Role and Regulation of Plants Phenolics in Abiotic Stress Tolerance

C H A P T E R

9 Role and Regulation of Plants Phenolics in Abiotic Stress Tolerance: An Overview Mohd Irfan Naikoo1, Mudasir Irfan Dar1, Fariha Raghib1, Hassan Jaleel2, Bilal Ahmad2, Aamir Raina3,4, Fareed Ahmad Khan1 and Fauzia Naushin3 1

Plant Ecology and Environment Laboratory, Department of Botany, Aligarh Muslim University, Aligarh, Uttar Pradesh, India 2Plant Physiology Laboratory, Department of Botany, Aligarh Muslim University, Aligarh, Uttar Pradesh, India 3Botany Section, Women’s College, Aligarh Muslim University, Aligarh, Uttar Pradesh, India 4 Mutation Breeding Laboratory, Department of Botany, Aligarh Muslim University, Aligarh, Uttar Pradesh, India

O U T L I N E 9.1 Introduction

157

9.2 Structure and Classification

158

9.3 Biosynthesis of Polyphenols

158

9.4 Phenolics and Abiotic Stress Tolerance 158 9.4.1 Phenolics as Ultraviolet Sunscreens 161 9.4.2 Plant Phenolics and Their Role in Heavy Metal Stress 162 9.4.3 Plant Phenolics and Their Role in Drought Stress 163

9.1 INTRODUCTION Plants are exposed to multifarious abiotic stresses in constantly changing environments that are unfavorable for growth and development (Zhu, 2016). These abiotic stresses include water (drought and flooding), heavy metals, salinity, excess or deficiency of nutrients, high and low temperatures (chilling and freezing), extreme levels of light (high and low), radiation

Plant Signaling Molecules. DOI: https://doi.org/10.1016/B978-0-12-816451-8.00009-5

9.4.4 Plant Phenolics and Their Role in Cold Stress 163 9.4.5 Plant Phenolics and Their Role in Nutrient Stress 163 9.5 Conclusion and Future Prospects

164

References

164

Further Reading

168

(UV-B and UV-A; ultraviolet, UV), ozone, sulfur dioxide, mechanical factors, and other less frequently occurring stressors (Pereira, 2016). Plants being rooted in the environment they grow in have to adapt with the changing conditions due to abiotic stresses and the accumulation of phenolics in plant tissues are considered as an adaptive response of plants to these adverse environmental conditions (Pereira, 2016; Lattanzio, 2013).

157

© 2019 Elsevier Inc. All rights reserved.

158

9. ROLE AND REGULATION OF PLANTS PHENOLICS IN ABIOTIC STRESS TOLERANCE: AN OVERVIEW

Plants synthesize an enormous number of chemicals categorized as primary and secondary metabolites. The primary metabolites, that is, sugars, fatty acids, amino, and nucleic acids being essential for plant growth and development are ubiquitously distributed in all plants (Fiehn, 2002; Wu and Chappell, 2008). Secondary metabolites being much more diverse than the primary metabolites structurally as well as chemically are the specialized compounds that are not directly essential for basic plant metabolism but are required by plants for survival in the environment. Plant phenolics or polyphenols are the most widely occurring groups of secondary metabolites with substantial physiological and morphological importance in plants. They are aromatic compounds with one or more hydroxyl groups and emerge from shikimate/ phenylpropanoid pathway or polyketide acetate/malonate pathway, producing monomeric and polymeric phenols and polyphenols (Randhir et al., 2004). Plant phenolics play an important role in plant growth, development, and reproduction, and a key role as defense compounds against abiotic stresses, such as high light, low temperatures, UV-B radiations, heavy metals and nutrient deficiency (Lattanzio, 2013), protection against pathogens and predators (Bravo, 1998), producing color and sensory characteristics of fruits and vegetables (Alasalvar et al., 2001), besides exhibiting other essential properties like antiallergenic, antimicrobial, and antioxidant activity (Balasundram et al., 2006). Plant phenolics or polyphenols are the most widely distributed secondary metabolites and predominate in the plant kingdom. Bacteria, fungi, and algae produce peculiar phenolic compounds whereas bryophytes are regular producers of polyphenols like flavonoids, but in the vascular plants a full range of phenolic compounds or polyphenols are found (Swain, 1975; Harborne, 1980). An estimation of about 2% of all the carbon photosynthesized by plants is converted into phenolic compounds (Robards and Antolovich, 1997). Several thousand phenolic compounds are known to be synthesized by higher plants and the characterization of these compounds is continuously increasing. Plant leaves contain esters; amides and glycosides of hydroxycinnamic acids (HCAs); glycosylated flavonoids, particularly flavonols; and proanthocyanidins and their derivatives. Lignin, suberin, and pollen sporopollenin are some other polyphenolic polymers. Some soluble phenolics like chlorogenic acid are widely distributed, whereas some are restricted to specific genera or families, thereby are handy biomarkers for taxonomic studies.

9.2 STRUCTURE AND CLASSIFICATION Structurally, phenolic compounds contain an aromatic ring with one or more hydroxyl substituents

attached to it, ranging from simple phenolic molecules to highly polymerized compounds, thereby showing great structural diversity, and are often referred to as polyphenols (Bravo, 1998). Most phenolic compounds naturally appear as conjugates with mono- and polysaccharides, coupled with one or more phenolic groups, and may also exist as functional derivatives like esters and methyl esters (Harborne, 1989; Harborne et al., 1999; Shahidi and Naczk, 1995). Phenolics though a very large and diverse group of chemical compounds can be classified in a number of ways. Harborne and Simmonds (1964) classified them into different groups based on the number of carbons in the molecule (Table 9.1).

9.3 BIOSYNTHESIS OF POLYPHENOLS Plant phenolics are biosynthesized in plants from a biosynthetic intermediate, phenylalanine and shikimic acid through the shikimic acid pathway (Fig. 9.1). The starting metabolites of the pathway are erythose-4phosphate and phosphoenolpyruvate (PEP), which are intermediates of pentose phosphate pathway (PPP) and glycolysis, respectively. The first step involves the conversion of glucose in the PPP to glucose-6-phosphate and then irreversibly to ribulose-5-phosphate by the aid of glucose-6-phosphate dehydrogenase (G6PDH). The PPP advances to produce erythrose-4-phosphate. Similarly from glycolysis, phosphoenolpyruvate is generated, which is then used together with erythrose-4-phosphate through the phenylpropanoid pathway to generate phenolic compounds after being channeled to the shikimic acid pathway to produce phenylalanine (Fig. 9.1).

9.4 PHENOLICS AND ABIOTIC STRESS TOLERANCE The great degree of interactions between plants and their changing environments has been a major driving force behind the emergence of specific natural products (Lattanzio, 2013). In this regard, the accumulation of phenolics in plant tissues is considered as an adaptive response of plants to adverse environmental conditions, thereby expanding evolutionary fitness. This accumulation resulted due to the activity of phenylalanine ammonia lyase (PAL), chalcone synthase (CHS), and other enzymes. Activity of PEPcarboxylase also increases, indicating a shift from sucrose production to the processes of defense and repair. Plant phenolics confer various physiological functions for survival and adaptation to environmental disturbances (Landolt et al., 1997; Andersen, 2003;

PLANT SIGNALING MOLECULES

TABLE 9.1 Classification of Phenolic Compounds Class

No. of C-atoms

Structure

Occurrence

Simple phenolics, benzoquinones

6

C6

Rare to common

Phenolic acids and related compounds

7

C6 C1

Common

Acethophenones, phenylacetic acids

8

C6 C2

Rare

HCAs, phenylpropanoids (coumarins, isocoumarins, chromones, chromenes)

9

C6 C3

Rare to common

Napthoquinones

10

C6 C4

Xanthones

13

C6 C1 C6

Rare

Stilbenes, anthraquinones

14

C6 C2 C6

Rare

Flavonoids, isoflavonoids

15

C6 C2 C6

Common

Betacyanins

18

Lignans, neolignans

18

(C6 C3)2

Biflavonoids

30

(C6 C3 C6)2

Rare

(C6 C3)n

Common

Lignin Melanins Condensed tannins (proanthocyanidins flavolans)

N

Rare

(C6)n (C6 C3 C6)n

FIGURE 9.1 The phenolic compound biosynthesis pathway. A schematic representation of the biosynthesis of phenolic compounds in the pentose phosphate, shikimate, and phenylpropanoid pathways in plants. Source: Redrawn from Lattanzio, V., 2013. Phenolic compounds: introduction. In: Ramawat, K.G., Merillon, J.M. (Eds.), Natural Products, Springer-Verlag: Berlin, Heidelberg. http://doi.org/10.1007/978-3-642-22144-6_57 and Lin et al. (2016).

160

9. ROLE AND REGULATION OF PLANTS PHENOLICS IN ABIOTIC STRESS TOLERANCE: AN OVERVIEW

Lattanzio et al., 2009). Plant phenolics are generally considered pivotal defense compounds when environmental stresses, such as high light or UV radiation, low temperatures, pathogen infection, herbivores, heavy metals, and nutrient deficiency, lead to increased production of free radicals and other oxidative species in plants. Plants respond to these biotic and abiotic stress factors by increasing their capacity to scavenge reactive oxygen species (ROS; Khan and Khan, 2017). The induction of secondary metabolism gene expression by the abovementioned environmental stresses is often mediated by integrating signaling molecules such as salicylic acid, jasmonic acid, and their derivatives (WinkelShirley, 2002; Gould and Lister, 2006; Nascimento and Fett-Neto, 2010; Khan and Khan, 2013; Khan et al., 2013, 2014, 2015; Per et al., 2018). Plants are exposed to various abiotic stresses during their life cycle. When a plant is subjected to abiotic stress, a number of genes are turned on or off, resulting in increasing levels of several metabolites and proteins, some of which may be responsible for conferring a certain degree of defense against these stresses (Ahmad et al., 2008; Jaleel et al., 2009; Tuteja et al., 2009). Abiotic stress promotes the production of damaging active oxygen species within the cells (Dar et al., 2017). Phenolics are varied secondary metabolites (flavonoids, tannins, hydroxycinnamate esters, and lignin) found abundantly in plant tissues and are actively involved in defense mechanisms against biotic and abiotic stress. As compared with nonstressed conditions, plants often produce a higher quantity of phenolic compounds under certain stress conditions (Selmar, 2008). Phenolic compounds performing as antioxidants terminate free radical chains and chelate redox-active metal ions that are capable of catalyzing lipid peroxidation (Schroeter et al., 2002). Phytophenolics, particularly polyphenols, function as antioxidants to support the primary ascorbatedependent detoxification system as a backup defense mechanism of vascular plants contrasting to monophenols (Yamasaki et al., 1995, 1999). Polyphenols are more effective antioxidants in vitro than ascorbate and tocopherols and have an ideal structural chemistry for free radical-scavenging activity. Antioxidative features of polyphenols arise from the ability of the polyphenol-derived radical to steady and delocalize the unpaired electron (chain-breaking function), their high reactivity as hydrogen or electron donors and from their capability to chelate transition metal ions (termination of the Fenton reaction) (Rice-Evans et al., 1997). Kagan and Tyurina (1997) reported that phenolics are univalently oxidized to their respective phenoxyl radicals when they function as antioxidants either by enzymatic or direct radical-scavenging

mechanisms. Plants synthesize phenolic compounds to survive in stress conditions (UV radiation, drought, salt, metal, and low temperature stress). Most plants constitutively synthesize phenylpropanoids including flavonoids and HCAs. However, accumulation of phenolics in plants can be induced by abiotic and biotic stresses, for example, UV radiation, high light illumination, low temperatures, wounding, low nutrients, and pathogen attack (Dixon and Paiva, 1995; Yamasaki et al., 1995). Certain secondary metabolic compounds are intensively synthesized under conditions of abiotic stress like drought where these act as antioxidants (Nascimento and Fett-Neto, 2010). Phenolic compounds accumulation in plant tissues is regarded as a distinctive plant stress characteristic. One among the largest three groups of secondary metabolites produced in plants, phenols have been alienated into five subgroups (coumarins, flavonoids, lignins, phenolic acids, and tannins) (Gumul et al., 2007), and are synthesized in plants via shikimic acid and chorismic acid pathways. Phenolic compounds have been regarded as metabolic alteration byproducts (Solecka, 1997). These not only serve a vital function of defense in plants but are also known to influence animals and humans that consume these phenol-enriched plant products (Franca et al., 2001; Amarowicz and Weidner, 2009). The expression of phenolic compounds has been, however, observed to be upregulated (Wro´bel et al., 2005; Weidner et al., 2009a) or downregulated (Weidner et al., 2007, 2009b) in response to diverse environmental stresses, thus leading to the increased or decreased content of the phenolic compounds. A number of studies have demonstrated the increased production of phenols in different plant tissues under abiotic stress conditions (Dixon and Paiva, 1995; Wro´bel et al., 2005; Weidner et al., 2009a). During water deficit and chilling stress conditions, Chung et al. (2006) have reported increased content of total phenolic compounds in Rehmannia glutinosa. Further confirmation has come from the studies of Posmyk et al. (2005) in soybean subjected to chilling stress. This accumulation is due to enhanced activities of enzymes, PAL, CHS, and other enzymes involved in their biosynthesis. Additionally, phosphoenolpyruvate (PEP)-carboxylase activity also increases, which suggests a shift from the production of sucrose to metabolic processes supporting defense and repair. Phenolics confer a variety of physiological functions to plants to survive and adapt to various environmental disturbances (Landolt et al., 1997; Andersen, 2003; Lattanzio et al., 2009). Phenolic acids are synthesized in response to abiotic stress through hydration, dehydration, and methylation of cinnamic acid (Dixon and Paiva, 1995). Many

PLANT SIGNALING MOLECULES

9.4 PHENOLICS AND ABIOTIC STRESS TOLERANCE

secondary metabolism products in plants that exhibit antioxidant properties belong to this class of compounds (Oszmanski, 1995). As antioxidants, these phenolic compounds scavenge ROS (Amarowicz et al., 2004, 2010; Caillet et al., 2006; Amarowicz and Weidner, 2009), catalyze oxygenation reactions by forming complexes with some metals, and hinder the activities of certain oxidizing enzymes (Elavarthi and Martin, 2010). As stated earlier, accumulation of phenols in plant tissues is a characteristic feature of several environmental stresses that divert considerable quantity of substrates from primary metabolism to the formation of secondary products leading to significant perturbations in the cellular homeostasis. Strong stimulation of mRNAs encoding G6PDH, a carbohydrate metabolism enzyme that provides shikimate pathway substrates, and 3-deoxyarabinoheptulosonate 7-phosphate synthase, which is a shikimate pathway enzyme required for phenylalanine biosynthesis has been observed in response to stress (Cheynier et al., 2013). Furthermore, accumulation of free proline in plants as a result of various biotic and abiotic stresses has been reported. Researchers have anticipated that a stress-stimulated enhancement in the shift of reducing equivalents into proline biosynthesis (cytosolic) as well as degradation (mitochondrial) cycle might be responsible for enabling sensitive regulation of redox potential in the cytosol (Logemann et al., 2000; Lattanzio et al., 2009; Verslues and Sharma, 2010). The abovementioned points imply that different environmental perturbations selectively induce the primary as well as secondary metabolic activities, which are directly and indirectly involved in the accretion of phenolic compounds (Cheynier et al., 2013; Lattanzio et al., 2009). A likely series of biochemical reactions occurring inside the cell, which convey a signal from the outside cell environment into the inside of the plant cell, leading to an effective physiological response, may thus be envisaged (Fig. 9.2) (Hare and Cress, 1997; Lattanzio et al., 2009). This signaling pathway proposes a connection between primary and secondary metabolism, which couples the accretion of proline (a stress metabolite) with the energy transfer toward the biosynthesis of phenylpropanoid through the oxidative PPP (Cheynier et al., 2013). Under various stress conditions, the plant undergoes forceful accumulation of ample amounts of free proline. It can be synthesized de novo or can be released by the protein degradation and is accompanied by NADPH oxidation. Enhanced NADP1/NADPH ratio leads to increased activity of the oxidative PPP, which in turn provides precursors for biosynthesis of phenolic compounds via the shikimic acid pathway (Cheynier et al., 2013; Lattanzio et al., 2009).

161

FIGURE 9.2 Showing the abiotic stress-mediated phenol biosynthesis in plants. Source: Redrawn from Cheynier et al. (2013); Lattanzio V., Cardinali, A., Ruta, C., Morone Fortunato, I., Lattanzio, V.M.T., Linsalata, V., et al., 2009. Relationship of secondary metabolism to growth in oregano (Origanum vulgare L.) shoot cultures under nutritional stress. Environ. Exp. Bot. 65, 54 62.

9.4.1 Phenolics as Ultraviolet Sunscreens Light is a well-known physical factor that can affect the synthesis of metabolites in plants. Exposure of ambient solar UV-B radiation (280 320 nm) to plants in open fields adversely affects DNA, proteins, and membranes and alters metabolism through the generation of ROS. Plants synthesize phenolic compounds, which act as a screen inside the epidermal cell layer to defend themselves from this damaging radiation and by adjusting the antioxidant systems at both the cell and whole organism level thereby intercepting mutagenesis and cell death by dimerization of thymine units in the DNA, and possible photo destruction of coenzymes NAD or NADP (Daayf and Lattanzio, 2008). Flavonoids with their high absorptivity at 250 270 and 335 360 nm act as good UV screens (Lattanzio, 2013; Winkel-Shirley, 2002; Carletti et al., 2003). Flavonoids and other phenolic compounds play a significant role in UV protection (Li et al., 1993). Increased flavonoid synthesis was observed in plants radiated with UV light, which confirms the ability of flavonoids to absorb radiation of high energy with the maximum absorption at 250 270 and 335 360 nm (Michalak, 2006; Falcone Ferreyra et al., 2012; Winkel-Shirley, 2002; Liang et al., 2006). It is an observed fact that tropical and high-altitude plants have a higher percentage of flavonoids than temperate plants. The change in the

PLANT SIGNALING MOLECULES

162

9. ROLE AND REGULATION OF PLANTS PHENOLICS IN ABIOTIC STRESS TOLERANCE: AN OVERVIEW

proportion of flavonoids composition of plant leaves is due to excess of light or UV radiation largely due the activation of flavonoid biosynthetic genes (Kolb et al., 2001). Several studies have confirmed that the excess of light or UV radiation changes the flavonoid composition of plant leaves (Olsson et al., 1998; Kolb et al., 2001). Plant defense mechanisms of polyphenols against UV radiation as direct shields has been regarded as a key biological function by several authors (Rozema et al., 2002; Burchard et al., 2000). Larcher (1995) revealed that phenolics, particularly anthocyanin, which accumulate in the epidermis can act as a darkening filter and protect the mesophyll from extreme radiation. Flavonoids (especially kaempferol derivatives), phenolic acid esters, or isoflavonoids and psoralens accumulate during stress and prevent UV-B from reaching the mesophyll (Stapleton, 1992). Flavones and flavonols, the two important groups of flavonoids found in flowers, accumulate in epidermal layers of leaves and stems and absorb light strongly in the UV-B region without interrupting visible (PAR) wavelengths, thus function to shield cells from UV-B radiation (Lake et al., 2009). Ryan et al. (2001) proved that flavonoids are essential in UV protection using mutants of Arabidopsis, UV-hypersensitive phenotypes that have a block in flavonoid production. Anthocyanin synthesis was stimulated by UV light from 280 to 320 nm synergistically when combined with red light in apples (Arakawa et al., 1985). Liu et al. (1995) revealed that flavonoid improved in barley and Kramer et al. (1991) also found increased content of polyamines in cucumber by UV-B radiation. Flavonols concentration also improved in Norway spruce (Picea abies) on UV-B exposure (Fischbach et al., 1999). Along similar lines, the increased production of the important anticancerous phenolic compounds, that is, vinblastine and vincristine, due to UV-B exposure in Catharanthus roseus has been reported by Bernard et al. (2009). Shiozaki et al. (1999) also revealed that flavonoids in the roots of pea plants was enhanced on UV (300 400 nm) exposure. Flavonols production was stimulated by UV-B in silver birch and grape leaves (Tegelberg et al., 2004). Moreover, photosynthetic pigments, condensed tannins were accumulated under six different daily doses of UV radiation (UV-A and UV-B), whereas its precursor, (1)-catechin, significantly decreased (Lavola et al., 2003). In a UV-tolerant rice cultivar, C-glycosylflavone contents increasingly appeared but were not found in a susceptible cultivar when exposed to different UV-B light levels (Markham et al., 1998). Furthermore, in several plant species, enhanced flavonoid levels have been measured at higher altitudes (Bachereau et al., 1998; Zidorn et al., 2005; Rieger et al., 2008; Spitaler et al.,

2008; Murai et al., 2009). It has been proven in several plant species that the expression of CHS is transcriptionally activated by UV light, which is the first enzyme in the flavonoid biosynthesis pathway (Koes et al., 1989; Schulze-Lefert et al., 1989).

9.4.2 Plant Phenolics and Their Role in Heavy Metal Stress Heavy metal toxicity is one of the important abiotic stresses that alter physiological and metabolic processes, thus leading to harmful effects in plants (Villiers et al., 2011). It has been reported that certain flavonoids exhibit the ability to provide heavy metal stress protection by transition metals chelation (e.g., Fe, Cu, Ni, Zn), which generates hydroxyl radical via Fenton’s reaction (Mira et al., 2002;Williams et al., 2004). Kidd et al. (2001) revealed that the chelation of these metals in the soil may be an effective form of defense against the effects of high metals concentration toxicity. Michalak (2006) observed that the biosynthesis of phenolic compounds that are precursors of lignin intensifies under stress conditions, for example, in plants subjected to heavy metal stress. Research on corn plants (Zea mays L.) confirmed this further when grown on soil contaminated with aluminum ions and root exudates were found with high levels of catechin and quercetin. Winkel-Shirley (2001) reported that flavonoids are involved in plants’ defense, growing in soils that are rich in toxic metals such as aluminum. The production of betalains in Beta vulgaris is stimulated by Cu21 (Trejo-Tapia et al., 2001). The hairy roots were exposed to metal ions to improve betalaines production (Thimmaraju and Ravishankar, 2004). Red cabbage seedlings accumulated phenolic compounds, total antioxidant capacity, and increased PAL activity when treated with copper (Posmyk et al., 2009). Accumulation of betacyanins in callus cultures of Amaranthus caudatus is stimulated by Cu21 (Obrenovic, 1990). Flavonoids accumulation was also observed in cell cultures of Ginkgo biloba treated with CuSO4 as compared with untreated cells (Kim et al., 1999). Similarly, association between concentration of CuSO4 and flavonoid level in cell cultures of Digitalis lanata was reported (Bota and Deliu, 2011). Nickel stress leads to significant decrease in anthocyanin levels as observed by Hawrylak et al. (2007). Michalak (2006) observed that plants with high content of tannins, such as tea, are able to tolerate high concentrations of manganese in a soil, as they are protected by the direct chelation of these ions. Lavid et al. (2001) reported the heavy metal ions binding with polyphenols in Nympheae where heavy metals (Hg, Pb, Cr) were chelating by the polyphenols rich methanol extract.

PLANT SIGNALING MOLECULES

9.4 PHENOLICS AND ABIOTIC STRESS TOLERANCE

9.4.3 Plant Phenolics and Their Role in Drought Stress Drought is the major abiotic stress that affects plant growth and development and causes losses in agricultural production. As has been reported by several studies, phenolics content increased in plants under water scarcity. Flavonoid accumulation is important to improve drought tolerance in wild-type and Arabidopsis thaliana mutants revealed by transcriptomic and metabolomic approaches (Nakabayashi et al., 2014). Ballizany et al. (2012) revealed that the quercetin (a flavonol) contents enhanced significantly in white clover under drought conditions, which was higher in the more drought-resistant genotypes. Kirakosyan et al. (2003) reported that under drought conditions, flavonols have been increased in other species also, such as Crataegus laevigata and Crataegus monogyna. Similarly, in Cistus clusii plants upon controlled drought treatments, and in plants collected from the field in summer, characterized by high temperatures and prolonged lack of rain in the Mediterranean climate, an increase in flavanol levels has been reported (Hernandez et al., 2004). Akula and Ravishankar (2011) reported that the defense mechanism against drought stress is triggered by bioactivity of leaf phenolic molecules. Phenolic acids and flavonoids as antioxidant accumulation and sunshields are involved in plants’ response to drought stress (Nichols et al., 2015). Larson (1988) also reported the increased level of flavonoids and phenolic acids in willow leaves under drought conditions causes oxidative stress. In droughtresistant tomato cultivars kaempferol and quercetin (flavonoids) were enhanced while reduced in drought sensitive cultivars reported by Sa´nchez-Rodrı´guez et al. (2011). In red-hulled and black-hulled rice the radical-scavenging ability depended on the concentrations of proanthocyanidins and anthocyanins, respectively (Oki et al., 2002). Flavonoids and phenolic acids were synthesized in a large amount in wheat leaves and cell-damaging oxidants also generated under drought stress (Ma et al., 2014). Chalker-Scott (1999) reported that plant tissues containing anthocyanins are usually rather resistant to drought. For example, a purple cultivar of chili resists water stress better than a green cultivar revealed by Bahler et al. (1991). In Chenopodium quinoa saponins content decreased from 0.46% to 0.38% dry weight (dw) in plants growing under low water deficit and in high water deficit conditions, respectively (Soliz-Guerrero et al., 2002). Phenolic compounds concentration was 10% improved in Hypericum brasiliense grown under drought stress as compared with control plants (De Abreu and Mazzafera, 2005). Similarly, phenolic compound were also increased in pea plants (Pisum sativum) when

163

grown under drought conditions (Nogue’s et al., 1998). In both leaves and flowers of Tridax procumbens significant increases of total phenolic content were observed under drought stress (Gnanasekaran and Kalavathy, 2017). Antioxidant capacity of phenolic acids was reflected by change in their contents during the process of finger millet malting (Subba Rao and Muralikrishna, 2002). Nichols et al. (2015) reported that the high levels of flavonols, quercetin, and kaempferol contents were related with improved stress tolerance capacity of white clover under drought conditions.

9.4.4 Plant Phenolics and Their Role in Cold Stress It has been observed that nonfreezing low temperatures enhance phenolic metabolism in plants (Akula and Ravishankar, 2011). Phenolic metabolism is stimulated at a critical low temperature, which is the threshold temperature at which chilling injury is also induced (Janska et al., 2010). This low temperature results in cold-induced stimulation of the PAL activity (EC 4.3.1.5) as well as other enzymes necessary for phenolic biosynthesis, leading to increased phenolic production and modified plant development either independently or by interaction with known plant growth promoters, especially ethylene (Lattanzio et al., 1994, 2001). Cold stress increases phenolic production into the cell wall either as suberin or lignin (Griffith and Yaish, 2004). Lignification and suberin deposition increase resistance to cold stress. These cell wall thickenings protect the plant from freezing stress. An increase in cell wall thickening could reduce cell collapse during freezing-induced dehydration and mechanical stress, thus providing freezing resistance of the plant (Chalker-Scott and Fuchigami, 1989). Apple trees are found to be associated with high levels of chlorogenic acid as an adaptive measure to cold climate (Perez-Ilzarbe et al., 1997). Christie et al. (1994) reported the anthocyanins accumulation during cold stress and Pedranzani et al. (2003) reported that cold and water stresses initiated changes in endogenous jasmonates in Pinus.

9.4.5 Plant Phenolics and Their Role in Nutrient Stress Plant growth depends on the supply of recycled nutrients. External nutrient supply and nutrient mineralization by soil microorganisms contribute the nutrient requirements. The factors regulating nutrient cycle include climate, substrate (litter) quality, and decomposer organisms. Polyphenols influence the supply

PLANT SIGNALING MOLECULES

164

9. ROLE AND REGULATION OF PLANTS PHENOLICS IN ABIOTIC STRESS TOLERANCE: AN OVERVIEW

and flow of inorganic and organic soil nutrients available for plants and/or microbes. Phenolic compounds find their way to the soil as leachates from the aboveas well as below-ground parts of plants and/or within above and belowground plant litter (Ha¨ttenschwiler and Vitousek, 2000). Polyphenols affect the composition and activity of decomposers thus influencing the rates of decomposition and nutrient cycling (Lattanzio et al., 2006). Phenolic compounds show a sensitive response to nutrient deficiency, thus providing a method for diagnosing nutrient disorders prior to the appearance of visible symptoms. Deficiencies of N, P, K, and S usually result in increased concentrations of phenolic compounds, and abundant N generally inhibits phenolic accumulation (Gershenzon, 1913; McClue, 1977). Visual symptoms of N or P deficiency are red or purple tints of the leaves due to accumulation of anthocyanins (Hewitt, 1963). Nutrient stress increased threefold anthocyanidins level and doubled quercetin-3-Oglucoside in tomato (Bongue-Bartelsman Phillips, 1995). Osmotic stress by sucrose and other agents regulate anthocyanin production in Vitis vinifera cultures (Tuteja and Mahajan, 2007).

9.5 CONCLUSION AND FUTURE PROSPECTS Plant phenolics are the most common and widespread secondary metabolites, comprising a large reservoir of natural chemical diversity with a huge range of compounds and enzymes and a wide spectrum of mechanisms of gene regulation, and transport of metabolites and enzymes. Plants accumulate phenolic compounds in their tissues as an adaptive response to adverse environmental stresses including wounding, pathogen attack, mineral deficiencies, and temperature stress. Polyphenols modify the developmental status of the plant independently or by interacting with plant growth promoters like ethylene. Furthermore, these compounds, the precursors for lignin and suberin, are polymerized into the cell wall. These cell wall thickenings protect the plant from freezing stress. An increase in cell wall thickening could reduce cell collapse during freezing-induced dehydration and mechanical stress, thus providing freezing resistance of the plant (Chalker-Scott and Fuchigami, 1989). Polyphenols influence the supply and flow of inorganic and organic soil nutrients available for plants and/or microbes. They also show a sensitive response to nutrient deficiency, thus providing a method for diagnosing nutrient disorders prior to the appearance of visible symptoms.

Despite a handful of studies on biosynthesis of phenolic compounds and their accumulation as an adaptive response against abiotic stresses, studies on the proper mechanism of their accumulation and their interactions with other cell metabolites are desperately needed to develop a complete understanding of their increased expression and imparting tolerance under such circumstances.

References Ahmad, P., Sarwat, M., Sharma, S., 2008. Reactive oxygen species, antioxidants and signaling in plants. J. Plant Biol. 51 (3), 167 173. Akula, R., Ravishankar, G.A., 2011. Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal. Behav. 6, 1720 1731. Alasalvar, C., Grigor, J.M., Zhang, D., Quantick, P.C., Shahidi, F., 2001. Comparison of volatiles, phenolics, sugars, antioxidant vitamins, and sensory quality of different colored carrot varieties. J. Agric. Food Chem. 49, 1410 1416. Amarowicz, R., Weidner, S., 2009. Biological activity of grapevine phenolic compounds. In: Roubelakis-Angelakis, K.A. (Ed.), Grapevine Molecular Physiology and Biotechnology, second ed Springer, New York, pp. 389 405. Amarowicz, R., Pegg, R.B., Rahimi-Moghaddam, P., Barl, B., Weil, J.A., 2004. Free-radical scavenging capacity and antioxidant activity of selected plant species from the Canadian prairies. Food Chem. 84, 551 562. Amarowicz, R., Weidner, S., Wojtowicz, I., Karmac, M., Kosinska, A., Rybarczyk, A., 2010. Influence of low-temperature stress on changes in the composition of grapevine leaf phenolic compounds and their antioxidant properties. Funct. Plant Sci. Biotechnol. 4, 90 96. Andersen, C., 2003. Source-sink balance and carbon allocation below ground in plants exposed to ozone. New Phytol. 157, 213 228. Arakawa, O., Hori, Y., Ogata, R., 1985. Relative effectiveness and interaction of ultraviolet-B, red and blue light in anthocyanin synthesis of apple fruit. Physiol. Plant. 64, 323 327. Bachereau, F., Marigo, G., Asta, J., 1998. Effect of solar radiation (UV and visible) at high altitude on CAM-cycling and phenolic compounds biosynthesis in Sedum album. Physiol. Plant. 104, 203 210. Bahler, B.D., Steffen, K.L., Orzolek, M.D., 1991. Morphological and biochemical comparison of a purple-leafed and a green-leafed pepper cultivar. HortScience. 26, 736. Balasundram, N., Sundram, K., Samman, S., 2006. Phenolic compounds in plants and agri-industrial by-products: antioxidant activity, occurrence, and potential uses. Food Chem. 99, 191 203. Ballizany, W.L., Hofmann, R.V., Jahufer, M.Z.Z., Barrett, B.B., 2012. Multivariate associations of flavonoid and biomass accumulation in white clover (Trifolium repens) under drought. Funct. Plant Biol. 39, 167 177. Bernard, Y.K., Binder Christie, A.M., Peebles Jacqueline, V., Shanks, K.-Y.S., 2009. The effects of UV-B stress on the production of terpenoid indole alkaloids in Catharanthus roseus hairy roots. Biotechnol. Prog. 25, 8615. Bongue-Bartelsman, M., Phillips, D.A., 1995. Nitrogen stress regulates gene expression of enzymes in the flavonoids biosynthetic pathway of tomato. Plant Physiol. Biochem. 33, 539 546. Bota, C., Deliu, C., 2011. The effect of copper sulphate on the production of flavonoids in Digitalis lanata cell cultures. Farmacia 59, 113 118. Bravo, L., 1998. Polyphenols: chemistry, dietary sources, metabolism, and nutritional significance. Nutr. Rev. 56, 317 333.

PLANT SIGNALING MOLECULES

REFERENCES

Burchard, P., Bilger, W., Weissenbock, G., 2000. Contribution of hydroxycinnamates and flavonoids to epidermal shielding of UVA and UV-B radiation in developing rye primary leaves as assessed by ultraviolet-induced chlorophyll fluorescence measurements. Plant Cell Environ. 23, 1373 1380. Caillet, S., Salmieri, S., Lacriox, M., 2006. Evaluation of free radicalscavenging properties of commercial grape phenol extracts by a fast colorimetric method. Food Chem. 95, 1 8. Carletti, P., Masi, A., Wonisch, A., Grill, D., Tausz, M., Ferretti, M., 2003. Changes in antioxidant and pigment pool dimensions in UV-B irradiated maize seedlings. Environ. Exp. Bot. 50, 149 157. Chalker-Scott, L., 1999. Environmental significance of anthocyanins in plant stress responses. Photochem. Photobiol. 70, 1 9. Chalker-Scott, L., Fuchigami, 1989. The role of phenolic compounds in plant stress responses. In: Li, P.H. (Ed.), Low Temperature Stress Physiology in Crops. CRC Press, Boca Raton, FL, pp. 67 76. Cheynier, V., Comte, G., Davies, K.M., Lattanzio, V., Martens, S., 2013. Plant phenolics: recent advances on their biosynthesis, genetics, and ecophysiology. Plant Physiol. Biochem. 72, 1 20. Christie, P.J., Alfenito, M.R., Walbot, V., 1994. Impact of low temperature stress on general phenylpropanoid and anthocyanin pathways: enhancement of transcript abundance and anthocyanin pigmentation in maize seedlings. Planta 194, 541 549. Chung, I.M., Kim, J.J., Lim, J.D., Yu, C.Y., Kim, S.H., Hahn, S.J., 2006. Comparison of resveratrol, SOD activity, phenolic compounds and free amino acid in Rehmannia glutinose under temperature and water stress. Environ. Exp. Bot. 56, 44 53. Daayf, F., Lattanzio, V. (Eds.), 2009. Recent advances in polyphenol research. John Wiley & Sons, West Sussex, UK. Dar, M.I., Naikoo, M.I., Khan, F.A., Rehman, F., Green, I.D., Naushin, F., et al., 2017. An introduction to reactive oxygen species metabolism under changing climate in plants. In: Khan, M.I. R., Khan, N.A. (Eds.), Reactive Oxygen Species and Antioxidant Systems in Plants: Role and Regulation under Abiotic Stress. Springer, Berlin, Germany, pp. 25 52. De Abreu, I.N., Mazzafera, P., 2005. Effect of water and temperature stress on the content of active constituents of Hypericum brasiliense Choisy. Plant Physiol. Biochem. 43 (3), 241 248. Dixon, R.A., Paiva, N., 1995. Stress-induced phenylpropanoid metabolism. Plant Cell. 7, 1085 1097. Elavarthi, S., Martin, B., 2010. Spectrophotometric assays for antioxidant enzymes in plants. Methods Mol. Biol. 639, 273 281. Falcone Ferreyra, M.L., Rius, S.P., Casati, P., 2012. Flavonoids: biosynthesis, biological functions, and biotechnological applications. Front Plant. Available from: https://doi.org/10.3389/ fpls.2012.00222. Fiehn, O., 2002. Metabolomics the link between genotypes and phenotypes. Plant Mol. Biol. 48, 155 171. Fischbach, R.J., Kossmann, B., Panten, H., Steinbrecher, R., Heller, W., Seidlitz, H.K., 1999. Seasonal accumulation of ultraviolet-B screening pigments in needles of Norway spruce (Picea abies (L.) Karst). Plant Cell Environ. 22, 27 37. Franca, S.C., Roberto, P.G., Marins, M.A., Puga, R.D., Rodrigeuz, A., Pereira, J.O., 2001. Biosynthesis of secondary metabolites in sugarcane. Gen. Mol. Biol. 24, 243 250. Gershenzon, J., 1913. Changes in levels of plant secondary metabolites under water and nutrient stress. Recent Adv. Phytochem. 18, 273 320. Gnanasekaran, N., Kalavathy, S., 2017. Drought stress signal promote the synthesis of more reduced phenolic compounds (chloroform insoluble fraction) in Tridax procumbens. Free Rad. Antioxid. 7 (1), 128 136. Gould, K.S., Lister, C., 2006. Flavonoid functions in plants. In: Andersen, Ø.M., Markham, K.R. (Eds.), Flavonoids Chemistry, Biochemistry and Applications. CRC Taylor & Francis, Boca Raton, FL, pp. 397 411.

165

Griffith, M., Yaish, M.W.F., 2004. Antifreeze proteins in overwintering plants: a tale of two activities. Trends Plant Sci. 9, 399 405. Available from: https://doi.org/10.1016/j.tplants.2004.06.007. PMID:15358271. Gumul, D., Korus, J., Achremowicz, B., 2007. The influence of extrusion on the content of polyphenols and antioxidant/antiradical activity of rye grains (Secale cereal L.). Acta Sci. Pol. 6, 103 111. Harborne, J.B., 1980. Plant phenolics. In: Bell, E.A., Charlwood, B.V. (Eds.), Encyclopedia of Plant Physiology, vol. 8, Secondary Plant Products. Springer, Berlin, pp. 329 402. Harborne, J.B., 1989. General procedures and measurement of total phenolics. In: Harborne, J.B. (Ed.), Methods in Plant Biochemistry: Volume 1 Plant Phenolics. Academic Press, London, pp. 1 28. Harborne, J.B., Simmonds, N.W., 1964. Natural distribution of the phenolic aglycones. In: Harborne, J.B. (Ed.), Biochemistry of Phenolic Compounds. Academic Press, London, pp. 77 128. Harborne, J.B., Baxter, H., Moss, G.P. (Eds.), 1999. Phytochemical Dictionary: Handbook of Bioactive Compounds from Plants. second ed Taylor & Francis, London. Hare, P.D., Cress, W.A., 1997. Metabolic implications of stressinduced proline accumulation in plants. Plant Growth Regul. 21, 79 102. Hawrylak, B., Matraszek, R., Szymanska, M., 2007. Response of lettuce (Lactuca sativa L.) to selenium in nutrient solution contaminated with nickel. Veg. Crop Res. Bull. 67, 63 70. Hernandez, I., Alegre, L., Munne-Bosch, S., 2004. Drought-induced changes in flavonoids and other low molecular weight antioxidants in Cistus clusii grown under Mediterranean field conditions. Tree Physiol. 24, 1303 1311. Hewitt, E.J., 1963. The essential nutrients: requirements and interactions in plants. In: Steward, F.C. (Ed.), Plant Physiology. Academic Press, New York & London, pp. 137 360. Ha¨ttenschwiler, S., Vitousek, P.M., 2000. The role of polyphenols in terrestrial ecosystem nutrient cycling. Trends Ecol. Evol. 15, 238 243. Jaleel, C.A., Gopi, R., Manivannan, P., Gomathinayagam, M., Riadh, K., Ine`s, J., et al., 2009. Antioxidant defense responses: physiological plasticity in higher plants under abiotic constraints. Acta Physiol. Plant 31 (3), 427 436. Janska, A., Marsik, P., Zelenkova, S., Ovesna, J., 2010. Cold stress and acclimation—what is important for metabolic adjustment? Plant Biol. 12, 395 405. Kagan, V.E., Tyurina, Y.Y., 1997. Recycling and redox cycling of phenolic antioxidants. Ann. N.Y. Acad. Sci. 854, 425 434. Khan, M.I.R., Khan, N., 2017. Reactive Oxygen Species and Antioxidant System in Plants: Role and Regulation Under Abiotic Stress. Springer Nature, Singapore978-981-10-5254-5. Khan, M.I.R., Khan, N.A., 2013. Salicylic acid and jasmonates: approaches in abiotic stress tolerance. Plant Biochem. Physiol. 1, 4. Khan, M.I.R., Iqbal, N., Masood, A., Per, T.S., Khan, N.A., 2013. Salicylic acid alleviates adverse effects of heat stress on photosynthesis through changes in proline production and ethylene formation. Plant Signal. Behav. 8, e26374. Khan, M.I.R., Asgher, M., Khan, N.A., 2014. Alleviation of saltinduced photosynthesis and growth inhibition by salicylic acid involves glycinebetaine and ethylene in mungbean (Vigna radiata L.). Plant Physiol. Biochem. 80, 67 74. Khan, M.I.R., Fatma, M., Per, T.S., Anjum, N.A., Khan, N.A., 2015. Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Front. Plant Sci. 6, 462. Kidd, P.S., Llugany, M., Poschenrieder, C., Gunse´, B., Barcelo´, J., 2001. The role of root exudates in aluminium resistance and silicon-induced amelioration of aluminium toxicity in three varieties of maize (Zea mays L.). J. Exp. Bot. 52, 1339 1352.

PLANT SIGNALING MOLECULES

166

9. ROLE AND REGULATION OF PLANTS PHENOLICS IN ABIOTIC STRESS TOLERANCE: AN OVERVIEW

Kim, M.S., Kim, C., Jo, D.H., Ryu, Y.W., 1999. Effect of fungal elicitor and heavy metals on the production of flavonol glycosides in cell cultures of Ginkgo biloba. J. Microbiol. Biotechnol. 9, 661 667. Kirakosyan, A., Seymour, E., Kaufman, P.B., Warber, S., Bolling, S., Chang, S.C., 2003. Antioxidant capacity of polyphenolic extracts from leaves of Crataegus laevigata and Crataegus monogyna (Hawthorn) subjected to drought and cold stress. J. Agric. Food Chem. 51, 3973 3976. Koes, R.E., Spelt, C.E., Mol, J.N.M., 1989. The chalcone synthase multigene family of Petunia hybrida (V30): differential, light regulated expression during flower development and UV light induction. Plant Mol. Biol. 12, 213 225. Kolb, C.A., Ka¨ser, M.A., Kopecky´, J., Zotz, G., Riederer, M., Pfu¨ndel, E.E., 2001. Effects of natural intensities of visible and ultraviolet radiation on epidermal ultraviolet screening and photosynthesis in grape leaves. Plant Physiol. 127, 863 875. Kramer, G.F., Norman, H.A., Krizek, D.T., Mirecki, R.M., 1991. Influence of UV-B radiation on polyamines, lipid peroxidation and membrane lipids in cucumber. Phytochemistry 30, 2101 2108. Lake, J.A., Field, K.J., Davey, M.P., Beerling, D.J., Lomax, B.H., 2009. Metabolomic and physiological responses reveal multi-phasic acclimation of Arabidopsis thaliana to chronic UV radiation. Plant Cell Environ. 32 (10), 1377 1389. Landolt, W., Gunthardt-Georg, M.S., Pfenninger, I., Einig, W., Hampp, R., Maurer, S., et al., 1997. Effect of fertilization on ozone-induced changes in the metabolism of birch (Betula pendula) leaves. New Phytol. 137, 389 397. Larcher, W., 1995. Physiological Plant Ecology. Springer, Berlin, Heidelberg. Larson, R.A., 1988. The antioxidants of higher plants. Phytochemistry 27, 969 978. Lattanzio, V., 2013. Phenolic compounds: introduction. In: Ramawat, K.G., Merillon, J.M. (Eds.), Natural Products. Springer-Verlag, Berlin, Heidelberg. Available from: http://doi.org/10.1007/9783-642-22144-6_57. Lattanzio, V., Cardinali, A., Di Venere, D., Linsalata, V., Palmieri, S., 1994. Browning phenomena in stored artichoke (Cynara scolymus L.) heads: enzymic or chemical reactions? Food Chem. 50, 1 7. Lattanzio, V., Di Venere, D., Linsalata, V., Bertolini, P., Ippolito, A., Salerno, M., 2001. Low temperature metabolism of apple phenolics and quiescence of Phlyctaena vagabonda. J. Agric. Food Chem. 49, 5817 5821. Lattanzio, V., Lattanzio, V.M.T., Cardinali, A., 2006. Role of phenolics in the resistance mechanisms of plants against fungal pathogens and insects. In: Imperato, F. (Ed.), Phytochemistry: Advances in Research. Research Signpost, Trivandrum, pp. 23 67. Lattanzio, V., Cardinali, A., Ruta, C., Morone Fortunato, I., Lattanzio, V.M.T., Linsalata, V., et al., 2009. Relationship of secondary metabolism to growth in oregano (Origanum vulgare L.) shoot cultures under nutritional stress. Environ. Exp. Bot. 65, 54 62. Lavid, N., Schwartz, A., Yarden, O., Tel-Or, E., 2001. The involvement of polyphenols and peroxidase activities in heavy metal accumulation by epidermal glands of waterlily (Nymphaeceaea). Planta. 212, 323 331. Lavola, A., Aphalo, P.J., Lahti, M., Julkunen-Tiitto, R., 2003. Nutrient availability and the effect of increasing UV-B radiation on secondary plant compounds in Scots pine. Environ. Exp. Bot. 49, 49 60. Li, J., Ou-Lee, T.M., Raba, R., Amundson, R.G., Last, R.L., 1993. Arabidopsis flavonoid mutants are hypersensitive to UV-B irradiation. Plant Cell 5, 171 179. Lin, D., Xiao, M., Zhao, J., Li, Z., Xing, B., Li, X., et al., 2016. An overview of plant phenolic compounds and their importance in human nutrition and management of type 2 diabetes. Molecules 21, 1374.

Liang, B., Huang, X., Zhang, G., Zhang, F., Zhou, Q., 2006. Effect of lanthanum on plants under supplementary ultraviolet-B radiation: effect of lanthanum on flavonoid contents in Soybean seedlings exposed to supplementary ultraviolet-B radiation. J. Rare Earths. 24, 613 616. Liu, L., Gitz III, D.C., McClure, J.,W., 1995. Effects of UV-B on flavonoids, ferulic acid, growth and photosynthesis in barley primary leaves. Physiol. Plant. 93, 734 738. Logemann, E., Tavernaro, A., Schulz, W., Somssich, I.E., Hahlbrock, K., 2000. UV light selectively coinduces supply pathways from primary metabolism and flavonoid secondary product formation in parsley. Proc. Natl. Acad. Sci. USA 97, 1903 1907. Ma, D., Sun, D., Wang, C., Li, Y., Guo, T., 2014. Expression of flavonoid biosynthesis genes and accumulation of flavonoid in wheat leaves in response to drought stress. Plant Physiol. Biochem. 80, 60 66. Markham, K.R., Tanner, G.J., Caasi-Lit, M., Whitecross, M.I., Nayudu, M., Mitchell, K.A., 1998. Possible protective role for 31, 41-dihydroxyflavones induced by enhanced UV-B in a UVtolerant rice cultivar. Phytochemistry 49, 1913 1919. McClue, J.W., 1977. The physiology of phenolic compounds in plants. Recent Adv. Phytochem. 12, 525 556. Michalak, A., 2006. Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Pol. J. Environ. Stud. 15, 523 530. Mira, L., Fernandez, M.T., Santos, M., Rocha, R., Floreˆncio, M.H., Jennings, K.R., 2002. Interactions of flavonoids with iron and copper ions: a mechanism for their antioxidant activity. Free Radic. Res. 36, 1199 1208. Murai, Y., Takemura, S., Takeda, K., Kitajima, K., Iwashina, T., 2009. Altitudinal variation of UV-absorbing compounds in Plantago asiatica. Biochem. Syst. Ecol. 37, 378 384. Nakabayashi, R., Yonekura-Sakakibara, K., Urano, K., Suzuki, M., Yamada, Y., Nishizawa, T., et al., 2014. Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. Plant J. 77, 367 379. Nascimento, N.C., Fett-Neto, A.G., 2010. Plant secondary metabolism and challenges in modifying its operation: an overview. In: FettNeto, A.G. (Ed.), Plant Secondary Metabolism Engineering Methods and Application, Methods in Molecular Biology, vol. 643. Humana Press, New York, pp. 1 13. Nichols, S.N., Hofmann, R.W., Williams, W.M., 2015. Physiological drought resistance and accumulation of leaf phenolics in white clover interspecific hybrids. Environ. Exp. Bot. 119, 40 47. Nogue’s, S., Allen, D.J., Morison, J.I.L., Baker, N.R., 1998. UltravioletB radiation effects on water relations, leaf development, and photosynthesis in droughted pea plants. Plant Physiol. 117 (1), 173 181. Obrenovic, S., 1990. Effect of Cu (11) D-penicillanine on phytochrome mediated betacyanin formation in Amaranthus caudatus seedlings. Plant Physiol. Biochem. 28, 639 646. Oki, T., Masuda, M., Kobayashi, M., Nishiba, Y., Furuta, S., Suda, L., et al., 2002. Polymeric procyanidins as radical-scavenging components in red-hulled rice. J. Agric. Food Chem. 50, 7524 7529. Olsson, L.C., Veit, M., Weissenbo¨ck, G., Bornman, J.F., 1998. Differential flavonoid response to enhanced UV-B radiation in Brassica napus. Phytochemistry 49, 1021 1028. Oszmanski, J., 1995. Polyphenols as antioxidants in food. Przem Spo_z 3, 94 96. in Polish. Pedranzani, H., Sierra-de-Grado, R., Vigliocco, A., Miersch, O., Abdala, G., 2003. Cold and water stresses produce changes in endogenous jasmonates in two populations of Pinus pinaster Ait. Plant Growth Regul. 52, 111 116.

PLANT SIGNALING MOLECULES

REFERENCES

Per, T.S., Khan, M.I.R., Anjum, N.A., Masood, A., Hussain, S.J., Khan, N.A., 2018. Jasmonates in plants under abiotic stresses: crosstalk with other phytohormones matters. Environ. Exp. Bot. 145, 104 120. Pereira, A., 2016. Plant abiotic stress challenges from the changing environment. Front. Plant Sci. 7, 1123. Perez-Ilzarbe, J., Hernandez, T., Estrella, I., Vendrell, M., 1997. Cold storage of apples (cv. Granny Smith) and changes in phenolic compounds. Z Lebensm Unters Forsch. 204, 52 55. Posmyk, M.M., Bailly, C., Szafranska, K., Jasan, K.M., Corbineau, F., 2005. Antioxidant enzymes and isoflavonoids in chilled soybean [Glycine max (L.) Merr.] seedlings. J. Plant Physiol. 162, 403 412. Posmyk, M.M., Balabusta, M., Wieczorek, M., Sliwinska, E., Janas, K. M., 2009. Melatonin applied to cucumber (Cucumis sativus L.) seeds improves germination during chilling stress. J. Pineal Res. (46), 214 223. Randhir, R., Lin, Y.-T., Shetty, K., 2004. Phenolics, their antioxidant and antimicrobial activity in dark germinated fenugreek sprouts in response to peptide and phytochemical elicitors. Asia Pac. J. Clin. Nutr. 13, 295 307. Rice-Evans, C.A., Miller, N.J., Paganga, G., 1997. Antioxidant properties of phenolic compounds. Trends Plant Sci. 2, 152 159. Rieger, G., Muller, M., Guttenberger, H., Bucar, F., 2008. Influence of altitudinal variation on the content of phenolic compounds in wild populations of Calluna vulgaris, Sambucus nigra, and Vaccinium myrtillus. J. Agric. Food Chem. 58, 9080 9086. Robards, R., Antolovich, M., 1997. Analytical chemistry of fruit bioflavonoids. A review. Analyst 122, 11R 34R. Rozema, J., Bjorn, L.O., Bornman, J.F., Gaberscik, A., Hader, D.P., Trost, T., et al., 2002. The role of UV-B radiation in aquatic and terrestrial ecosystems 2 an experimental and functional analysis of the evolution of UV-absorbing compounds. J. Photochem. Photobiol. B. 66, 2 12. Ryan, K.G., Swinny, E.E., Winefield, C., Markham, K.R., 2001. Flavonoids and UV photoprotection in Arabidopsis mutants. Z. Naturforsch. 56, 745 754. Sa´nchez-Rodrı´guez, E., Moreno, D.A., Ferreres, F., del Mar RubioWilhelmi, M., Ruiz, J.M., 2011. Differential responses of five cherry tomato varieties to water stress: changes on phenolic metabolites and related enzymes. Phytochemistry 72, 723 729. Schroeter, H., Boyd, C., Spencer, J.P., Williams, R.J., Cadenas, E., Rice-Evans, C., 2002. MAPK signaling in neurodegeneration: influences of flavonoids and of nitric oxide. Neurobiol. Aging. 23, 861 880. Schulze-Lefert, P., Dangl, J.L., Becker-Andre, M., Hahlbrock, K., Schulz, W., 1989. Inducible in vivo DNA footprints define sequences necessary for UV light activation of the parsley chalcone synthase gene. EMBO J. 8, 651 656. Selmar, D., 2008. Potential of salt and drought stress to increase pharmaceutical significant secondary compounds in plants. Landbauforsch. Volkenrode. 58, 139 144. Shahidi, F., Naczk, M., 1995. Food Phenolics: Sources, Chemistry, Effects, Applications. Technomic Publishing Company Inc, Lancaster, PA. Shiozaki, N., Hattori, I., Gojo, R., Tezuka, T., 1999. Activation of growth and nodulation in symbiotic system between pea plants and leguminous bacteria by near UV radiation. J. Photochem. Photob. B. Biol. 50, 33 37. Solecka, D., 1997. Role of phenylpropanoid compounds in plant responses to different stress factors. Acta Physiol. Plant. 19, 257 268. Soliz-Guerrero, J.B., de Rodriguez, D.J., Rodriguez-Garcia, R., Angulo-Sanchez, J.L., Mendez-Padilla, G., 2002. Quinoasaponins: concentration and composition analysis. In: Janick, J., Whipkey,

167

A. (Eds.), Trends in New Crops and New Uses. ASHS Press, Alexandria, p. 110. Spitaler, R., Winkler, A., Lins, I., Yanar, S., Stuppner, H., Zidorn, C., 2008. Altitudinal variation of phenolic contents in flowering heads of Arnica montana cv. ARBO: a 3-year comparison. J. Chem. Ecol. 34, 369 375. Stapleton, A.E., 1992. Ultraviolet radiation and plants: burning questions. Plant Cell. 4, 1353 1358. Subba Rao, M.V., Muralikrishna, G., 2002. Evaluation of the antioxidant properties of free and bound phenolic acids from native and malted finger millet (Ragi, Eleusine, coracana, Indaf-15). J. Agric. Food Chem. 50, 889 892. Swain, T., 1975. Evolution of flavonoid compounds. In: Harborne, J.B., Mabry, T.J., Mabry, H. (Eds.), The Flavonoids. Chapman & Hall, London, pp. 1096 1138. Tegelberg, R., Julkunen-Tiitto, R., Aphalo, P.J., 2004. Red: farred light ratio and UV-B radiation: their effects on leaf phenolics and growth of silver birch seedlings. Plant Cell Environ. 27, 1005 1013. Thimmaraju, B.N., Ravishankar, G.A., 2004. In situ and ex situ adsorption and recovery of betalains from hairy root cultures of Beta vulgaris. Biotechnol. Prog. 20, 777 785. Trejo-Tapia, G., Jimenez-Aparicio, A., Rodriguez-Monroy, M., De Jesus-Sanchez, A., Gutierrez-Lopez, G., 2001. Influence of cobalt and other microelements on the production of betalains and the growth of suspension cultures of Beta vulgaris. Plant Cell Tissue Organ. Cult. 67, 19 23. Tuteja, N., Mahajan, S., 2007. Calcium signaling network in plants: an overview. Plant Signal. Behav. 2, 79 85. PMID: 19516972. Tuteja, N., Ahmad, P., Panda, B.B., Tuteja, R., 2009. Genotoxic stress in plants: shedding light on DNA damage, repair and DNA repair helicases. Mutat. Res. 681, 134 149. Verslues, P.E., Sharma, S., 2010. Proline metabolism and its implications for plant environment interaction. Arabidopsis Book 8, 0140. Available from: https://doi.org/10.1199/tab.0140. Villiers, F., Ducruix, C., Hugouvieux, V., Jarno, N., Ezan, E., Garin, J., et al., 2011. Investigating the plant response to cadmium exposure by proteomic and metabolomic approaches. Proteomics 11 (9), 1650 1663. Weidner, S., Karama´c, M., Amarowicz, R., Szypulska, E., Golgowska, A., 2007. Changes in composition of phenolic compounds and antioxidant properties of Vitis amurensis seeds germinated under osmotic stress. Acta Physiol. Plant 29, 238 290. ´ Weidner, S., Karolak, M., Karama´c, M., Kosinska, A., Amarowicz, R., 2009a. Phenolic compounds and properties of antioxidants in grapevine roots (Vitis vinifera) under drought stress followed by regeneration. Acta Soc. Bot. Pol. 78, 97 103. Weidner, S., Kordala, E., Brosowska-Arend, T.W., Karama, M., ´ Kosinska, A., Amarowicz, R., 2009b. Phenolic compounds and properties of antioxidants in grapevine roots followed by recovery. Acta Soc. Bot. Pol. 78, 279 286. Williams, R.J., Spencer, J.P., Rice-Evans, C., 2004. Flavonoids: antioxidants or signaling molecules? Free Radic. Biol. Med. 36, 838 849. Winkel-Shirley, B., 2001. Flavonoid biosynthesis, a colorful model for genetics, biochemistry, cell biology and biotechnology. Plant Physiol. 26, 485 493. Winkel-Shirley, B., 2002. Biosynthesis of flavonoids and effects of stress. Curr. Opin. Plant Biol. 5, 218 223. Wro´bel, M., Karma´c, M., Amarowicz, R., Fra˛czek, E., Weidner, S., 2005. Metabolism of phenolic compounds in Vitis riparia seeds during stratification and during germination under optimal and low temperature stress conditions. Acta Physiol. Plant 27 (3A), 313 320.

PLANT SIGNALING MOLECULES

168

9. ROLE AND REGULATION OF PLANTS PHENOLICS IN ABIOTIC STRESS TOLERANCE: AN OVERVIEW

Wu, S., Chappell, J., 2008. Metabolic engineering of natural products in plants; tools of the trade and challenges for the future. Curr. Opin. Biotechnol. 19, 145 152. Yamasaki, H., Heshiki, R., Ikehara, N., 1995. Leaf-goldening induced by high light in Ficus microcarpa L. f., a tropical fig. J. Plant Res. 108, 171 180. Yamasaki, H., Takahashi, S., Heshiki, R., 1999. The tropical fig Ficus microcarpa L. f. cv. Golden Leaves lacks heat-stable dehydroascorbate reductase activity. Plant Cell Physiol. Zhu, J.K., 2016. Abiotic stress signalling and responses in plants. Cell 167 (2), 313 324. Zidorn, C., Schubert, B., Stuppner, H., 2005. Altitudinal differences in the contents of phenolics in flowering heads of three members of the tribe Lactuceae (Asteraceae) occurring as introduced species in New Zealand. Biochem. Syst. Ecol. 33, 855 872.

Further Reading Alscher, R.G., Donahue, H.L., Cramer, C.L., 1997. Reactive oxygen species and antioxidants: relationships in green cells. Physiol. Plant 100, 224 233. Blumthaler, M., Ambach, M., Ellinger, R., 1997. Increase in solar UV radiation with altitude. J. Photochem. Photobiol. B 39, 130 134. Draper, J., 1997. Salicylate, superoxide synthesis and cell suicide in plant defence. Trends Plant Sci. 2, 162 165. Lattanzio, V., Linsalata, V., Palmieri, S., Van Sumere, C.F., 1989. The beneficial effect of citric and ascorbic acid on the phenolic browning reaction in stored artichoke (Cynara scolymus L.) heads. Food Chem. 33, 93 106.

PLANT SIGNALING MOLECULES