Next Article in Journal / Special Issue
Assessing Combining Abilities of Popcorn Inbred Lines for Agronomic and Root Traits under Contrasting Water Conditions: Towards Developing Drought-Tolerant Genotypes
Previous Article in Journal
Algae Polysaccharides (Carrageenan and Alginate)—A Treasure-Trove of Antiviral Compounds: An In Silico Approach to Identify Potential Candidates for Inhibition of S1-RBD Spike Protein of SARS-CoV2
Previous Article in Special Issue
Varietal Differences of Yield, Morphological, and Biochemical Parameters of Allium cepa L. under Precipitation Excess in Different Phenological Phases
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Stresses
Volume 3
Issue 3
10.3390/stresses3030040
stresses-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

An Overview of Plant Phenolics and Their Involvement in Abiotic Stress Tolerance

by
Krishna Kumar
1,†,
Pratima Debnath
2,†,
Sailendra Singh
1,* and
Navin Kumar
3,*
1
Migal Galilee Research Institute, Kiryat Shmona 1101600, Israel
2
CSIR-National Botanical Research Institute, Lucknow 226001, India
3
Institute of Plant Sciences, Agricultural Research Organization, Rishon LeZion 7505101, Israel
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Stresses 2023, 3(3), 570-585; https://doi.org/10.3390/stresses3030040
Submission received: 10 June 2023 / Revised: 24 July 2023 / Accepted: 28 July 2023 / Published: 8 August 2023
(This article belongs to the Collection Feature Papers in Plant and Photoautotrophic Stresses)
Browse Figures
Versions Notes

Abstract

:
Secondary metabolites, such as phenols and salicylic, play a crucial role in the regulation of development and tolerance mechanisms against a wide range of stresses. During adverse conditions such as biotic and abiotic stresses, plants induce the biosynthesis of phenolic compounds to provide tolerance. Phenolics are secondary aromatic metabolites synthesized through the shikimate/phenylpropanoid pathway or polyketide acetate/malonate pathway, which produce monomeric and polymeric phenolics. Phenolic compounds in plants not only take part in preventing stresses but also in regulating physiological activities. These compounds significantly regulate both below- and above-ground defense mechanisms. Plants synthesize thousands of phenolic compounds throughout their evolution to survive in changing environments. Environmental factors, such as high light, cold, drought, heavy metals, etc., increase the accumulation of phenolics to neutralize any toxic effects. This review focuses on the biosynthesis of phenolic compounds and their updated studies against abiotic stresses.

1. Introduction

Phenolic compounds are ubiquitously present in the plant kingdom. Phenolics are very rarely present in bacteria, fungi, and algae. Vascular plants are the primary source of a wide range of polyphenols, while lower plants such as bryophytes are the leading producers of flavonoids [1,2]. Plant phenolics can be defined by ‘phenol’, a chemical term describing a phenyl ring bearing one or more hydroxyl substituents. Several classes of phenolics have been categorized based on their basic skeleton [3]. Phenolic compounds range from simple to low molecular weight, single aromatic-ringed to large and complex tannins and their derived polyphenols. Phenolic compounds are broadly classified into two major groups: flavonoids and non-flavonoids [3]. Secondary metabolites, such as phenolic compounds, do not directly affect plant growth and development. They regulate other associated pathways for their function via signal transduction. These compounds protect plants from disease/damage and also contribute to the plant’s color, aroma and flavor [4]. During the last four decades, several researchers have shown keen interest in investigating their regulatory mechanism, which involves tolerance mechanisms, against several biotic and abiotic factors such as microbial infections, pollinators, seed-dispersing animals, UV, temperature, drought, etc. Phenolic compounds function as signal molecules and are also involved in forming root nodules in legume plants for the nitrogen fixation [5]. They exhibit diverse structures, from single aromatic rings (caffeic acid and ferulic acid) to more complex polymeric structures such as lignins/lignans, coumarins, quinones, tannins, and flavonoids (Figure 1). This review highlights the importance of plant phenol compounds in plant abiotic stress response.

2. Different Types of Phenolic Compounds and Their Biosynthesis

Plants produce an exceptionally diverse array of low molecular mass compounds, often called secondary metabolites, and they are essential for anticipating and responding to biotic and abiotic stress. [6]. These metabolites are generally derived from different biosynthetic routes such as isoprenoid, phenylpropanoid, alkaloid, or fatty acid pathways. The phenolic compound is derived either from the shikimic acid pathway or pentose phosphate through phenylpropanoid metabolism [7]. The phenolic compound contains benzene rings with one or more hydroxyl substituents, which are synthesized from simple phenolic molecules to highly polymerized compounds according to their demand function. The primary metabolisms, such as glycolysis and pentose phosphate pathways, provide compounds such as phosphoenolpyruvate and erythrose-4-phosphate to initiate the biosynthesis of phenolic compounds. Together, phosphoenolpyruvate and erythrose-4-phosphate produce shikimic acid via the shikimate pathway. Further, this pathway provides L-phenylalanine, which takes part in the phenylpropanoid pathway to produce p-coumaroyl CoA. This compound initiates the synthesis of phenylpropanoids and monolignols to produce more complex phenolic compounds such as stilbenes or flavonoids after reacting with three malonic acid molecules [8] (Figure 2). An overview of these participating pathways has been summarized below.

2.1. Flavonoids

Flavonoids are polyphenolic molecules containing 15 carbon atoms with two aromatics rings. Flavonoids are the most diverse class of phenolic compounds and are present in all types of plants within the plant kingdom [9]. They mostly accumulate in very high concentrations in the leaf’s epidermis and fruits’ skins. The flavonoid biosynthesis is mainly initiated through the phenylpropanoid pathway. During normal conditions, flavonoids act as a signaling molecule and UV protectant and regulate plant hormones such as auxin and cytokinin [10]. However, during stress conditions, they protect from oxidative damage [11]. Stress-induced dihydroxy B-ring-substituted flavonoids actively scavenge ROS [12]. Flavonoids are classified into many groups, and the main subclasses are flavonols, flavan-3-ols, isoflavones, flavones, anthocyanidins, and flavanones (Figure 2). Minor flavonoid groups are dihydroflavonols, flavan-3,4-diols, coumarins, chalcones, dihydrochalcones, and aurones. Flavonoids contain various substituents such as hydroxyl groups, present at the skeleton’s 4th, 5th, and 7th positions.

2.1.1. Flavonoid Biosynthetic Pathway

Plants produce an exceptionally diverse array of low molecular mass compounds, often called secondary metabolites, which are essential for anticipating and responding to biotic and abiotic stress. These metabolites are generally derived from different biosynthetic routes such as isoprenoid, phenylpropanoid, alkaloid, or fatty acid pathways. The phenolic compound is derived either from the shikimic acid pathway, phenylpropanoid, or both [13]. The shikimic acid pathway is a major route for the biosynthesis of aromatic compounds in plants and microorganisms. Phenylalanine, tyrosine, and tryptophan are the primary metabolites that provide the precursor for most of the secondary metabolite compounds. Flavonoids are synthesized from phenylalanine which is derived from the shikimate pathway [7,14] (Figure 3). The shikimate pathway initiates with the molecule as phosphoenol pyruvate (PEP) and D-erythrose-p-phosphate and forms the intermediate precursor-shikimic acid following several steps (Figure 3). This shikimic acid gets converted to chorismic acid, which leads to the synthesis of phenylpropanoid pathway, starts with aromatic amino acid, phenylalanine, and tyrosine. The derived phenylalanine gets converted to coumaric, caffeic, and ferulic acids through the activity of phenylalanine ammonia-lyase (PAL), cinnamic acid 4-hydroxylase (C4H), and 4-coumarate: CoA ligase (4CL), which ultimately opens the lignin biosynthesis route in the plant systems. The coumaric acid also leads towards the biosynthesis of hydroxycinnamic acids such as caffeic, ferulic, and chlorogenic acids. On the other hand, the shikimic acid from the shikimate pathway also contributes towards the synthesis of gallic acid by the action of shikimate dehydrogenase (SDH). Synthesized gallic acid is then converted to glucogallin by UDP-3-glucosyltransferase (UGT), which then produces two important tannins-gallotannins and ellagitannins of the hydrolysable tannin pathway (Figure 3).
In general, the flavonoid biosynthesis pathway (Figure 3) also includes several intermediates such as flavanones (naringenin, hesperitin, dihydrokaempferol and eriodictyol), flavanols (kaempferol, myricetin, quercetin) and flavanone glycosides (delphinidin 3-O-glucoside, quercetin 3-O-glucoside). Flavanones are an important phenolic class that mostly occurs in citrus fruits such as lemons and oranges. The formation of naringenin chalcone from the condensation of p-coumaroyl-CoA with three malonyl CoA residues, catalyzed by chalcone synthase (CHS), is described in Figure 3. The product naringenin chalcone is then converted to naringenin by the action of chalcone isomerase (CHI) and finally to dihydrokaempferol. This dihydrokaempferol further diverges for the production of different classes of flavonoids, including isoflavones, flavanones, flavones, flavanols, flavan-3-ols and anthocyanins (Figure 3).

2.1.2. Flavone and Flavanone Biosynthesis

The dehydrogenation of flavanones results in the formation of flavones (2-aryl-4H-chromen-4-ones) by the action of enzyme flavone synthase via the conversion of flavanones to flavones, for example as leteolin, apigenin, and galangin. Such conversion requires NADPH and oxygen to introduce a double bond between the C-2 and C-3 residues in flavanones (Figure 3).

2.1.3. Isoflavonoid Biosynthesis

A leguminous plant predominantly accumulates the isoflavonoids and the responsible enzymes for their biosynthesis, as have been identified and characterized earlier [15]. During these pathways, microsomal cytochrome P450 isoflavone synthase catalyzes and converts naringenin and isoquiritigenin into the isoflavones genistein and daidzein, respectively [16].

2.1.4. Anthocyanin Biosynthesis

Cyanidin, pelargonidin, and delphinidin are the most commonly explored anthocyanidins; they are present in flowers and fruits and are also responsible for their distinct colour variations [13]. The regulatory mechanism of anthocyanin biosynthesis has been explored broadly, starting with the hydroxylation of flavanones to produce dihydroflavonols by flavanone 3-hydroxylase (F3H) (Figure 3). Then, dihydroflavonols were reduced to flavan-3,4-diols (leucoanthocyanins) by the enzyme dihydroflavonol reductase (DFR). Anthocyanidin synthase (ANS) catalyzes the last step in the biosynthesis of anthocyanins. Finally, Flavonoid-3-O-glucosyltransferase (FGT) transfers the glucosyl moiety from UDP glucose to the 3-hydroxyl group of anthocyanidins and forms anthocyanins (Figure 3).

2.2. Non-Flavonoids

Non-flavonoids are classified as phenolics acid, tannins, stilbenes and lignans [17]. Most of the non-flavonoids present in fruits and vegetables have dietary significance. Phenolic acids such as gallic acid, acts as a precursor of hydrolysable tannins. Similarly, C6–C3 hydroxycinammates (p-Coumaroyl) and their derivatives are polyphenolic C6–C2–C6 stilbenes. However, lignans derived from phenylpropanoid E-coniferyl alcohol.

Stilbene Biosynthesis

The stilbene is also synthesized by the condensation of p-coumaroyl CoA with three units of malonyl CoA, catalyzed by the enzyme stilbene synthase. Stilbene synthase and chalcone synthase (CHS) are structurally very similar enzymes. Stilbene synthase is induced by a wide range of stresses such as UV radiation and bacterial and fungal infections [17].

3. Responses of Phenolic Compound to Abiotic Stress

Plants regularly synthesize secondary metabolites in response to environmental changes, which leads to the ability to adapt and survive in response to environmental cues and various kinds of stresses. Accumulations of phenolic compounds in plants are associated with the growth conditions and factors related to metabolic pathways, which can be associated with stress conditions or signaling (Figure 4) [18]. Plants are exposed to a diverse range of abiotic stresses (temperature, drought, salinity, alkalinity, UV) and pathogens/herbivores, which cause severe damage to the plants [15]. These biotic and abiotic factors increase reactive oxygen species (ROS), causing oxidative damage in plants. ROS such as superoxide anion (O2−), hydrogen peroxide (H2O2), singlet oxygen (1O2), and the hydroxyl radical (HO˙) are highly reactive compounds which react with different biomolecules, leading to an alteration in biochemical and physiological activities. ROS generally generates in lower amounts during the cellular metabolic process, where it works as a signal molecule. However, several external factors highly enhance the level of ROS, which starts to cause oxidative damage. Oxidative stress elevates several stress mechanisms in plants, such as different enzymatic antioxidants (superoxide dismutase, SOD; catalase, CAT; ascorbate peroxidase, APX; glutathione reductase, GR; monodehydroascorbate reductase, MDHAR; dehydroascorbate reductase, DHAR; glutathione peroxidase, GPX; guaiacol peroxidase, GOPX; glutathione S-transferase, GST; nicotinamide adenine dinucleotide phosphate (NADPH) oxidase-like alternative oxidase, AOX; thioredoxins, TRXs; glutaredoxin, GRX; etc.) and nonenzymatic antioxidants (ascorbic acid, AsA; glutathione, GSH; phenolic acids; alkaloids; flavonoids; carotenoids; α-tocopherol; nonprotein amino acids; etc.) [16]. In nonenzymatic antioxidants, the elevated level of phenolic compounds during oxidative stress, potentially protects plants from oxidative damage [16]. Phenols directly or indirectly other defence mechanisms, which protect plants from massive damage, caused by oxidative stress. Oxidative bursts damage several biomolecules, such as nucleic acids, proteins and lipids. When ROS reacts with the membrane lipids, it converts into lipid peroxides (LOOH), producing different carbonyl compounds such as aldehydes and ketones. Some of these compounds contain carbonyl-conjugated C-C bonds, known as reactive carbonyl species (RCS). RCS contains one or more carbonyl groups, generally known for their toxic effects on organisms [19].
On the other hand, during antioxidative activities, phenols oxidized into univalent form by enzymatic or nonenzymatic activities with respect to phenoxyl radicals. Phytophenols, such as polyphenols, support ascorbate-dependent antioxidative defence mechanisms to protect plants against oxidative damage [20]. In another defence mechanism against ROS, flavonoids and other polyphenols such as quercetin, rutin, and catechin react with some of the biometal ions (Fe(II) and Cu(I)) as a chelating agent to reduce lipid alkoxyl radicals (a strong oxidant, participating in lipid-peroxidation) [21]. Simultaneously, polyphenols provide rapid chemical scavenging for free radical damage on biomolecules through H-atom donation or electron transfer. Similarly, the number of hydroxy groups in the aromatic B-ring of flavonoids directly participates in ROS scavenging activity. However, few studies indicate that phenolic compounds, such as phoretin (which synthesizes in tea and apple) [22] and pelargonidin (which synthesizes in brown rice) [23], act as RCS scavengers. Besides these, several multi-omics technologies are used to understand the mechanism of different phenolic compounds against abiotic stresses. This review discusses the recent updates in the responses of phenolic compounds to different abiotic stresses.

3.1. Drought

The integral approach to stabilizing the negative impacts of drought stress on plants is enhancing their inherent accumulation of phenolic compounds [24]. Studies of many plant species revealed an improved accumulation of flavonoids under drought conditions that provide resistance to these plants [25]. The distinct antioxidant properties of phenolic acids and flavonoids prevent plants from the adverse effects of water deficit conditions. Drought stress induces the biosynthesis of phenolic and flavonoids, ultimately leading to enhanced plant production [26,27]. The enhanced accumulation of kaempferol and quercetin in tomatoes helps them to cope with the improved drought conditions via detoxification of H2O2. The accumulation of phenolic compounds results from modulation in the phenylpropanoids pathway. Many of the important protein-encoding genes of these pathways are regulated by the drought, which leads to the stimulation of phenolic compounds. A study reported that drought stress enhances potato tubers’ polyphenol biosynthesis genes (PAL, HCT, C3H, CHS, CHI, F3H, DFR, and AN1) [28]. Similarly, a recent study indicated that drought stress upregulates the biosynthesis of flavonoids by regulating the heat shock factors. In this study, under drought conditions, MdHSFA8a (Malus domestica heat shock factor A8a) was released from MdHSP90-MdHSFA8a (Malus domestica heat shock factor 90) complexes and interacted with an AP2/ERF family transcriptional factor MdRAP2.12 to activate the genes involved in the flavonoid biosynthesis in Malus domestica [29]. In another study, different types of anthocyanins, such as A11, A9, A8, and A5 were found to be induced by short-term drought stress in Arabidopsis, in which A11 was the major anthocyanin [30]. The impact of drought stress on the accumulation of phenolic and related processes is also described in Table 1.

3.2. Salt Stress

Salt stress causes osmotic disturbance in plants, which reduces the volume of vacuoles and cytoplasm cells, ultimately leading to cellular dehydration. Additionally, higher salt concentration also induces oxidative stress via the generation of ROS such as superoxide anions, hydrogen peroxide, and hydroxyl ions. To counter this type of adverse effect, a differential accumulation of specific secondary metabolites occurs in plants [41,42]. Phenolic compounds are well known for their potential antioxidant properties, which help to scavenge ROS under salt stress [43,44,45]. Salt stress induces the phenylpropanoid biosynthetic pathway, which consequently elevates various kinds of phenolic compound biosynthesis [44,46,47]. The polyphenols content increases in different plant tissue with an increase in salinity level [48]. A report demonstrated that total phenolic content increased in red pepper under a moderate increase in salinity level [49]. In tobacco plants, NtCHS1 (Nicotiana tabacum chalcone synthase 1) enhanced the accumulation of flavonoids upon the salinity stress, which lead to the scavenging of ROS [43]. In Vitis vinifera, the induction of a transcriptional factor, such as VvbHLH (Vitis vinifera basic helix–loop–helix), enhances flavonoid biosynthesis and protects from salt stress damage [50,51]. In Glycine max, an upregulation of the flavone synthase gene was observed against salt stress, which indicates that the flavones play a crucial role under salinity stress [52]. Other phenolic compounds, such as anthocyanin and phenolic acid, are also induced by salinity stress [44,53]. An overview of the positive effect of salt stress on the endogenous levels of phenolic compounds in different plant species is given in Table 2.

3.3. Heavy Metal

Heavy metals are a potential abiotic stress factor, which reduces growth and physiology by generating oxidative stress [24]. These metals lead to changes in the metabolic as well as the photosynthetic activity of plants. Metal/metalloid ions, mainly lead, nickel, silver, cadmium, arsenic, etc., enhance the production of secondary metabolites, which helps plants to cope with stresses [26]. The accumulation of heavy metals triggers oxidative bursts by generating ROS such as O2−, H2O2, and HO˙, which cause several biomolecular damages, leading to to toxicity in the plant and ultimately a retard its growth and productivity [63,64,65,66]. Heavy metals contain several donating electrons in their outer shell, which are in a cellular condition gained by native O2, leading to highly reactive ROS. To cope with this adverse effect, plants enhance the biosynthesis of secondary metabolite production, especially phenolic compounds. Under metal toxicity, flavonoids play a crucial role, which enhances the metal chelation and reduces the hydroxyl radicles from the plant’s tissue [67,68].
Metal toxicity mainly induces the accumulation of flavonoids such as anthocyanins and flavones [69,70]. During metal stress, the upregulation of some of the key enzymes, such as chalcone synthase, shikimate dehydrogenase, cinnamyl alcohol dehydrogenase, and polyphenol oxidase, induces phenylpropanoid biosynthesis in plants [70]. The key enzymes, such as SKDH (Shikimate dehydrogenase) and G6PDH (glucose-6-phosphate dehydrogenase), catalyze several biological actions needed for the synthesis of the starting precursors for the phenylpropanoid biosynthesis, during metal stress [71]. A recent study demonstrated that an elevated accumulation of Pb and Cu induces the activities of PAL (Phenylalanine ammonia-lyase) and TAL (tyrosine ammonia-lyase) in winter wheat plants, which are the key enzymes of phenylpropanoid biosynthesis [72]. Generally, activating the phenylpropanoid pathway synthesizes nonenzymatic compounds such as flavonoids, coumarins, and lignans, which protect plants from oxidative stress [73]. Similarly, in another study, chlorogenic acid was found to be enhanced against Pb stress in Zea mays [69]. Polyphenols such as tannins contain unique structures, facilitating electrostatic, hydrogen bonding, and hydrophobic interactions with metal ions. Simultaneously, the catechol or galloyl groups of tannin compounds provide chelating sites for metals, which protect them from metal toxicity [74].

3.4. UV Radiation

Light quality and UV radiation also influence the synthesis of secondary metabolites in plants [75,76]. UV radiation damages the protein structure and causes a mutation in the genome, which is harmful in nature and leads to ROS generation in plants. To overcome the detrimental effects of UV radiation, plants elevate the biosynthesis of secondary metabolites production. The higher accumulation of secondary metabolites such as alkaloids [60], terpenoids [59], and phenolic compounds protect from UV radiation [43]. A higher level of phenolic compound underneath epidermal cells provides a protective layer, which further prevents thymine dimerization and ultimately reduces DNA damage [24]. Many reports suggest that plants accumulate more flavonoids under high light and UV radiations [59,77], which can screen the UV and visible lights by absorbing capacity and protecting the plant from damage [78,79].
There is ahigher accumulation of phenolic compounds as a result of the induction of flavonoid biosynthesis pathway genes under high light and UV radiation [80,81]. Flavonoids are potential scavengers of ROS, specifically, those flavonoids which contain a catechol group in the B-ring of the flavonoid skeleton (e.g., quercetin derivatives). An excess of light or UV-B radiation induces the biosynthesis of dihydroxy B-ring-substituted flavonoids (e.g., luteolin derivatives) at the cost of other less effective flavonoids (e.g., kaempferol derivatives) [82]. The essential biosynthesis pathway genes of flavonoids such as CHS, CHI, FLS, DFR, FHT, FGT, and PAL are induced with UV radiation [83,84]. Simultaneously, acylated anthocyanins absorb UV radiation and provide tolerance against UV stress in plants [85]. A few reports indicate that the higher accumulation of phenolic compounds is also caused by the jasmonic acid and ABA-mediated modulation of phenylpropanoid pathways under UV radiation [86,87]. Table 3 briefly summarizes the effect of UV exposure on the endogenous phenolic composition of plants.

3.5. Some Other Abiotic Factors

Abiotic factors such as nanoparticles, aerosol, temperature and pesticides also stimulate the production of phenolic compounds in plants. Phenolic compounds prevent plants from the phytotoxic effects of these abiotic stresses [99]. Plants also produce and accumulate more anthocyanins, flavonoids, flavanols, and phenolic acids upon temperature stress, and these metabolites protect plant cells from any damage caused by these types of stress [100,101,102,103]. Under pesticide stress, plants enhance phenolic compounds to avoid any toxic effects. The accumulation of phenolic compounds results from upregulating key biosynthetic genes and activating the key enzymes of phenylpropanoid-branched chain reactions such as PAL and CHS [103,104]. It was also reported that the plant Festuca trachyphylla under heat stress conditions increased biosynthesis and the accumulation of phenolic compounds such as 4-hydroxybenzoic acid, benzoic acid, caffeic acid, coumaric acid, cinnamic acid, gallic acid, homo-vanillic acid, ferulic acid, and salicylic acid [105]. The accumulation of these compounds enhanced plant resistance via detoxifying ROS, which is generated under heat-stress conditions [106]. The plant produces more phenolic compounds, such as suberin or lignin, which strengthen the plant cell wall and help the plant to avoid chilling injuries [24].

4. Effect of Biostimulants on Polyphenols Accumulation

Plant biostimulants are substances or microorganisms that, when applied to plants, aim to enhance their nutrient uptake, physiological processes, and stress tolerance, ultimately promoting plant growth and development [107]. Biostimulants can be treated as an additive to fertilizers, and they support the uptake of nutrients, promote plant growth, and increase their tolerance to abiotic stress. Biostimulants can stimulate the synthesis of secondary metabolites, including polyphenols, in plants. These compounds act as signaling molecules that trigger the plant’s defense responses against stress factors such as pests, pathogens, and abiotic stresses such as drought and heat [107]. Polyphenols, on the other hand, are a diverse group of secondary metabolites found in plants that have various biological activities and are of interest for their potential health benefits for both plants and humans. The effects of plant biostimulants on polyphenols can vary depending on the specific biostimulant used, the plant species involved, and the environmental conditions. A study reported that the biostimulants Kelpak and Asahi SL significantly enhance polyphenols in potato leaves and tubers [108]. Similarly, a biostimulant (VIVEMA TWIN) made from a combination of condensed and hydrolysable tannins was used against salt stress in Solanum lycopersicum L. This study indicated that the application of biostimulant VIVEMA TWIN upregulated several of the genes (285 genes) involved in root development and salt stress tolerance. Another biostimulant (BALOX®) based on polyphenols at 1.4% (w/w) and glycine betaine at 3.0% (w/w) was reported to enhance the salt stress tolerance and polyphenols content in tomato plants. This biostimulant enhanced plant growth, especially at the root level and in saline soil conditions [109]. Similarly, A. nodosum seaweed extract was reported to significantly enhance the phenolic compound content of grapes [110]. In a study, protein hydrolysate was used as a biostimulant to enhance phenolic compounds in tomato plants. In this study, protein hydrolysate not only enhanced phenolic compounds but also significantly increased the level of ascorbic acid and lycopene, which indicates its potential role in the enhancement of antioxidants and stress-responsive compounds [111]. Biostimulant application is a non-toxic and feasible option for agriculture to boost the phenolic compounds in plants to aid against abiotic stresses.

5. Conclusions

Plants are sessile in nature and adapt to various protective mechanisms for their better survival with respect to diverse environmental cues. Secondary metabolites such as flavonoids, phenolics, stilbenes, hydroxycinnamic acids, etc., are produced in extremely lower concentrations within plants under normal environmental conditions for signaling and metabolism. However, external abiotic factors such as drought, light, temperature, etc., retards overall plant growth/development. Furthermore, it leads to the induction of biosynthesis of specific types of secondary metabolites to combat the wide range of adverse effects. In addition, other abiotic factors, such as pesticides, can also accelerate the endogenous phenolic biosynthesis and facilitate resistance against the phytotoxic consequences of these abiotic stresses. In recent years, integrating multiple omics methods such as transcriptome, proteome, and metabolome has become essential to understanding and identifying the crucial stress-responsive genes in plants during abiotic stresses. Amongst the secondary metabolism in plants, the phenylpropanoid pathway is likely the most studied pathway in terms of abiotic stresses. The change in the environmental condition acts as a stimulus which activates the phenylpropanoid pathways via induction of the signaling process and transcriptional upregulation of the key pathway genes. These compounds provide resistance to the plant and regulate multiple of its functions. Some polyphenolic compounds serve as a scavenger that removes the ROS molecules generated during oxidative bursts, and some of them function as protective in nature, such as flavonoids and anthocyanins. Although there are several reports available in which induction of the phenylpropanoid pathway leads to a change in phenylpropanoid metabolite composition irrespective of the kinds of stimuli, few studies have indicated whether these responses share a similar type of mechanism, and which specific conditions are responsible for the shift from primary metabolites to phenylpropanoid pathways. In addition, the application of biostimulant is a sustainable approach to inducing phenolic compounds in plants to aid against abiotic stresses. However, their mechanisms of action are, in some cases, still a challenge and need to be recognized because the nature of their beneficial influence is not fully understood. Biostimulants are, therefore, a hot topic in agriculture and still require in-depth research.

Author Contributions

The study was completed with keeping in mind all the ethics and scientific accuracy. K.K., S.S. and P.D. have written the manuscript. S.S. and N.K. have edited and corrected the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

No new data were created or analyzed in this study. Data sharing is not applicable to this article.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Soares, C.; Carvalho, M.E.; Azevedo, R.A.; Fidalgo, F. Plants facing oxidative challenges—A little help from the antioxidant networks. Environ. Exp. Bot. 2019, 161, 4–25. [Google Scholar] [CrossRef]
  2. Guo, H.; Feng, X.; Hong, C.; Chen, H.; Zeng, F.; Zheng, B.; Jiang, D. Malate secretion from the root system is an important reason for higher resistance of Miscanthus sacchariflorus to cadmium. Physiol. Plant 2017, 159, 340–353. [Google Scholar] [CrossRef] [PubMed]
  3. Al Mamari, H.H. Phenolic compounds: Classification, chemistry, and updated techniques of analysis and synthesis. In Phenolic Compounds: Chemistry, Synthesis, Diversity, Non-Conventional Industrial, Pharmaceutical and Therapeutic Applications; IntechOpen: Rijeka, Croatia, 2021; pp. 73–94. [Google Scholar]
  4. Pandey, K.B.; Rizvi, S.I. Plant polyphenols as dietary antioxidants in human health and disease. Oxidative Med. Cell. Longev. 2009, 2, 270–278. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  5. Lateif, K.A.; Bogusz, D.; Hocher, V. The role of flavonoids in the establishment of plant roots endosymbioses with arbuscular mycorrhiza fungi, rhizobia and Frankia bacteria. Plant Signal. Behav. 2001, 7, 636–664. [Google Scholar] [CrossRef] [Green Version]
  6. Piasecka, A.; Kachlicki, P.; Stobiecki, M. Analytical methods for detection of plant metabolomes changes in response to biotic and abiotic stresses. Int. J. Mol. Sci. 2019, 20, 379. [Google Scholar] [CrossRef] [Green Version]
  7. Mandal, S.M.; Chakraborty, D.; Dey, S. Phenolic acids act as signaling molecules in plant-microbe symbioses. Plant Signal. Behav. 2010, 5, 359–368. [Google Scholar] [CrossRef] [Green Version]
  8. Santos-Sánchez, N.F.; Salas-Coronado, R.; Hernández-Carlos, B.; Villanueva-Cañongo, C. Shikimic acid pathway in biosynthesis of phenolic compounds. In Plant Physiological Aspects of Phenolic Compounds; IntechOpen: Rijeka, Croatia, 2019; pp. 35–48. [Google Scholar]
  9. Mutha, R.E.; Anilkumar, U.T.; Surana, S.J. Flavonoids as natural phenolic compounds and their role in therapeutics: An overview. Future J. Pharm. Sci. 2021, 7, 25. [Google Scholar] [CrossRef]
  10. Kurepa, J.; Shull, T.E.; Karunadasa, S.S.; Smalle, J.A. Modulation of auxin and cytokinin responses by early steps of the phenylpropanoid pathway. BMC Plant Biol. 2018, 18, 278. [Google Scholar] [CrossRef] [Green Version]
  11. Shomali, A.; Das, S.; Arif, N.; Sarraf, M.; Zahra, N.; Yadav, V.; Aliniaeifard, S.; Chauhan, D.K.; Hasanuzzaman, M. Diverse physiological roles of flavonoids in plant environmental stress responses and tolerance. Plants 2022, 11, 3158. [Google Scholar] [CrossRef]
  12. Agati, G.; Azzarello, E.; Pollastri, S.; Tattini, M. Flavonoids as antioxidants in plants: Location and functional significance. Plant Sci. 2012, 196, 67–76. [Google Scholar] [CrossRef]
  13. Cho, J.S.; Nguyen, V.P.; Jeon, H.W.; Kim, M.H.; Eom, S.H.; Lim, Y.J.; Kim, W.C.; Park, E.J.; Choi, Y.I.; Ko, J.H. Overexpression of PtrMYB119, a R2R3-MYB transcription factor from Populus trichocarpa, promotes anthocyanin production in hybrid poplar. Tree Physiol. 2016, 36, 1162–1176. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  14. Hodges, D.M.; Toivonen, P.M. Quality of fresh-cut fruits and vegetables as affected by exposure to abiotic stress. Postharvest Biol. Technol. 2008, 48, 155–162. [Google Scholar] [CrossRef]
  15. Zafari, S.; Sharifi, M.; Ahmadian Chashmi, N.; Mur, L.A. Modulation of Pb-induced stress in Prosopis shoots through an interconnected network of signaling molecules, phenolic compounds and amino acids. Plant Physiol. Biochem. 2016, 99, 11–20. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  16. Dehghanian, Z.; Habibi, K.; Dehghanian, M.; Aliyar, S.; Lajayer, B.A.; Astatkie, T.; Minkina, T.; Keswani, C. Reinforcing the bulwark: Unravelling the efficient applications of plant phenolics and tannins against environmental stresses. Heliyon 2022, 8, e09094. [Google Scholar] [CrossRef]
  17. Uchida, K.; Sawada, Y.; Ochiai, K.; Sato, M.; Inaba, J.; Hirai, M.Y. Identification of a Unique Type of Isoflavone O-Methyltransferase, GmIOMT1, Based on Multi-Omics Analysis of Soybean under Biotic Stress. Plant Cell Physiol. 2020, 61, 1974–1985. [Google Scholar] [CrossRef]
  18. Chowdhary, V.; Alooparampil, S.; Pandya, R.V.; Tank, J.G. Physiological function of phenolic compounds in plant defense system. In Phenolic Compounds: Chemistry, Synthesis, Diversity, Non-Conventional Industrial, Pharmaceutical and Therapeutic Applications; IntechOpen: Rijeka, Croatia, 2021. [Google Scholar]
  19. Zhang, H.; Troise, A.D.; Qi, Y.; Wu, G.; Zhang, H.; Fogliano, V. Insoluble dietary fibre scavenges reactive carbonyl species under simulated physiological conditions: The key role of fibre-bound polyphenols. Food Chem. 2021, 349, 129018. [Google Scholar] [CrossRef]
  20. Sakihama, Y.; Cohen, M.F.; Grace, S.C.; Yamasaki, H. Plant phenolic antioxidant and prooxidant activities: Phenolics-induced oxidative damage mediated by metals in plants. Toxicology 2002, 177, 67–80. [Google Scholar] [CrossRef]
  21. Aboul-Enein, H.Y.; Kruk, I.; Kładna, A.; Lichszteld, K.; Michalska, T. Scavenging effects of phenolic compounds on reactive oxygen species. Biopolymers 2007, 86, 222–230. [Google Scholar] [CrossRef]
  22. Zhu, Q.; Zheng, Z.-P.; Cheng, K.-W.; Wu, J.-J.; Zhang, S.; Tang, Y.S.; Sze, K.-H.; Chen, J.; Chen, F.; Wang, M. Natural polyphenols as direct trapping agents of lipid peroxidation-derived acrolein and 4-hydroxy-trans-2-nonenal. Chem. Res. Toxicol. 2009, 22, 1721–1727. [Google Scholar] [CrossRef]
  23. Colzani, M.; Regazzoni, L.; Criscuolo, A.; Baron, G.; Carini, M.; Vistoli, G.; Lee, Y.-M.; Han, S.-I.; Aldini, G.; Yeum, K.-J. Isotopic labelling for the characterisation of HNE-sequestering agents in plant-based extracts and its application for the identification of anthocyanidins in black rice with giant embryo. Free Rad. Res. 2018, 52, 896–906. [Google Scholar] [CrossRef]
  24. Naikoo, M.I.; Dar, M.I.; Raghib, F.; Jaleel, H.; Ahmad, B.; Raina, A.; Khan, F.A.; Naushin, F. Role and Regulation of Plants Phenolics in Abiotic Stress Tolerance: An Overview. In Plant Signaling Molecules; Elsevier: Amsterdam, The Netherlands, 2019; pp. 157–168. [Google Scholar]
  25. Nakabayashi, R.; Yonekura-Sakakibara, K.; Urano, K.; Suzuki, M.; Yamada, Y.; Nishizawa, T.; Matsuda, F.; Kojima, M.; Sakakibara, H.; Shinozaki, K.; et al. Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. Plant J. 2014, 77, 367–379. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  26. Rezayian, M.; Niknam, V.; Ebrahimzadeh, H. Differential responses of phenolic compounds of Brassica napus under drought stress. Iran. J. Plant Physiol. 2018, 8, 2417–2425. [Google Scholar]
  27. Li, M.; Li, Y.; Zhang, W.; Li, S.; Gao, Y.; Ai, X.; Zhang, D.; Liu, B.; Li, Q. Metabolomics analysis reveals that elevated atmospheric CO2 alleviates drought stress in cucumber seedling leaves. Anal. Biochem. 2018, 559, 71–85. [Google Scholar] [CrossRef]
  28. André, C.M.; Schafleitner, R.; Legay, S.; Lefèvre, I.; Aliaga, C.A.A.; Nomberto, G.; Hoffmann, L.; Hausman, J.-F.; Larondelle, Y.; Evers, D. Gene expression changes related to the production of phenolic compounds in potato tubers grown under drought stress. Phytochemistry 2009, 70, 1107–1116. [Google Scholar] [CrossRef] [PubMed]
  29. Wang, N.; Liu, W.; Yu, L.; Guo, Z.; Chen, Z.; Jiang, S.; Xu, H.; Fang, H.; Wang, Y.; Zhang, Z.; et al. HEAT SHOCK FACTOR A8a modulates flavonoid synthesis and drought tolerance. Plant Physiol. 2020, 184, 1273–1290. [Google Scholar] [CrossRef]
  30. Kovinich, N.; Kayanja, G.; Chanoca, A.; Otegui, M.S.; Grotewold, E. Abiotic stresses induce different localizations of anthocyanins in Arabidopsis. Plant Signal. Behav. 2015, 10, e1027850. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  31. Silva, F.L.B.; Vieira, L.G.E.; Ribas, A.F.; Moro, A.L.; Neris, D.M.; Pacheco, A.C. Proline accumulation induces the production of total phenolics in transgenic tobacco plants under water deficit without increasing the G6PDH activity. Theor. Exp. Plant Physiol. 2018, 30, 251–260. [Google Scholar] [CrossRef]
  32. Ghasemi Pirbalouti, A.; Malekpoor, F.; Salimi, A.; Golparvar, A. Exogenous application of chitosan on biochemical and physiological characteristics, phenolic content and antioxidant activity of two species of basil (Ocimum ciliatum and Ocimum basilicum) under reduced irrigation. Sci. Hortic. 2017, 217, 114–122. [Google Scholar] [CrossRef]
  33. Griesser, M.; Weingart, G.; Schoedl-Hummel, K.; Neumann, N.; Becker, M.; Varmuza, K.; Liebner, F.; Schuhmacher, R.; Forneck, A. Severe drought stress is affecting selected primary metabolites, polyphenols, and volatile metabolites in grapevine leaves (Vitis vinifera cv. Pinot noir). Plant Physiol. Biochem. 2015, 88, 17–26. [Google Scholar] [CrossRef]
  34. Galieni, A.; Di Mattia, C.; De Gregorio, M.; Speca, S.; Mastrocola, D.; Pisante, M.; Stagnari, F. Effects of nutrient deficiency and abiotic environmental stresses on yield, phenolic compounds and antiradical activity in lettuce (Lactuca sativa L.). Sci. Hortic. 2015, 187, 93–101. [Google Scholar] [CrossRef]
  35. Khalil, N.; Fekry, M.; Bishr, M.; El-Zalabani, S.; Salama, O. Foliar spraying of salicylic acid induced accumulation of phenolics, increased radical scavenging activity and modified the composition of the essential oil of water stressed Thymus vulgaris L. Plant Physiol. Biochem. 2018, 123, 65–74. [Google Scholar] [CrossRef] [PubMed]
  36. Garcia-Calderon, M.; Pons-Ferrer, T.; Mrazova, A.; Pal’ove-Balang, P.; Vilkova, M.; Perez-Delgado, C.M.; Vega, J.M.; Eliasova, A.; Repcak, M.; Marquez, A.J.; et al. Modulation of phenolic metabolism under stress conditions in a Lotus japonicus mutant lacking plastidic glutamine synthetase. Front. Plant Sci. 2015, 6, 760. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  37. Hodaei, M.; Rahimmalek, M.; Arzani, A.; Talebi, M. The effect of water stress on phytochemical accumulation, bioactive compounds and expression of critical genes involved in flavonoid biosynthesis in Chrysanthemum morifolium L. Ind. Crops Prod. 2018, 120, 295–304. [Google Scholar] [CrossRef]
  38. Alvarez, S.; Marsh, E.L.; Schroeder, S.G.; Schachtman, D.P. Metabolomic and proteomic changes in the xylem sap of maize under drought. Plant Cell Environ. 2008, 31, 325–340. [Google Scholar] [CrossRef]
  39. Anjum, S.A.; Ashraf, U.; Tanveer, M.; Khan, I.; Hussain, S.; Shahzad, B.; Zohaib, A.; Abbas, F.; Saleem, M.F.; Ali, I.; et al. Drought Induced Changes in Growth, Osmolyte Accumulation and Antioxidant Metabolism of Three Maize Hybrids. Front. Plant Sci. 2017, 8, 69. [Google Scholar] [CrossRef] [Green Version]
  40. Quan, N.T.; Anh, L.H.; Khang, D.T.; Tuyen, P.T.; Toan, N.P.; Minh, T.N.; Minh, L.T.; Bach, D.T.; Ha, P.T.T.; Elzaawely, A.A.; et al. Involvement of Secondary Metabolites in Response to Drought Stress of Rice (Oryza sativa L.). Agriculture 2016, 6, 23. [Google Scholar] [CrossRef] [Green Version]
  41. Acosta-Motos, J.R.; Ortuño, M.F.; Bernal-Vicente, A.; Diaz-Vivancos, P.; Sanchez-Blanco, M.J.; Hernandez, J.A. Plant Responses to Salt Stress: Adaptive Mechanisms. Agronomy 2017, 7, 18. [Google Scholar] [CrossRef] [Green Version]
  42. Chen, S.; Wu, F.; Li, Y.; Qian, Y.; Pan, X.; Li, F.; Wang, Y.; Wu, Z.; Fu, C.; Lin, H.; et al. NtMYB4 and NtCHS1 Are Critical Factors in the Regulation of Flavonoid Biosynthesis and Are Involved in Salinity Responsiveness. Front. Plant Sci. 2019, 10, 178. [Google Scholar] [CrossRef]
  43. Bistgani, Z.E.; Hashemi, M.; DaCosta, M.; Craker, L.; Maggi, F.; Morshedloo, M.R. Effect of salinity stress on the physiological characteristics, phenolic compounds and antioxidant activity of Thymus vulgaris L.; Thymus daenensis Celak. Ind. Crops Prod. 2019, 135, 311–320. [Google Scholar] [CrossRef]
  44. Valifard, M.; Mohsenzadeh, S.; Kholdebarin, B.; Rowshan, V. Effects of salt stress on volatile compounds, total phenolic content and antioxidant activities of Salvia mirzayanii. S. Afr. J. Bot. 2014, 93, 92–97. [Google Scholar] [CrossRef]
  45. Rossi, L.; Borghi, M.; Francini, A.; Lin, X.; Xie, D.Y.; Sebastiani, L. Salt stress induces differential regulation of the phenylpropanoid pathway in Olea europaea cultivars Frantoio (salt-tolerant) and Leccino (salt-sensitive). J. Plant Physiol. 2016, 204, 8–15. [Google Scholar] [CrossRef]
  46. Al-Ghamdi, A.A.; Elansary, H.O. Synergetic effects of 5-aminolevulinic acid and Ascophyllum nodosum seaweed extracts on Asparagus phenolics and stress related genes under saline irrigation. Plant Physiol. Biochem. 2018, 129, 273–284. [Google Scholar] [CrossRef]
  47. Guo, H.; Chen, H.; Hong, C.; Jiang, D.; Zheng, B. Exogenous malic acid alleviates cadmium toxicity in Miscanthus sacchariflorus through enhancing photosynthetic capacity and restraining ROS accumulation. Ecotoxicol. Environ. Saf. 2017, 141, 119–128. [Google Scholar] [CrossRef]
  48. Navarro, J.M.; Flores, P.; Garrido, C.; Martinez, V. Changes in the contents of antioxidant compounds in pepper fruits at ripening stages, as affected by salinity. Food Chem. 2006, 96, 66–73. [Google Scholar] [CrossRef]
  49. Golkar, P.; Taghizadeh, M. In vitro evaluation of phenolic and osmolite compounds, ionic content, and antioxidant activity in safflower (Carthamus tinctorius L.) under salinity stress. Plant Cell Tiss. Org. Cult. 2018, 134, 357–368. [Google Scholar] [CrossRef]
  50. Wang, F.; Zhu, H.; Chen, D.; Li, Z.; Peng, R.; Yao, Q. A grape bHLH transcription factor gene, VvbHLH1, increases the accumulation of flavonoids and enhances salt and drought tolerance in transgenic Arabidopsis thaliana. Plant Cell Tiss. Org. Cult. 2016, 125, 387–398. [Google Scholar] [CrossRef]
  51. Yan, J.; Wang, B.; Jiang, Y.; Cheng, L.; Wu, T. GmFNSII-controlled soybean flavone metabolism responds to abiotic stresses and regulates plant salt tolerance. Plant Cell Physiol. 2014, 55, 74–86. [Google Scholar] [CrossRef] [Green Version]
  52. Dkhil, B.B.; Denden, M. Effect of salt stress on growth, anthocyanins, membrane permeability and chlorophyll fluorescence of Okra (Abelmoschus esculentus L.) seedlings. Am. J. Plant Physiol. 2012, 7, 174–183. [Google Scholar] [CrossRef] [Green Version]
  53. Daayf, F.; Lattanzio, V. Recent Advances in Polyphenol Research; John Wiley & Sons: Hoboken, NJ, USA, 2009. [Google Scholar]
  54. Lucini, L.; Borgognone, D.; Rouphael, Y.; Cardarelli, M.; Bernardi, J.; Colla, G. Mild Potassium Chloride Stress Alters the Mineral Composition, Hormone Network, and Phenolic Profile in Artichoke Leaves. Front. Plant Sci. 2016, 7, 948. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  55. Scagel, C.F.; Lee, J.; Mitchell, J.N. Salinity from NaCl changes the nutrient and polyphenolic composition of basil leaves. Ind. Crops Prod. 2019, 127, 119–128. [Google Scholar] [CrossRef]
  56. Kaur, L.; Zhawar, V.K. Phenolic parameters under exogenous ABA, water stress, salt stress in two wheat cultivars varying in drought tolerance. Ind. J. Plant Physiol. 2015, 20, 151–156. [Google Scholar] [CrossRef]
  57. Ma, Y.; Wang, P.; Gu, Z.; Tao, Y.; Shen, C.; Zhou, Y.; Han, Y.; Yang, R. Ca2+ involved in GABA signal transduction for phenolics accumulation in germinated hulless barley under NaCl stress. Food Chem. X 2019, 2, 100023. [Google Scholar] [CrossRef] [PubMed]
  58. Çoban, Ö.; Göktürk Baydar, N. Brassinosteroid effects on some physical and biochemical properties and secondary metabolite accumulation in peppermint (Mentha piperita L.) under salt stress. Ind. Crops Prod. 2016, 86, 251–258. [Google Scholar] [CrossRef]
  59. Martinez, V.; Mestre, T.C.; Rubio, F.; Girones-Vilaplana, A.; Moreno, D.A.; Mittler, R.; Rivero, R.M. Accumulation of Flavonols over Hydroxycinnamic Acids Favors Oxidative Damage Protection under Abiotic Stress. Front. Plant Sci. 2016, 7, 838. [Google Scholar] [CrossRef] [Green Version]
  60. De Azevedo Neto, A.D.; Prisco, J.T.; Enéas-Filho, J.; Abreu, C.E.B.D.; Gomes-Filho, E. Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ. Exp. Bot. 2006, 56, 87–94. [Google Scholar] [CrossRef]
  61. Ma, X.; Xia, H.; Liu, Y.; Wei, H.; Zheng, X.; Song, C.; Chen, L.; Liu, H.; Luo, L. Transcriptomic and metabolomic studies disclose key metabolism pathways contributing to well-maintained photosynthesis under the drought and the consequent drought-tolerance in rice. Front. Plant Sci. 2016, 7, 1886. [Google Scholar] [CrossRef] [Green Version]
  62. Minh, L.T.; Khang, D.T.; Ha, P.T.T.; Tuyen, P.T.; Minh, T.N.; Quan, N.V.; Xuan, T.D. Effects of salinity stress on growth and phenolics of rice (Oryza sativa L.). Int. Lett. Nat. Sci. 2016, 57, 1–10. [Google Scholar] [CrossRef]
  63. Shahzad, B.; Tanveer, M.; Che, Z.; Rehman, A.; Cheema, S.A.; Sharma, A.; Song, H.; Ur Rehman, S.; Zhaorong, D. Role of 24-epibrassinolide (EBL) in mediating heavy metal and pesticide induced oxidative stress in plants: A review. Ecotoxicol. Environ. Saf. 2018, 147, 935–944. [Google Scholar] [CrossRef]
  64. Pandey, N.; Sharma, C.P. Effect of heavy metals Co2+, Ni2+ and Cd2+ on growth and metabolism of cabbage. Plant Sci. 2002, 163, 753–758. [Google Scholar] [CrossRef]
  65. Villiers, F.; Ducruix, C.; Hugouvieux, V.; Jarno, N.; Ezan, E.; Garin, J.; Junot, C.; Bourguignon, J. Investigating the plant response to cadmium exposure by proteomic and metabolomic approaches. Proteomics 2011, 11, 1650–1663. [Google Scholar] [CrossRef] [PubMed]
  66. Mira, L.; Fernandez, M.T.; Santos, M.; Rocha, R.; Florencio, M.H.; Jennings, K.R. Interactions of flavonoids with iron and copper ions: A mechanism for their antioxidant activity. Free Radic. Res. 2002, 36, 1199–1208. [Google Scholar] [CrossRef] [PubMed]
  67. Williams, R.J.; Spencer, J.P.; Rice-Evans, C. Flavonoids: Antioxidants or signalling molecules? Free. Radic. Biol. Med. 2004, 36, 838–849. [Google Scholar] [CrossRef] [PubMed]
  68. Trejo-Tapia, G.; Jimenez-Aparicio, A.; Rodriguez-Monroy, M.; De Jesus-Sanchez, A.; Gutierrez-Lopez, G. Influence of cobalt and other microelements on the production of betalains and the growth of suspension cultures of Beta vulgaris. Plant Cell Tiss. Org. Cult. 2001, 67, 19–23. [Google Scholar] [CrossRef]
  69. Kısa, D.; Elmasta¸s, M.; Öztürk, L.; Kayır, Ö. Responses of the phenolic compounds of Zea mays under heavy metal stress. Appl. Biol. Chem. 2016, 59, 813–820. [Google Scholar] [CrossRef]
  70. Kováčik, J.; Klejdus, B.; Hedbavny, J.; Štork, F.; Bačkor, M. Comparison of cadmium and copper effect on phenolic metabolism, mineral nutrients and stress-related parameters in Matricaria chamomilla plants. Plant Soil 2009, 320, 231. [Google Scholar] [CrossRef]
  71. Jańczak-Pieniążek, M.; Cichoński, J.; Michalik, P.; Chrzanowski, G. Effect of Heavy Metal Stress on Phenolic Compounds Accumulation in Winter Wheat Plants. Molecules 2023, 28, 241. [Google Scholar] [CrossRef]
  72. Fraser, C.M.; Chapple, C. The phenylpropanoid pathway in Arabidopsis. Arab. Book 2011, 9, e0152. [Google Scholar] [CrossRef] [Green Version]
  73. Vogt, T. Phenylpropanoid biosynthesis. Mol. Plant 2010, 3, 2–20. [Google Scholar] [CrossRef] [Green Version]
  74. Dutta, S.; Mitra, M.; Agarwal, P.; Mahapatra, K.; De, S.; Sett, U.; Roy, S. Oxidative and genotoxic damages in plants in response to heavy metal stress and maintenance of genome stability. Plant Signal. Behav. 2018, 13, e1460048. [Google Scholar] [CrossRef] [Green Version]
  75. Castellarin, S.D.; Pfeiffer, A.; Sivilotti, P.; Degan, M.; Peterlunger, E.; Di Gaspero, G. Transcriptional regulation of anthocyanin biosynthesis in ripening fruits of grapevine under seasonal water deficit. Plant Cell Environ. 2007, 30, 1381–1399. [Google Scholar] [CrossRef] [Green Version]
  76. Taïbi, K.; Taïbi, F.; Ait Abderrahim, L.; Ennajah, A.; Belkhodja, M.; Mulet, J.M. Effect of salt stress on growth, chlorophyll content, lipid peroxidation and antioxidant defence systems in Phaseolus vulgaris L. S. Afr. J. Bot. 2016, 105, 306–312. [Google Scholar] [CrossRef]
  77. Agati, G.; Tattini, M. Multiple functional roles of flavonoids in photoprotection. New Phytol. 2010, 186, 786–793. [Google Scholar] [CrossRef]
  78. Landi, M.; Tattini, M.; Gould, K.S. Multiple functional roles of anthocyanins in plant-environment interactions. Environ. Exp. Bot. 2015, 119, 4–17. [Google Scholar] [CrossRef]
  79. Lattanzio, V. Phenolic Compounds: Introduction. In Natural Products: Phytochemistry, Botany and Metabolism of Alkaloids, Phenolics and Terpenes; Ramawat, K.G., Mérillon, J.-M., Eds.; Springer: Berlin/Heidelberg, Germany, 2013; pp. 1543–1580. [Google Scholar]
  80. Kolb, C.A.; Kaser, M.A.; Kopecky, J.; Zotz, G.; Riederer, M.; Pfundel, E.E. Effects of natural intensities of visible and ultraviolet radiation on epidermal ultraviolet screening and photosynthesis in grape leaves. Plant. Physiol. 2001, 127, 863–875. [Google Scholar] [CrossRef]
  81. Ghasemi, S.; Kumleh, H.H.; Kordrostami, M. Changes in the expression of some genes involved in the biosynthesis of secondary metabolites in Cuminum cyminum L. under UV stress. Protoplasma 2019, 256, 279–290. [Google Scholar] [CrossRef] [PubMed]
  82. Del Valle, J.C.; Buide, M.L.; Whittall, J.B.; Valladares, F.; Narbona, E. UV radiation increases phenolic compound protection but decreases reproduction in Silene littorea. PLoS ONE 2020, 15, e0231611. [Google Scholar] [CrossRef] [PubMed]
  83. Goyal, A.; Siddiqui, S.; Upadhyay, N.; Soni, J. Effects of ultraviolet irradiation, pulsed electric field, hot water and ethanol vapours treatment on functional properties of mung bean sprouts. J. Food Sci. Technol. 2014, 51, 708–714. [Google Scholar] [CrossRef] [Green Version]
  84. Xu, Y.; Charles, M.T.; Luo, Z.; Mimee, B.; Veronneau, P.Y.; Rolland, D.; Roussel, D. Preharvest Ultraviolet C Irradiation Increased the Level of Polyphenol Accumulation and Flavonoid Pathway Gene Expression in Strawberry Fruit. J. Agric. Food Chem. 2017, 65, 9970–9979. [Google Scholar] [CrossRef]
  85. Bi, X.; Zhang, J.; Chen, C.; Zhang, D.; Li, P.; Ma, F. Anthocyanin contributes more to hydrogen peroxide scavenging than other phenolics in apple peel. Food Chem. 2014, 152, 205–209. [Google Scholar] [CrossRef]
  86. Demkura, P.V.; Abdala, G.; Baldwin, I.T.; Ballare, C.L. Jasmonate-dependent and -independent pathways mediate specific effects of solar ultraviolet B radiation on leaf phenolics and antiherbivore defense. Plant Physiol. 2010, 152, 1084–1095. [Google Scholar] [CrossRef] [Green Version]
  87. Berli, F.J.; Fanzone, M.; Piccoli, P.; Bottini, R. Solar UV-B and ABA are involved in phenol metabolism of Vitis vinifera L. increasing biosynthesis of berry skin polyphenols. J. Agric. Food Chem. 2011, 59, 4874–4884. [Google Scholar] [CrossRef] [PubMed]
  88. Moreira-Rodriguez, M.; Nair, V.; Benavides, J.; Cisneros-Zevallos, L.; Jacobo-Velazquez, D.A. UVA, UVB Light, and Methyl Jasmonate, Alone or Combined, Redirect the Biosynthesis of Glucosinolates, Phenolics, Carotenoids, and Chlorophylls in Broccoli sprouts. Int. J. Mol. Sci. 2017, 18, 2330. [Google Scholar] [CrossRef] [Green Version]
  89. Mariz-Ponte, N.; Mendes, R.J.; Sario, S.; De Oliveira, J.F.; Melo, P.; Santos, C. Tomato plants use non-enzymatic antioxidant pathways to cope with moderate UV-A/B irradiation: A contribution to the use of UV-A/B in horticulture. J. Plant Physiol. 2018, 221, 32–42. [Google Scholar] [CrossRef] [PubMed]
  90. Alonso, R.; Berli, F.J.; Fontana, A.; Piccoli, P.; Bottini, R. Malbec grape (Vitis vinifera L.) responses to the environment: Berry phenolics as influenced by solar UV-B, water deficit and sprayed abscisic acid. Plant Physiol. Biochem. 2016, 109, 84–90. [Google Scholar] [CrossRef] [PubMed]
  91. Chen, Z.; Ma, Y.; Weng, Y.; Yang, R.; Gu, Z.; Wang, P. Effects of UV-B radiation on phenolic accumulation, antioxidant activity and physiological changes in wheat (Triticum aestivum L.) seedlings. Food Biosci. 2019, 30, 100409. [Google Scholar] [CrossRef]
  92. Chen, Z.; Ma, Y.; Yang, R.; Gu, Z.; Wang, P. Effects of exogenous Ca2+ on phenolic accumulation and physiological changes in germinated wheat (Triticum aestivum L.) under UV-B radiation. Food Chem. 2019, 288, 368–376. [Google Scholar] [CrossRef]
  93. Huyskens-Keil, S.; Eichholz, I.; Kroh, L.; Rohn, S. UV-B induced changes of phenol composition and antioxidant activity in black currant fruit (Ribes nigrum L.). J. App. Bot. Food Qual. 2012, 81, 140–144. [Google Scholar]
  94. Nascimento, L.; Leal-Costa, M.V.; Menezes, E.A.; Lopes, V.R.; Muzitano, M.F.; Costa, S.S.; Tavares, E.S. Ultraviolet-B radiation effects on phenolic profile and flavonoid content of Kalanchoe pinnata. J. Photochem. Photobiol. B 2015, 148, 73–81. [Google Scholar] [CrossRef]
  95. Liu, M.; Cao, B.; Zhou, S.; Liu, Y. Responses of the flavonoid pathway to UV-B radiation stress and the correlation with the lipid antioxidant characteristics in the desert plant Caryopteris mongolica. Acta Ecol. Sin. 2012, 32, 150–155. [Google Scholar] [CrossRef]
  96. Thomas, D.T.T.; Jos, T.P. UV radiation priming: A means of amplifying the inherent potential for abiotic stress tolerance in crop plants. Environ. Exp. Bot. 2017, 138, 57–66. [Google Scholar] [CrossRef]
  97. Reddy, V.S.; Goud, K.V.; Sharma, R.; Reddy, A.R. Ultraviolet-B-responsive anthocyanin production in a rice cultivar is associated with a specific phase of phenylalanine ammonia lyase biosynthesis. Plant Physiol. 1994, 105, 1059–1066. [Google Scholar] [CrossRef] [Green Version]
  98. Jan, R.; Khan, M.-A.; Asaf, S.; Lubna; Waqas, M.; Park, J.-R.; Asif, S.; Kim, N.; Lee, I.-J.; Kim, K.-M. Drought and UV Radiation Stress Tolerance in Rice Is Improved by Over accumulation of Non-Enzymatic Antioxidant Flavonoids. Antioxidants 2022, 11, 917. [Google Scholar] [CrossRef] [PubMed]
  99. Sharma, A.; Yuan, H.; Kumar, V.; Ramakrishnan, M.; Kohli, S.K.; Kaur, R.; Thukral, A.K.; Bhardwaj, R.; Zheng, B. Castasterone attenuates insecticide induced phytotoxicity in mustard. Ecotoxicol. Environ. Saf. 2019, 179, 50–61. [Google Scholar] [CrossRef]
  100. Ancillotti, C.; Bogani, P.; Biricolti, S.; Calistri, E.; Checchini, L.; Ciofi, L.; Gonnelli, C.; Del Bubba, M. Changes in polyphenol and sugar concentrations in wild type and genetically modified Nicotiana langsdorffii Weinmann in response to water and heat stress. Plant Physiol. Biochem. 2015, 97, 52–61. [Google Scholar] [CrossRef]
  101. Wang, L.; Shan, T.; Xie, B.; Ling, C.; Shao, S.; Jin, P.; Zheng, Y. Glycine betaine reduces chilling injury in peach fruit by enhancing phenolic and sugar metabolisms. Food Chem. 2019, 272, 530–538. [Google Scholar] [CrossRef]
  102. Zlotek, U.; Szymanowska, U.; Baraniak, B.; Karas, M. Antioxidant activity of polyphenols of adzuki bean (Vigna angularis) germinated in abiotic stress conditions. Acta Sci. Pol. Technol. Aliment. 2015, 14, 55–63. [Google Scholar] [CrossRef] [Green Version]
  103. Sharma, A.; Kumar, V.; Thukral, A.K.; Bhardwaj, R. Epibrassinolide-imidacloprid interaction enhances non-enzymatic antioxidants in Brassica juncea L. Ind. J. Plant Physiol. 2016, 21, 70–75. [Google Scholar] [CrossRef]
  104. Sharma, A.; Thakur, S.; Kumar, V.; Kanwar, M.K.; Kesavan, A.K.; Thukral, A.K.; Bhardwaj, R.; Alam, P.; Ahmad, P. Pre-sowing Seed Treatment with 24-Epibrassinolide Ameliorates Pesticide Stress in Brassica juncea L. through the Modulation of Stress Markers. Front. Plant Sci. 2016, 7, 1569. [Google Scholar] [CrossRef] [Green Version]
  105. Wang, J.; Yuan, B.; Huang, B. Differential Heat-Induced Changes in Phenolic Acids Associated with Genotypic Variations in Heat Tolerance for Hard Fescue. Crop. Sci. 2019, 59, 667–674. [Google Scholar] [CrossRef]
  106. Cingoz, G.S.; Gurel, E. Effects of salicylic acid on thermotolerance and cardenolide accumulation under high-temperature stress in Digitalis trojana Ivanina. Plant Physiol. Biochem. 2016, 105, 145–149. [Google Scholar] [CrossRef] [PubMed]
  107. Drobek, M.; Frąc, M.; Cybulska, J. Plant biostimulants: Importance of the quality and yield of horticultural crops and the improvement of plant tolerance to abiotic stress—A review. Agronomy 2019, 9, 335. [Google Scholar] [CrossRef] [Green Version]
  108. Zarzecka, K.; Gugała, M.; Sikorska, A.; Mystkowska, I.; Baranowska, A.; Niewęgłowski, M.; Dołęga, H. The effect of herbicides and biostimulants on polyphenol content of potato (Solanum tuberosum L.) tubers and leaves. J. Saudi Soc. Agri. Sci. 2019, 18, 102–106. [Google Scholar] [CrossRef]
  109. Zuzunaga-Rosas, J.; González-Orenga, S.; Tofei, A.M.; Boscaiu, M.; Moreno-Ramón, H.; Ibáñez-Asensio, S.; Vicente, O. Effect of a biostimulant based on polyphenols and glycine betaine on tomato plants’ responses to salt stress. Agronomy 2022, 12, 2142. [Google Scholar] [CrossRef]
  110. Frioni, T.; Sabbatini, P.; Tombesi, S.; Norrie, J.; Poni, S.; Gatti, M.; Palliotti, A. Effects of a Biostimulant Derived from the Brown Seaweed Ascophyllum Nodosum on Ripening Dynamics and Fruit Quality of Grapevines. Sci. Hortic. 2018, 232, 97–106. [Google Scholar] [CrossRef]
  111. Rouphael, Y.; Colla, G.; Giordano, M.; El-Nakhel, C.; Kyriacou, M.C.; De Pascale, S. Foliar Applications of a Legume-Derived Protein Hydrolysate Elicit Dose-Dependent Increases of Growth, Leaf Mineral Composition, Yield and Fruit Quality in Two Greenhouse Tomato Cultivars. Sci. Hortic. 2017, 226, 353–360. [Google Scholar] [CrossRef]
Stresses 03 00040 g001
Figure 1. Structural representation of the phenolic compounds.
Figure 1. Structural representation of the phenolic compounds.
Stresses 03 00040 g001
Stresses 03 00040 g002
Figure 2. Structural representation of the major flavonoid classes.
Figure 2. Structural representation of the major flavonoid classes.
Stresses 03 00040 g002
Stresses 03 00040 g003
Figure 3. Schematic representation of the flavonoids and their intermediates (shikimate, phenylpropanoid, flavanones, flavanols, flavan-3-ol, flavanol glycosides, anthocyanidins and anthocyanin biosynthetic pathway). The respective enzymes catalyzing the reaction in each pathway have been denoted in red colour. Abbreviation: 3-deoxy-D-arabinoheptulosonic acid-7-phosphate synthase (DAHPS); 3-dehydroquinate synthase (DHQS); 3-dehydroquinate dehydratase (DHD); Shikimate kinase (SK); chorismate synthase (CS); shikimate dehydrogenase (SDH), UDP-3-glucosyltransferase (UGT); Phenylalanine ammonia lyase (PAL); cinnamate-4-hydroxylase (C4H); 4-coumarate-CoA ligase (4CL); coumaryol-3-hydroxylase (C3H); Caffeoyl-O-methyltransferase (COMT); Chalcone synthase (CHS); Hydroxycinnamoyl-CoA: skimimate/quinate hydroxycinnamoyltransferase (HCT); hydroxycinnamoyl (CoA); quinate hydroxycinnamoyl transferase (HQT); chalcone-flavanone isomerase (CHI); fatty alcohol hydroxycinnamoyl transferase (FHT); flavonoid 3′,5′-hydroxylase (F3′5′H); flavonol 3′ hydroxylase (F3′H); dihydroflavonol 4-reductase (DFR); flavonol synthase (FLS); anthocyanidin synthase (ANS); anthocyanidin reductase (ANR); leucocyanidin reductase (LAR); flavonoid-3-O-glucosyltransferase (GT).
Figure 3. Schematic representation of the flavonoids and their intermediates (shikimate, phenylpropanoid, flavanones, flavanols, flavan-3-ol, flavanol glycosides, anthocyanidins and anthocyanin biosynthetic pathway). The respective enzymes catalyzing the reaction in each pathway have been denoted in red colour. Abbreviation: 3-deoxy-D-arabinoheptulosonic acid-7-phosphate synthase (DAHPS); 3-dehydroquinate synthase (DHQS); 3-dehydroquinate dehydratase (DHD); Shikimate kinase (SK); chorismate synthase (CS); shikimate dehydrogenase (SDH), UDP-3-glucosyltransferase (UGT); Phenylalanine ammonia lyase (PAL); cinnamate-4-hydroxylase (C4H); 4-coumarate-CoA ligase (4CL); coumaryol-3-hydroxylase (C3H); Caffeoyl-O-methyltransferase (COMT); Chalcone synthase (CHS); Hydroxycinnamoyl-CoA: skimimate/quinate hydroxycinnamoyltransferase (HCT); hydroxycinnamoyl (CoA); quinate hydroxycinnamoyl transferase (HQT); chalcone-flavanone isomerase (CHI); fatty alcohol hydroxycinnamoyl transferase (FHT); flavonoid 3′,5′-hydroxylase (F3′5′H); flavonol 3′ hydroxylase (F3′H); dihydroflavonol 4-reductase (DFR); flavonol synthase (FLS); anthocyanidin synthase (ANS); anthocyanidin reductase (ANR); leucocyanidin reductase (LAR); flavonoid-3-O-glucosyltransferase (GT).
Stresses 03 00040 g003
Stresses 03 00040 g004
Figure 4. Schematic diagram of the regulation of gene expressions and enzymatic activities involved in the phenolic compound’s biosynthesis against abiotic stress tolerance in plants. Abbreviation: phenylalanine ammonia lyase (PAL); chalcone synthase (CHS); chalcone-flavanone isomerase (CHI); cinnamate-4-hydroxylase (C4H); 4-coumarate-CoA ligase (4CL); 4-coumarate-CoA ligase (4CL); flavonol 3′ hydroxylase (F3′H); flavonoid 3′,5′-hydroxylase (F3′5′H); flavonol synthase (FLS); flavone synthase (FNS); UDP flavonoid glycosyltransferase (UFG); isoflavone synthase (IFS); isoflavone reductase (IFR); dihydroflavonol 4-reductase (DFR); anthocyanidin synthase (ANS).
Figure 4. Schematic diagram of the regulation of gene expressions and enzymatic activities involved in the phenolic compound’s biosynthesis against abiotic stress tolerance in plants. Abbreviation: phenylalanine ammonia lyase (PAL); chalcone synthase (CHS); chalcone-flavanone isomerase (CHI); cinnamate-4-hydroxylase (C4H); 4-coumarate-CoA ligase (4CL); 4-coumarate-CoA ligase (4CL); flavonol 3′ hydroxylase (F3′H); flavonoid 3′,5′-hydroxylase (F3′5′H); flavonol synthase (FLS); flavone synthase (FNS); UDP flavonoid glycosyltransferase (UFG); isoflavone synthase (IFS); isoflavone reductase (IFR); dihydroflavonol 4-reductase (DFR); anthocyanidin synthase (ANS).
Stresses 03 00040 g004
Table 1. The positive impact of drought stress on the endogenous levels of phenolic compounds in different plant species.
Table 1. The positive impact of drought stress on the endogenous levels of phenolic compounds in different plant species.
Plant SpeciesIncreased Endogenous Level of Phenolic CompoundsReferences
Brassica napusTotal phenols, flavonoid and flavonols[26]
Cucumis sativusVanillic acid, 4-hydroxycinnamic acid[27]
Nicotiana tabacumLignin[31]
Ocimum spp.Total phenols[32]
Vitis viniferaPolyphenols (4-coumaric acid, caffeic acid, ferulic acid, cis-resveratrol-3-O-glucoside, caftaric acid, epicatechin gallate, kaempferol-3-O-glucoside, cyanidin-3-O-glucoside)[33]
Lactuca sativaCaftaric acid, rutin[34]
Thymus vulgarisTotal flavonoids, polyphenols[35]
Lotus japonicusKaempferol, quercetin[36]
Chrysanthemum morifoliumTotal phenolics, anthocyanins, chlorogenic acid, luteolin, rutin, ferulic acid, apigenin and quercetin[37]
Zea maysp-coumaric acid and caffeic acid increased[38]
Zea maysTotal phenols[39]
Oryza sativaFlavonoids[25]
Oryza sativaVanillic acid and p-hyroxybenzoic acid[40]
Table 2. Overview of the positive effect of salt stress on the endogenous levels of phenolic compounds in different plant species.
Table 2. Overview of the positive effect of salt stress on the endogenous levels of phenolic compounds in different plant species.
Plant SpeciesIncreased Phenolic CompoundsReferences
Carthamus tinctoriusTotal phenols and flavonoids[47]
Cynara cardunculusLuteolin-O-glucoside, apigenin 6-c-glucoside 8-c-arabinoside, gallocatechin, leucocyanidin, quercitrin[54]
Ocimum basilicumCaffeic acid, caftaric acid, cinnamyl malic acid, feruloyl tartaric acid, quercetin-rutinoside, rosmarinic acid[55]
Triticum aestivumTotal phenols[56]
Hordeum vulgareTotal phenols[57]
Carthamus tinctoriusTotal phenols and flavonoids[50]
Mentha piperitaTotal phenols[58]
Solanum lycopersiconTotal caffeoylquinic acid[59]
Asparagus aethiopicusPhenolics (apigenin, chlorogenic acid, caffeic acid)[52]
Red pepperTotal phenolic compound[48]
Zea maysAnthocyanin[60]
Oryza sativaHydroxycinnamic acid and ferulic acid[61]
Oryza sativaFerulic and p-coumaric acid[62]
Table 3. Outline of the affirmative impact of UV light exposure on phenolic compounds in different plant species.
Table 3. Outline of the affirmative impact of UV light exposure on phenolic compounds in different plant species.
Plant SpeciesIncreased Endogenous Level of Phenolic CompoundsReferences
Brassica oleraceaGallic acid, sinapic acid[88]
Cuminum cyminumTotal phenolics, anthocyanins[81]
Solanum lycopersicumTotal phenolics[89]
Vigna radiataTotal flavonoids and phenols[83]
Vitis viniferaStilbenes, quercetin, kaempferol[90]
Triticum aestivumTotal phenolics, ferulic acid, p-coumaric acid, vanillic acid[91,92]
Ribes nigrumFlavonols, anthocyanins, hydroxycinnamic hydroxybenzoic acids[93]
Kalanchoe pinnataTotal flavonoids, quercitrin[94]
Triticum aestivumTotal phenolics[89]
Caryopteris mongolicaFlavonoids, anthocyanidins[95]
Zea maysAnthocyanin[96]
Oryza sativaAnthocyanin[97]
Oryza sativaKaempferol and quercetin[98]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Kumar, K.; Debnath, P.; Singh, S.; Kumar, N. An Overview of Plant Phenolics and Their Involvement in Abiotic Stress Tolerance. Stresses 2023, 3, 570-585. https://doi.org/10.3390/stresses3030040

AMA Style

Kumar K, Debnath P, Singh S, Kumar N. An Overview of Plant Phenolics and Their Involvement in Abiotic Stress Tolerance. Stresses. 2023; 3(3):570-585. https://doi.org/10.3390/stresses3030040

Chicago/Turabian Style

Kumar, Krishna, Pratima Debnath, Sailendra Singh, and Navin Kumar. 2023. "An Overview of Plant Phenolics and Their Involvement in Abiotic Stress Tolerance" Stresses 3, no. 3: 570-585. https://doi.org/10.3390/stresses3030040

Article Metrics

Back to TopTop