growth and development. Light enhanced the biosynthesis of secondary metabolites including gingerol and zingiberene in culture of Zingiber officinale L. plant (Table 1) [27]. UV-B exposure increased in flavonoids content in barley [28] and polyamines in cucumber, flavonols in Norway spruce, Picea abies. Yu et al. [41] investigated that light enhanced the biosynthesis of terpenoid indole alkaloids in Catharanthus roseus L plants (Table 1)