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The Classification, Molecular Structure and Biological Biosynthesis of Flavonoids, and Their Roles in Biotic and Abiotic Stresses

Wei-Bing Zhuang, Yu-Hang Li, Xiao-Chun Shu and 4 more

Molecules · 2023 · Review · CC BY

Abstract

With the climate constantly changing, plants suffer more frequently from various abiotic and biotic stresses. However, they have evolved biosynthetic machinery to survive in stressful environmental conditions. Flavonoids are involved in a variety of biological activities in plants, which can protect plants from different biotic (plant-parasitic nematodes, fungi and bacteria) and abiotic stresses (salt stress, drought stress, UV, higher and lower temperatures). Flavonoids contain several subgroups, including anthocyanidins, flavonols, flavones, flavanols, flavanones, chalcones, dihydrochalcones and dihydroflavonols, which are widely distributed in various plants. As the pathway of flavonoid biosynthesis has been well studied, many researchers have applied transgenic technologies in order to explore the molecular mechanism of genes associated with flavonoid biosynthesis; as such, many transgenic plants have shown a higher stress tolerance through the regulation of flavonoid content. In the present review, the classification, molecular structure and biological biosynthesis of flavonoids were summarized, and the roles of flavonoids under various forms of biotic and abiotic stress in plants were also included. In addition, the effect of applying genes associated with flavonoid biosynthesis on the enhancement of plant tolerance under various biotic and abiotic stresses was also discussed.

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From PubMed Central, U.S. National Library of Medicine, as current on Oct 24, 2026. Paragraph numbers are ours, so an answer can point at one.

1. Introduction

1Flavonoid compounds, one of the main classes of plant secondary metabolites, are commonly present in plants. Over 9000 flavonoid derivatives have been identified in various plants, which are further divided into different subfamilies depending on the modification of their basic structure. Some plant flavonoids may be used as dietary compounds, which can improve human health and prevent many diseases. Based on the epidemiological, clinical and animal studies, flavonoids may exert beneficial effects on human health when an individual is suffering from various diseases, such as cardiovascular disease and cancer.

2Phenolic compounds are a group of metabolites derived from the secondary pathways of plants that contains flavonoids, phenolic acids, tannins, lignans, and coumarins. Among them, flavonoid compounds are naturally distributed in fruits, seeds, flowers and the leaves of plants, and play important roles in regulating the growth and development of plants. Plant flavonoids are involved in pollination, auxin transport inhibition, male fertility, allelopathy, seed development and flower coloring. Moreover, flavonoids have also been reported to play protective roles against abiotic stresses through ROS detoxification, including UV-B radiation, low temperatures, salt, drought, and heavy metal stress. In addition, flavonoids also offer protection against biotic stresses, and are capable of participating in plant–microbe interaction; they are also especially involved in the symbioses of plants with rhizobia and mycorrhizal fungi, as well as in the interactions between pathogenic microorganisms and plants. Some flavonoids (particularly anthocyanins) act as major flower pigments, which help plants attract pollinators.

3Genetically modified (GM) plants are those whose genomes have been modified via the introduction of foreign DNA derived from bacteria, fungi, viruses, or animals; this process has been used to verify the gene function and generate GM plants. Up to now, two common systems have been used for gene transfer in the generation of GM plants: the Agrobacterium-mediated system and the gene-gun-mediated system. With the development of transgenic technology, genetic modification has been widely used to verify the gene functions in the flavonoid biosynthesis pathway, and the roles of flavonoids in plant development and response to (a)biotic stresses.

4Flavonoids have attracted significant attention in recent years. This review summarizes the recent progress made in the research of flavonoids, including their classification, biosynthesis and mechanisms of responding to adversity. Moreover, the application of flavonoids in modern biotechnologies and the prospects of flavonoids in response to various stresses are also reviewed here.

2. Flavonoids Classification

5Flavonoids, a diverse group of natural substances with variable phenolic structures, are widely distributed in plants. So far, over 9000 flavonoids have been identified, which are further classified into seven subgroups depending on the modification of their basic structure; these subgroups include flavones, flavanones, isoflavones, flavonols or catechins, and anthocyanins.

2.1. Flavones

6Flavones, one of the important subgroups of flavonoids, contain the backbone of 2-phenylchromen-4-one (2-phenyl-1-benzopyran-4-one) (Figure 1A), and are widely distributed in leaves, flowers, and fruits of many plants, such as celery, parsley, red pepper, chamomile, mint, and ginkgo. Flavones possess the C2′-C3′ double bond and C-ring, bearing a ketone at position C4′. Most flavones have an A-ring, bearing a hydroxyl group at position C5’, with hydroxylation usually occurring at position C7′ of the A-ring and positions C3′ and C4′ of the B-ring. In addition, the glycosylation of flavones mainly occurs at positions C5′ and C7′ of the B-ring, and their methylation and acylation happens in the B-ring of the hydroxyl groups. The major flavones are apigenin, luteolin, baicalein, chrysin and their derivatives.

2.2. Flavonols

7Flavonols, known as 3-hydroxyflavone, process a hydroxyl group at position C3′ of the C-ring (Figure 1B) and are glycosylated to some extent. Flavonols are the building blocks of proanthocyanidins, which are abundant in vegetables and fruits such as onions, lettuce, tomatoes, apples, grapes and so on. Glycosylation and methylation mainly contribute to the diversity of flavonol compounds. O-glycoside, as the main substituent, occurs at position 7 of the A-ring and position 3 of the C-ring, and generates flavonol glycosides; these mainly include kaempferol, quercetin, limocitrin, and isorhamnetin. Over the past 15 years, the number of flavanones identified has significantly increased. Dietary flavonols play important roles in human health due to their anti-oxidant, cardio-protective, anti-bacterial, anti-viral and anti-cancer activities.

2.3. Flavanones

8Flavanones, also called dihydroflavones, have the saturated C-ring. The unsaturated double bond between positions C2′ and C3′ of the C-ring is the only chemical structural difference between flavanones and other flavonoids (Figure 1C). Flavanones are mainly distributed in all citrus fruits, and have hydroxyl groups at positions C5′ and C7′ of the A-ring and have hydroxyl/methoxy substituents at positions C3′ or C4′ of the B-ring. O-glycoside, as the main substituent, occurs at position 7 of the flavanone aglycone, and produces the flavanone glycosides. The substituents of flavanone glycosides contain glucoside, rhamnoside, rutinoside, and neohesperidoside. The flavanones can be divided into hesperitin, naringin, naringenin, eriodictyol, hesperidin, pinocembrin, and likvirtin based on their structural differences. Among them, naringenin and hesperetin, as the main flavanones, are mainly present in lemons, oranges, limes, tangerines and grapefruit.

2.4. Isoflavonoids

9Isoflavones contain a C-ring with a B-ring at position 3 (Figure 1D), which is the only chemical structural difference compared to other flavonoids. Isoflavonoids are mainly distributed in leguminous plants, and play important roles in microbial signaling and nodule induction in legumes. Isoflavones can be divided into two groups, genistein and daidzin, which exist in the chemical structures of aglycone, 7-O-glucoside, 6′-O-acetylglucoside, and 6′-O-malondialdehyde glucoside. Isoflavones have strong antioxidant properties, which can reduce the damage caused by free radicals to plant cells and improve their resistance to UV-B radiation, salt stress and osmotic stress.

2.5. Neoflavonoids

10There is a 4-phenyl coumarin backbone and no hydroxyl substitution at position C2′ in neoflavonoids (Figure 1E), which are rarely found in food plants. Neoflavonoids are mainly divided into four substructure types based on their basic skeleton structure, namely dalbergia phenols, dalbergia quinones, dalbergia lactones, and benzoyl benzenes.

2.6. Flavanols, Flavan-3-ols or Catechins

11Flavanols, known as dihydroflavonols/catechins, are the 3-hydroxy derivatives of flavanones (Figure 1F) and are naturally occurring plant-based nutrients due to their antioxidant properties. Flavanols are also referred to flavan-3-ols, as the hydroxyl group is always bound to position 3 of the C-ring. Unlike other flavonoids, flavanols have no double bond between positions C2′ and C3′ of the C-ring. Flavanols are abundant in manly fruits, such as bananas, apples, blueberries, and pears, and are divided into several types: catechin, gallocatechin, catechin 3-gallat, gallocatechin 3-gallate, epicatechin, epicatechin 3-gallate, and epicatechin 3-gallate. Flavanols and their metabolites play important roles in plant responses to various stresses due to their potent antioxidant and free radical scavenging activities.

2.7. Anthocyanins

12Anthocyanins, the glycosylated polyphenolic compounds, are a group of soluble vacuolar pigments that generate a series of orange, red, purple and blue colors in vegetative and re-productive plant organs. So far, over 650 anthocyanins have been identified in various plants and grouped into the following six categories: cyanidin, delphinidin, malvidin, pelargonidin, peonidin, petunidin, and the corresponding derivatives. Unlike other flavonoids, except flavanols, anthocyanins carry no ketone group at position 4 of the C-ring (Figure 1G). Anthocyanins are mainly found in the outer cell layer of various fruits and vegetables, such as black currants, grapes, and berries.

3.1. Regulation of Flavonoid Biosynthesis

13The biosynthesis of flavonoids occurs at the convergence of the shikimate and acetate pathways, with the former producing p-coumaroyl-CoA and the latter involved in a C2 elongation reaction (Figure 2). Phenylalanine ammonia lyase (PAL) catalyzes the deamination of phenylalanine into trans-cinnamic acid and ammonia; this is the first step of the phenylpropanoid pathway. Next, cinnamic acid hydroxylase (C4H), a cytochrome P450-dependent hydroxylase, hydroxylates the trans-cinnamic acid to produce p-coumaric acid. The 4-coumaric acid CoA ligase (4CL) catalyzes 4-coumaric acid to generate 4-coumaroyl CoA, which is a key intermediate in the biosynthesis of lignin and flavonoids. Chalcone synthase (CHS) catalyzes the formation of naringenin chalcone from one p-coumaroyl CoA and three malonyl-CoA molecules. Malonyl-CoA is the essential building block of natural products such as fatty acids, polyketides, and flavonoids. Naringenin chalcone is converted to produce flavanones through chalcone isomerase (CHI), which is cyclized to produce naringenin under the catalytic action of CHI. Naringenin, a general precursor of flavonoid compounds, is catalyzed by flavone synthase I and II (FNSI and II) and isoflavone synthase (IFS) to generate flavones and iso-flavones, respectively. In addition, naringenin is also catalyzed by flavanone-3-hydroxylase (F3H), flavonol 3′-hydroxylase (F3′H), and flavonol 3′5′-hy-droxylase (F3′5′H) to produce dihy-drokaempferol, dihydroquercetin, and dihydromyricetin, respectively. The dihydroflavonols are further converted to flavonols (kaempferol, quercetin, and myricetin) by flavonol synthase (FLS), which is also converted to leucoanthocyanidins under the catalysis of the dihydroflavonol 4-reductase (DFR). Anthocyanidins are then formed from leucoanthocyanidins by leucoanthocyanidin dioxygenase (LDOX), and are further catalyzed by uridine diphosphate (UDP)-glucose flavonoid-3-O-glycosyltransferase (UFGT). Leucoanthocyanidins and anthocyanidins can also be converted to proanthocyanidins by leucoanthocyanidin reductase (LAR) and anthocyanidin reductase (ANR), respectively. Finally, anthocyanins are stabilized via the modification of glycosylation, methylation, and acylation.

3.2. Transcription Factors (TFs) Regulate Flavonoid Biosynthesis

14Genes involved in flavonoid biosynthesis are classically divided into early biosynthetic genes (EBGs; CHI, CHS, F3′H and F3H) and late biosynthetic genes (LBGs; FLS, DFR, and ANS). Flavonoid biosynthesis is not only affected by plant hormones, but also regulated by various stresses. These environmental or developmental regulations mostly rely on the regulatory effect of TFs on structural genes in the flavonoid biosynthesis pathway (EBGs and LBGs). Based on the differences in the DNA-binding characteristics, several families of TFs have been described as regulators of flavonoid biosynthesis and metabolism in many plants; these include MYB, bHLH, WD40, bZIP, NAC, MADS box, Dof, and WRKY. MYB proteins include highly conserved N-terminal MYB repeats (1R, R2R3, 3R, and atypical). The flavonoid pathway genes are predominantly regulated by the R2R3-MYB transcription factors. The overexpression of NtMYB3 (an R2R3-MYB from narcissus) in transgenic tobacco inhibits flavonoid biosynthesis by decreasing the expression level of the FLS gene. In Ginkgo biloba, GBMYBF2 significantly inhibits the expression of structural genes (GBPAL, GBFLS, GBANS, and GBCHI) and thus reduces the accumulation of flavonoids. In soybean, GMMYB100 negatively regulates flavonoid biosynthesis by inhibiting the promoter activities of CHS and CHI. Under light conditions, the overexpression of PPMYB17 in pear calli can activate the expression of genes associated with flavonoid biosynthesis (PPCHS, PPCHI, PPF3H, PPFLS and PPUFGT), especially the expression of FLS; this enhances the biosynthesis of flavonoids in pear fruit. FTMYB31 has been isolated from Fagopyrum tataricum, the overexpression of which in tobacco enhances the expression level of CHS, F3H and FLS, and promotes the accumulation of flavonoid biosynthesis in plants. The SbMYB8 protein from Scutellaria baicalensis can bind to the GmMYB92 BS3 sequence in the SbCHS promoter region, which positively regulates the expression of SbCHS, and increase the flavonoid content and antioxidant enzyme activity in transgenic tobacco. The bHLH TFs play important roles in the regulation of many secondary metabolites, including flavonoids. In citrus, CsMYC2 is involved in the regulation of flavonoid biosynthesis through increasing the expression of UFGT. The bHLH protein CmbHLH2 can directly bind to the promoter of CmDFR, which promotes the accumulation of flavonoids in chrysanthemum plants. Interestingly, the R2R3-MYB TFs from subgroups 5, 6, and 15, bHLH from subgroup IIIf, and WD40 can interact with each other or orchestrate with others to regulate the expression of genes associated with flavonoid biosynthesis in many plants. The TT2–TT8–TTG1 complex plays important roles in the regulation of LBGs (DFR, LDOX, TT19, TT12, AHA10, and BAN). Moreover, the MBW complex can also tissue-specifically regulate the expression of the genes involved in flavonoid biosynthesis. The MYB5–TT8–TTG1 complex can regulate the expression of genes associated with flavonoid biosynthesis, such as DFR, LDOX, and TT12, in the endothelium, whereas the TT2–EGL3/GL3–TTG1 complex can regulate the expression of genes associated with flavonoid biosynthesis, such as LDOX, BAN, AHA10, and DFR, in the chalaza.

15In addition, the bZIP, NAC, Dof, and WRKY TFs have also been reported to regulate flavonoid biosynthesis. SlHY5, a bZIP protein from tomato, is affected by Cry1A proteins under blue light irradiation, which binds to the promoters of genes associated with flavonoid biosynthesis, such as PAL, CHS1 and CHS2, and thereby promotes the accumulation of flavonoids. VvibZIPC22 can activate the promoters of VviCHS and VviCHI, which increases the accumulation of flavonoids in plants. The overexpression of NtHY5 in tobacco increases the expression level of genes associated with phenylpropanoid, which can regulate the biosynthesis of flavonoids and enhance plant tolerance to salt stress. The Arabidopsis ANAC078 increases the expression level of CHS, F3’H, DFR, and LDO genes, thereby promoting the accumulation of flavonoids under strong light conditions. MdNAC52, an apple NAC TF, increases the content of flavonoids, including anthocyanins and procyanidins, in plants by binding to the promoters of MdMYB9 and MdMYB11, or by binding directly to the LAR; both of these mechanisms further regulate the expression level of flavonoids. The Arabidopsis AtDOF4 positively regulates the expression of late flavonoid genes (DFR, LDOX and TT19) and the MYB transcription factor PAP1 to promote the accumulation of flavonoids in plants. In addition, the overexpression of MdWRKY11 in apple callus promotes the expression of F3H, FLS, DFR, ANS and UFGT, which increases the content of flavonoids and anthocyanins.

3.3. Non-Coding RNA Regulates Flavonoid Biosynthesis

16In addition, flavonoid biosynthesis is also affected by non-coding RNA, such as lncRNA (long non-coding RNA) and microRNA. lncRNA may act as a precursor and endogenous target mimic of miRNA in order to indirectly regulate protein-coding genes (PCgenes). lncRNA (MSTRG.9304 and XR_001591906) can regulate the expression of the CHS gene in peanut seed development. miPEP858a-edited and miPEP858a-overexpressing lines can regulate flavonoid biosynthesis in Arabidopsis, which also alters the growth and development of plants. miR156 fine-tunes the anthocyanin biosynthetic pathway in poplar via the regulation of transcription factors, structural genes and other microRNAs.

4. The Roles of Flavonoid Compounds in Various Stresses

17The dynamic changes in flavonoid compounds are not only regulated by plant growth and development, but are also affected by various environmental factors; these encompass both abiotic stresses, such as heavy metal stress, drought stress, UV, salt and low temperatures, and biotic stresses, including plant-parasitic nematodes, fungi and bacteria.

4.1. Biotic Stress

18Various kinds of secondary metabolites that play important defense roles, including flavonoids, are produced when plants are infected with pathogens and pests and are suffering from biotic stresses. Plants can be destroyed by various biotic stresses, such as bacteria, viruses, nematodes, fungi and insects. Hypersensitive responses (HR) are a major element of plant disease resistance, and include the induction of lytic enzymes, the production of phytoalexins and the reinforcement of the cell wall. Among these, phytoalexins are chemicals that play important roles in mediating plant responses to pests and pathogens. Numerous studies have shown that some flavonoid compounds act as phytoalexins against pathogenic bacteria, fungi, and nematodes.

4.1.1. The Roles of Flavonoids in the Invasion of Nematodes

19Plant-parasitic nematodes can destroy the host plant by causing wounds and infecting it with microbial diseases; this destruction leads to a massive yield loss and tremendous economic losses throughout the world. When plant-parasitic nematodes damage plants, some brown spots, galls, spots, cysts, rotting or swelling is generally formed on the roots or on the aboveground tubers. Flavonoids and their derivatives, for example, coumestrol and glyceollin, play a variety of roles in the interaction between plants and nematodes, and are stimulated by nematode invasion. Coumestrol, an important phytoalexin, is an isoflavonoid-like compound that can be produced in the lima bean when it is suffering from Pratylenchus penetrans infection. Moreover, the infection of soybean roots with the root-knot nematode (Meloidogyne incognita) leads to an increase in the glyceollin content, which reduces the crop yield loss caused by nematodes. In addition, the phytoalexin glyceollin is accumulated in the soybean root, and it has been found that there is an increase in its glyceollin content on the 2nd, 4th and 6th day after inoculation. O-methyl-apigenin-C-deoxyhexoside-O-hexoside, a major phytoalexin in oat, has been extracted from the oat roots and shoots infected with nematodes; this was shown to reduce the invasion of cereal cyst nematodes significantly, including P. neglectus and H. avenae. However, the defense mechanism of flavonoids against parasitic nematodes is still unclear.

4.1.2. The Roles of Flavonoids in the Invasion of Pathogenic Fungi

20Tremendous crop yield losses occur in plants when they are invaded with several kinds of plant pathogenic fungi. To escape from various kinds of biotic stresses, plants have evolved mechanisms to resist biotic stresses, and the production of phytoalexins is an effective method for defending against the invasion of pathogenic fungi. The flavonol aglycone rhamnetin is a fungi-toxic phytoalexin that enhances the resistance of cucumber to a powdery mildew. There is an increase in the content of nobiletin, heptamethoxyflavone, tangeretin and sinensetin in citrus fruits when they are infected with Phytophthora citrophthora, which is positively correlated with their antifungal effects. Naringenin and hesperetin have been proven to be the best antifungal compounds in flavonoids. An increase in the content of isoflavonoids in tangelo Nova fruits is detected when they are treated with 6-benzylaminopurine, and the fruit resistance is enhanced by 60% when suffering from the invasion of pathogenic fungus. In addition, the content of several kinds of phytoalexin is increased in soybean cotyledons when they are treated with four Aspergillus species, and the content of coumestrol and phytoalexins glyceollin is the highest after infection with A. sojae and A. niger, respectively.

4.1.3. Antibacterial Effects of Flavonoids

21Many researches have indicated that flavonoids can be used as antibacterial agents in plants to make them grow and develop better. Plants can produce many kinds of phytoalexins, which are antimicrobial secondary metabolites, under various stresses, such as microbial attack. Bean plants infected with Pseudomonas spp. produce antibacterial phytoalexins in bean leaves, which may enhance the plant’s resistance to Pseudomonas spp.. It has been shown that there is an increase in coumestrol in the infected bean leaves, which blocks the bacterial colonization of P. mars-prunorum and P. phaseolicola. There is also an increase in daidzein and coumestrol in soybean leaves when the plants are infected with non-pathogenic bacteria (P. lachrymans) and pathogenic bacteria (P. glycinea), indicating that coumestrol can inhibit pathogenic bacterial colonization and improve the plant’s resistance to P. glycinea. Moreover, kievitone and phaseollinisoflavan also have antibacterial activity, which strongly inhibits the growth of Achromobacter and Xanthomonas species. Recently, an isoflavonoid was proven to have a strong antagonistic effect on Staphylococcus aureus, which can be extracted from the roots of Erythrina poeppigiana.

4.2.1. UV Stress

22Plants can rapidly produce reactive oxygen species (ROS) when they suffer under high flux, long-term UV radiation and HL (high light), which cause oxidative damage to biomolecules (DNA, proteins, RNA and membranes). Under UV induction and HL, plants can produce flavonoids, mainly in their epidermal cells. As different flavonoid compounds have different UV absorption capacities, flavonoids can play important roles when plants suffer from UV induction and HL, being especially useful as a protective shield. Previous studies have reported that flavonols, flavones, and anthocyanins are all involved in UV and high light stress protection in plants. Under UV radiation, an increase in flavonoids, such as via the production of luteolin 7-O-glycosides and quercetin 3-O, improves their hydroxylation levels and strengthens their antioxidant activity, which contributes to the ROS-detoxification of the plant cell and relieves the oxidative damage caused by UV stress. Compared with the content of kaempferol under UV-B radiation, there is a higher content of quercetin and a higher ratio of quercetin/kaempferol in the leaves of some plants, which indicate that UV-B radiation could induce the substitution of the orthodihydroxy B-ring in quercetin; this would increase their adaptive dissociation. Compared with low-altitude plants, high-altitude plants are subjected to high UV-B exposure. There are higher levels of rhamnosylisoorientin and maysin in the leaves of high-altitude maize lines compared to those detected in the leaves of low-altitude maize lines, which indicates that these two flavones might play important protective roles against UV-B radiation via an adaptive response. Moreover, UV radiation can cause the accumulation of anthocyanin in many plants, which improves the coloration in the fruit skin of apples and other fruits. Coumaroyl and mustapoyl derivatives are formed by the acylation of anthocyanins and phenylpropanoid acids, which may increase UV absorption compared to anthocyanins alone. Therefore, coumaroyl and sinapoyl derivatives might play important roles under UV-B radiation stress. As flavonoids contain phenolic hydroxyl groups, they also exhibit antioxidant activity in the development and growth of plants. The abundant flavonoids in chloroplasts are mainly dihydroxy B-ring-substituted flavonoids, such as lignan and quercetin, which play important roles in the elimination of ROS. Under excessive light stress, the H2O2 produced by chloroplasts can be accumulated in the vesicles, which can be further scavenged by flavonoid compounds. The ROS can be generated in different cell types and subcellular regions, which can be scavenged by many kinds of flavonols.

23Many genes associated with flavonoid biosynthesis could play important roles in plants under excessive light and UV stress, including structural genes (PAL, 4CL, CHS, DFR, CHI and F3’5’H) and transcription factors (MYB, bHLH, NAC, and bZIP) (Table 1). Under UV stress, the accumulation of photo-protectant flavonoids (e.g., flavones, isoflavonoids, neoflavonoids, flavanols, and anthocyanins) could absorb some harmful solar wave lengths (e.g., UV) in order to mitigate oxidative damage to cells, LDL or DNA.

4.2.2. Cold Stress

24Cold stresses are common stresses during the process of growth and development in plants; these include chilling stress, with temperatures of 0–20 °C, and freezing stress, with temperatures of <0 °C, both of which can seriously affect plant growth and development and reduce crop productivity, especially for crops that are sensitive to low temperatures. Chilling stress can affect plant growth from germination to maturity, and can also determine the distribution of plants around the world. There are significant differences among various plants regarding when and how they suffer from chilling stress. Some plants can grow well at chilling temperatures, such as some overwintering cereals and Arabidopsis, while other plants struggle to survive at chilling temperatures, such as many tropical and subtropical plants (maize, rice and tobacco). Previous studies have reported that plants undergo a series of physiological and cellular changes under low-temperature conditions, including changes in calcium signal, photosynthesis, metabolism and membrane structure. Freezing stress is much more harmful to plants than low-temperature stress, and may even lead to plant death. Under natural conditions, freezing damage starts from extracellular ice nucleation. Once ice nuclei are formed, they gradually become larger and form ice crystals, which diffuse into the apoplast. In the apoplast, ice crystals can induce water outflow, which can lead to cell dehydration. When ice crystals diffuse into cells, irreversible damage occurs. Flavonoids play an important role in coping with freezing stress. Schulz et al. revealed that flavonoids are the determining factor in the freezing resistance and cold adaptation of Arabidopsis, which suggests that the complete loss or substantial reduction in flavonoids leads to the damage of the freezing resistance mechanism. Previous studies have reported that several flavonoids (flavones, flavonols, flavanols, and anthocyanins) display a strong resistance to cold stress. In Cryptomeria japonica, cold stress can enhance the production of anthocyanins, flavonoids and flavonols through the up-regulation of FLS, which provides a good basis for the molecular mechanism of response to cold stress in spruce. In addition, an increase in anthocyanins in their epidermal cells can decrease the osmotic potential of cells and delay freezing through the surface nucleate. When Fagopyrum tataricum was subjected to cold stress, the total content of anthocyanins in the epidermis and cortex cells of hypocotyl was twice those in cotyledons, which improved their cold resistance. Moreover, many genes associated with flavonoid biosynthesis are up-regulated when suffering from cold stress, including structure genes (CHI, CHS, C4H, ANS, UFGT, F3H, and DFR) and TFs (MADS-box, bZIP, MYB, and bHLH), further confirming that flavonoids play a key role in enhancing cold resistance (Table 1).

4.2.3. Salt Stress

25Salinity stress is a major threat to global food production, which can inhibit plant growth and development through osmotic stress, cytotoxicity caused by the excessive absorption of Na+ and Cl−, and nutritional deficiencies. Research shows that 20% of the world’s irrigated land suffers from excess soluble salts. The limiting effect of excess soluble salts in the soil on plant growth and development is mainly mediated through two mechanisms: osmotic stress and ion toxicity. The increased ion concentration in soil causes a low solute/osmotic potential, reduces the ability of plant roots to uptake water, and eventually blocks plant growth and development. Moreover, ion toxicity caused by sodium accumulation damages the cell membrane and disturbs various plant physiological processes, such as photosynthesis, respiration, transpiration and osmoregulation, which eventually cause plant necrosis or chlorosis. Yan et al. found that NaCl treatment significantly increases the content of flavonoid glycosides through the up-regulation of GMFNSII-1 and GMFNSII-2 in Glycine max, indicating that flavonoid glycosides play a positive role in enhancing salt tolerance. Salt stress also increases the luteolin content in Cajanus cajan by upregulating the expression level of CcPCL1 and CcF3′H-5, which greatly enhances the salt tolerance of plants. Moreover, the content of flavonoids accumulates differentially between the roots and leaves of Solenostemma argel under salt stress; this improves the antioxidant capacity and osmoregulatory capacity of plants under salt stress. Wang et al. found that high salt stress (85 mmol/L) promotes anthocyanin biosynthesis in cultivated purple sweet potato, and that low salinity has a significant effect on the biosynthesis of phenolic acids and flavonols in the plant. Under low salt stress, plants can regulate genes to control the concentrations of cellular Na+ and K+ in plasma; however, they lose this ability under high salt stress. In addition, it has also been found that salt stress increases the content of isoflavones by regulating the expression of GMIFS1, which improves the antioxidant capacity and osmotic stress tolerance of soybean.

4.2.4. Drought Stress

26Drought is a major environmental stress factor that affects various physiological and biochemical processes in plants. To escape from environmental stresses, plants have evolved complex mechanisms to respond to stress at the physiological and biochemical levels, including the production of compatible osmolytes, endogenous hormonal changes, and molecular changes. The plants mediate the balance between growth and resistance to stress by modulating the architecture of the root system and stomatal closure under moderate drought stress. Plants can induce cellular protection against severe drought stress, modulate the antioxidant enzyme systems to remove ROS, and accumulate proteins to maintain cell turgor.

27Flavonoids, including anthocyanins, flavonols, flavanols, and flavones, play a major role in the response to drought stress. Under drought stress conditions, plants can accumulate anthocyanins to protect them against excessive sunlight and prevent water loss by reducing stomatal transpiration and density; this allows them to survive in a severe drought environment. The biosynthesis of catechin in the tea plant was shown to be induced under drought stress, increasing the plant’s ROS scavenging capacity and enhancing its drought stress tolerance. There was an increase in cyanidin, delphinidin 3-O-glucoside, and cyanidin 3-O-glucoside in the calyx of Roselle Cultivars at physiological maturity under 35% water-loss stress. There was an increase in the flavonoid content, total phenolic capacity and antioxidant capacity under water deficit stress in Peppermint. Moreover, Mechri et al. found that the concentrations of catechin, quercetin, luteolin 7-O-glucoside, and apigenin 7-O-glucoside in olive leaves increased after drought treatments, indicating that these phenolic compounds regulate the olive water status and reduce the oxidative damage caused by water deficit stress.

28Numerous studies have shown that genes associated with flavonoid biosynthesis are regulated independently by drought stress, such as PAL, CHS, CHI, F3H, DFR, ANS, NAC, WRKY, bZIP, MYB, and bHLH (Table 1). For example, the expression level of TaCHS, TaCHI, TaF3H, TaFNS, TaFLS, TaDFR and TaANS in wheat has been shown to rapidly increase after drought stress, thus increasing the total contents of phenols, flavonoids, and anthocyanins. Transcriptome analysis has indicated that several TFs (bHLH, NAC, MYB, and WRKY) play important roles in response to cold and drought stress during seed germination. In addition, the transcriptome analysis of Cicer arietinum treated with drought stress was conducted, and the results showed that AP2-EREBP, bHLH, bZIP, MYB, NAC, WRKY and MADS were involved in the drought stress response.

4.2.5. Heavy Metal Stress

29In recent decades, the rapid development of industry and the use of pesticides have caused heavy metal contamination in the soil. Heavy metal stress has notable adverse effects on crop productivity and growth. Heavy metals, including lead (Pb), cadmium (Cd), nickel (Ni), cobalt (Co), zinc (Zn), chromium (Cr), iron (Fe), arsenic (As), and silver (Ag), are present in dispersed form in rock formations, and are considered to be one of the potential threats to crop plant productivity. Although all heavy metals are non-biodegradable and immobile, heavy metals can be absorbed by plant root systems via diffusion, endocytosis or through metal transporters. Heavy metal stress causes the inactivation of enzymes and interferes with the substitution reactions of essential metal ions from biomolecules. Heavy metal stress destroys the membrane integrity and alters the basic plant metabolic reactions, such as photosynthesis, respiration and homeostasis. Moreover, heavy metal stress generates ROS, such as superoxide radical (O−2), hydroxyl radical (OH) and hydrogen peroxide (H2O2), and the cytotoxic compound, which leads to lipid peroxidation; this damages biomolecules and destroys DNA strands.

30In order to escape from environments containing heavy metals, plants have gradually evolved mechanisms to cope with these heavy metals. The functional roles of flavonoids in the response to heavy metal stress have received some attention. For example, studies have shown that the contents of flavonols (quercetin and kaempferol) increases in Arabidopsis via the upregulation of FLS1 under lead stress (Pb) treatment, thus alleviating lead toxicity. Cd stress has been shown to induce the accumulation of isoflavone compounds such as malonylolonin, medicarpin, coumestrol, formonetin, and medicarpin3-O-b-(60-malonylglucoside) in Medicago truncatula roots after Cd stress, thus alleviating Cd toxicity. Moreover, Cd stress has been shown to increase the accumulation of anthocyanins via the upregulation of CHS and DFR in Azolla imbricata, thus improving their ROS scavenging ability and enhancing the tolerance of Azolla imbricata to Cd stress.

5. Transgenic Technologies Used in Enhancing Stress Resistance

31In agricultural biotechnology, many techniques are used to alter the genetic structure of plants to produce genetically modified plants. Transgenic technology can be used to improve plant traits (yield and quality), as well as to solve agricultural problems (biotic and abiotic stresses).

5.1. Transgenic Technology Used in Enhancing UV and HL Resistance

32Transgenic plants that carry structure genes and TFs for UV/HL tolerance are being developed, mainly by using Agrobacterium methods. The overexpression of the CHS gene has been shown to enhances resistance to high levels of light in Arabidopsis leaves by increasing the content of anthocyanins. The overexpression of the MnFNSI gene from Morus notabilis in tobacco has been shown to increase the content of flavones in leaves and enhance their tolerance to UV-B stress. The heterologous expression of Pn2-ODD1 in Arabidopsis has also awarded plants tolerance to UV-B radiation and oxidative stress by increasing their antioxidant capacity. Arabidopsis lacking ANS have been shown to be sensitive to high light levels due to the impairment of anthocyanin photoprotection. Moreover, TFs involved in the flavonoid biosynthesis have been found to play important roles under UV stress. The overexpression of GmMYB12B2 in Arabidopsis promotes flavonoid biosynthesis and improves the tolerance of transgenic Arabidopsis to salt and UV stress. In transgenic apple, MdWRKY72 and MdBBX20 enhance the plant resistance to UV-B stress through the regulation of genes associated with anthocyanin biosynthesis (MdANS, MdDFR, MdUFGT, and MdMYB1). The overexpression of ANAC078 in Arabidopsis increases the content of anthocyanin, and enhances the tolerance of plants to HL stress, which is opposite to the ANAC078 mutant plants.

5.2. Transgenic Technology Used in Enhancing Salt Resistance

33Transgenic plants that carry structure genes and TFs for salt tolerance are currently being developed. For example, the overexpression of EaCHS1 in tobacco has been shown to increase the production of downstream flavonoids and the expression of related genes in the phenylpropanoid pathway, and to maintain ROS homeostasis; this improves the plant’s resistance to salinity stress during seed germination and root development. The overexpression of AtDFR in Brassica napus increases the content of anthocyanins, which enhances its salt tolerance in comparison with wild-type plants under high-salt stress conditions. Moreover, transgenic Arabidopsis overexpressing the wheat TaDFR-I gene augments the accumulation of anthocyanin and promotes the tolerance of plants to high salt penetration. Transgenic Arabidopsis plants overexpressing PnF3H significantly increase the expression level of resistance genes (AtSOS3, AtP5CS1, AtHKT1, AtCAT1 and AtAPX1), reduce the hydrogen peroxide content and enhance the salt and oxidative stress tolerance of plants. Moreover, many TFs associated with flavonoid biosynthesis, such as WD40, MYB, bHLH, bZIP, NAC, WRKY, and MADS-box, played important roles in response to salt stress. Transgenic Arabidopsis overexpressing TaWD40 from Triticum aestivum significantly improves the tolerance of plants to salt osmotic stresses. The overexpression of grapevine VvbHLH1 in Arabidopsis increases the flavonoid contents and enhances the salt tolerance of plants.

5.3. Transgenic Technology Used in Enhancing Drought Resistance

34Transgenic plants carrying structure genes and TFs for drought tolerance have been reported. For example, transgenic tobacco overexpressing the IbC4H gene from the purple sweet potato has been shown to significantly promote the biosynthesis of flavonoids such as anthocyanins and flavonols, enhance the ROS scavenging capacity of plants, and improve their drought resistance. The overexpression of Lycium chinense LcF3H in tobacco also increases the flavan-3-ol content (including catechin and epicatechin) and improve the antioxidant system, which strengthens the drought stress tolerance of the plant. In addition, the overexpression of EcbHLH57 from Eleusine coracana in tobacco leads to the accumulation of more flavonoids, such as flavonols and flavanols, and enhances the photosynthetic rate and stomatal conductance; these factors significantly improve the tolerance of the plant to salt stress and drought stress. The transgenic Arabidopsis that overexpresses ZmWRKY40 promotes the biosynthesis of flavonoids, increases POD and CAT activities, and reduces the ROS content, which improves the drought stress tolerance of the plant.

5.4. Transgenic Technology Used in Enhancing Low Temperature Resistance

35Low temperatures significantly increase the content of flavonoids via the regulation of genes involved in flavonoid biosynthesis. The overexpression of SlF3H in tobacco plants strongly induces the expression of CHS, CHI, and FLS, and increases the contents of anthocyanins and other flavonoids; this improves the tolerance of the plant to cold stress. Transgenic Arabidopsis that overexpress OrbHLH001 has been shown to increases the accumulation of flavonoids such as flavonols, anthocyanins, and flavanones through the regulation of CHS, CHI, F3H, and C4H, which enhance the tolerance of transgenic Arabidopsis to freezing and salt stress. The overexpression of SlNAM1 in tobacco plants accumulates many more anthocyanins and other flavonoids, thus improving the cold tolerance of the plants.

6. Conclusions and Future Prospects

36The biosynthesis of flavonoids is the most studied pathway of secondary metabolism in plants. The defensive role of flavonoids in plants against various biotic and abiotic stresses was reviewed in Figure 3, and their significant contributions to plant resistance were also discussed. Flavonoids contain several subgroups, including anthocyanidins, flavonols, flavones, flavanols, flavanones, chalcones, dihydrochalcones and dihydroflavonols, which are widely distributed in various plants. However, the detailed functions of particular flavonoids are still not clear, and need to be explored. The roles of specialized flavonoids in response to various stresses are also worth evaluating. With the rapid advancements made in sequencing technology, there have been major achievements regarding the identification of candidate genes associated with flavonoid biosynthesis. Although many genes have been identified, some specific genes associated with certain important flavonoids are poorly understood, and need to be studied further. Although many researchers have explored the functions of genes associated with flavonoid biosynthesis through transgenic approaches, it may take a long time to verify their gene functions. It is evident that flavonoids play important protective roles against harmful biotic and abiotic stresses, but that the knowledge of flavonoids under various stresses is still incomplete and requires extensive research.

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Lou H., Hu L., Lu H., Wei T., Chen Q. Metabolic engineering of microbial cell factories for biosynthesis of flavonoids: A review. Molecules. 2021;26:4522.
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82.
Aron P.M., Kennedy J.A. Flavan-3-ols: Nature, occurrence and biological activity. Mol. Nutr. Food Res. 2008;52:79-104.
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Yao L.H., Jiang Y.M., Shi J., Tomas-Barberan F.A., Datta N., Singanusong R., Chen S.S. Flavonoids in food and their health benefits. Plant Foods Hum. Nutr. 2004;59:113-122.
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Dutta M.S., Mahapatra P., Ghosh A., Basu S. Estimation of the reducing power and electrochemical behavior of few flavonoids and polyhydroxybenzophenones substantiated by bond dissociation energy: A comparative analysis. Mol. Divers. 2022;26:1101-1113.
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85.
Krysa M., Szymańska-Chargot M., Zdunek A. FT-IR and FT-Raman fingerprints of flavonoids—A review. Food Chem. 2022;393:133430.
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Pico J., Xu K., Guo M., Mohamedshah Z., Ferruzzi M.G., Martinez M.M. Manufacturing the ultimate green banana flour: Impact of drying and extrusion on phenolic profile and starch bioaccessibility. Food Chem. 2019;297:124990.
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87.
Zhang T., Wei X., Miao Z., Hassan H., Song Y., Fan M. Screening for antioxidant and antibacterial activities of phenolics from Golden Delicious apple pomace. Chem. Cent. J. 2016;10:47.
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88.
Pal D., Verma P. Flavonoids: A powerful and abundant source of antioxidants. Int. J. Pharm. Pharm. Sci. 2013;5:95-98.
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89.
Ding T., Cao K., Fang W., Zhu G., Chen C., Wang X., Wang L. Evaluation of phenolic components (anthocyanins, flavanols, phenolic acids, and flavonols) and their antioxidant properties of peach fruits. Sci. Hortic. 2020;268:109365.
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90.
Awad M.A., Hadi F.H. Effect of aqueous extract of green tea on gene expression of CYP17, CYP11A, LH beta subunit and LHr genes in males wistar rats exposed to oxidative stress by streptozotocin. J. Madenat Alelem Univ. Coll. 2019;11:6-15.
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91.
Chemistry and Biological Activities of Flavonoids: An Overview · 2013
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92.
Bartwal A., Mall R., Lohani P., Guru S.K., Arora S. Role of secondary metabolites and brassinosteroids in plant defense against environmental stresses. J. Plant Growth Regul. 2013;32:216-232.
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93.
Yang S., Mi L., Wu J., Liao X., Xu Z. Strategy for anthocyanins production: From efficient green extraction to novel microbial biosynthesis. Crit. Rev. Food Sci. Nutr. 2022;1-16.
Not in our library10.1080/10408398.2022.2067117
94.
Nanoemulsion and Nanoliposome Based Strategies for Improving Anthocyanin Stability and Bioavailability · 2019
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95.
Qaisar U., Afzal M., Tayyeb A. Commercial Application of Plant pigments. Int. J. Biotech Trend. Technol. 2019;9:18-22.
Not in our library10.14445/22490183/ijbtt-v9i3p604
96.
Fang J. Classification of fruits based on anthocyanin types and relevance to their health effects. Nutrition. 2015;31:1301-1306.
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97.
Veberic R., Slatnar A., Bizjak J., Stampar F., Mikulic-Petkovsek M. Anthocyanin composition of different wild and cultivated berry species. LWT-Food Sci. Technol. 2015;60:509-517.
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98.
Anthocyanidins and anthocyanins: colored pigments as food, pharmaceutical ingredients, and the potential health benefits · 2017
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99.
Mikulic-Petkovsek M., Slatnar A., Schmitzer V., Stampar F., Veberic R., Koron D. Chemical profile of black currant fruit modified by different degree of infection with black currant leaf spot. Sci. Hortic. 2013;150:399-409.
Not in our library10.1016/j.scienta.2012.11.038
100.
Chaves-Silva S., Dos Santos A.L., Chalfun-Júnior A., Zhao J., Peres L.E., Benedito V.A. Understanding the genetic regulation of anthocyanin biosynthesis in plants–tools for breeding purple varieties of fruits and vegetables. Phytochemistry. 2018;153:11-27.
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101.
Badhani A., Rawat S., Bhatt I.D., Rawal R.S. Variation in Chemical Constituents and Antioxidant Activity in Y ellow H imalayan (R ubus ellipticus S mith) and Hill Raspberry (R ubus niveus T hunb.). J. Food Biochem. 2015;39:663-672.
Not in our library10.1111/jfbc.12172
102.
Kim A.N., Lee K.Y., Jeong E.J., Cha S.W., Kim B.G., Kerr W.L., Choi S.G. Effect of vacuum–grinding on the stability of anthocyanins, ascorbic acid, and oxidative enzyme activity of strawberry. Lwt. 2021;136:110304.
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103.
Tohge T., de Souza L.P., Fernie A.R. Current understanding of the pathways of flavonoid biosynthesis in model and crop plants. J. Exp. Bot. 2017;68:4013-4028.
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104.
Gho Y.S., Kim S., Jung K.H. Phenylalanine ammonia-lyase family is closely associated with response to phosphate deficiency in rice. Genes Genom. 2020;42:67-76.
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105.
Kim J.I., Hidalgo-Shrestha C., Bonawitz N.D., Franke R.B., Chapple C. Spatio-temporal control of phenylpropanoid biosynthesis by inducible complementation of a cinnamate 4-hydroxylase mutant. J. Exp. Bot. 2021;72:3061-3073.
Not in our library10.1093/jxb/erab055
106.
Li M., Guo L., Wang Y., Li Y., Jiang X., Liu Y., Xie D., Gao L., Xia T. Molecular and biochemical characterization of two 4-coumarate: CoA ligase genes in tea plant (Camellia sinensis). Plant Mol. Biol. 2022;109:579-593.
Not in our library10.1007/s11103-022-01269-6
107.
Sun T., Li S., Song X., Pei G., Diao J., Cui J., Shi M., Chen L., Zhang W. Re-direction of carbon flux to key precursor malonyl-CoA via artificial small RNAs in photosynthetic Synechocystis sp. PCC 6803. Biotechnol. Biofuels. 2018;11:26.
Not in our library10.1186/s13068-018-1032-0
108.
Wang Y., Chen H., Yu O. A plant malonyl-CoA synthetase enhances lipid content and polyketide yield in yeast cells. Appl. Microbiol. Biot. 2014;98:5435-5447.
Not in our library10.1007/s00253-014-5612-z
109.
Three AP2/ERF family members modulate flavonoid synthesis by regulating type IV chalcone isomerase in citrus · 2020
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110.
Cheng A.X., Han X.J., Wu Y.F., Lou H.X. The function and catalysis of 2-oxoglutarate-dependent oxygenases involved in plant flavonoid biosynthesis. Int. J. Mol. Sci. 2014;15:1080-1095.
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Dastmalchi M., Dhaubhadel S. Soybean chalcone isomerase: Evolution of the fold, and the differential expression and localization of the gene family. Planta. 2015;241:507-523.
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112.
Hacquard S., Wang E., Slater H., Martin F. Impact of global change on the plant microbiome. Spec. Issue. 2022;234:1907-1909.
Not in our library10.1111/nph.18187
113.
Baba S.A., Ashraf N. Functional characterization of flavonoid 3′-hydroxylase, CsF3′ H, from Crocus sativus L: Insights into substrate specificity and role in abiotic stress. Arch. Biochem. Biophys. 2019;667:70-78.
Not in our library10.1016/j.abb.2019.04.012
114.
Flavonoids a Bioactive Compound from Medicinal Plants and Its Therapeutic Applications · 2022
No notice
115.
Sun L., Fan X., Zhang Y., Jiang J., Sun H., Liu C. Transcriptome analysis of genes involved in anthocyanins biosynthesis and transport in berries of black and white spine grapes (Vitis davidii). Hereditas. 2016;153:17.
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116.
Li H., Tian J., Yao Y.Y., Zhang J., Song T.T., Li K.T., Yao Y.C. Identification of leucoanthocyanidin reductase and anthocyanidin reductase genes involved in proanthocyanidin biosynthesis in Malus crabapple plants. Plant Physiol. Biochem. 2019;139:141-151.
Not in our library10.1016/j.plaphy.2019.03.003
117.
Ma S., Hu R., Ma J., Fan J., Wu F., Wang Y., Huang L., Feng G., Li D., Nei G., et al. Integrative analysis of the metabolome and transcriptome provides insights into the mechanisms of anthocyanins and proanthocyanidins biosynthesis in Trifolium repens. Ind. Crops Prod. 2022;187:115529.
Not in our library10.1016/j.indcrop.2022.115529
118.
Rauf A., Imran M., Abu-Izneid T., Iahtisham U.H., Patel S., Pan X., Naz S., Silva A.S., Saeed F., Suleria H.A.R. Proanthocyanidins: A comprehensive review. Biomed. Pharmacother. 2019;116:108999.
Not in our library10.1016/j.biopha.2019.108999
119.
Dongbao C.A.I., Xusheng L.I., Jianxia S.U.N., Weibin B.A.I. Advances in the Techniques of Stabilizing Anthocyanin. Future Food Sci. 2021;1:1.
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120.
Guo N., Cheng F., Wu J., Liu B., Zheng S., Liang J., Wang X. Anthocyanin biosynthetic genes in Brassica rapa. BMC Genom. 2014;15:426.
Not in our library10.1186/1471-2164-15-426
121.
Ethylene mediates the branching of the jasmonate‐induced flavonoid biosynthesis pathway by suppressing anthocyanin biosynthesis in red Chinese pear fruits · 2019
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122.
Xu W., Dubos C., Lepiniec L. Transcriptional control of flavonoid biosynthesis by MYB–bHLH–WDR complexes. Trends Plant Sci. 2015;20:176-185.
Not in our library10.1016/j.tplants.2014.12.001
123.
Fenn M.A., Giovannoni J.J. Phytohormones in fruit development and maturation. Plant J. 2021;105:446-458.
Not in our library10.1111/tpj.15112
124.
Corso M., Perreau F., Mouille G., Lepiniec L. Specialized phenolic compounds in seeds: Structures, functions, and regulations. Plant Sci. 2020;296:110471.
Not in our library10.1016/j.plantsci.2020.110471
125.
Guo X., Wang Y., Zhai Z., Huang T., Zhao D., Peng X., Feng C., Xiao Y., Li T. Transcriptomic analysis of light-dependent anthocyanin accumulation in bicolored cherry fruits. Plant Physiol. Biochem. 2018;130:663-677.
Not in our library10.1016/j.plaphy.2018.08.016
126.
Sukumari Nath V., Kumar Mishra A., Kumar A., Matoušek J., Jakše J. Revisiting the role of transcription factors in coordinating the defense response against citrus bark cracking viroid infection in commercial hop (Humulus Lupulus L.). Viruses. 2019;11:419.
Not in our library10.3390/v11050419
127.
Li K., Xing C., Yao Z., Huang X. Pbr MYB 21, a novel MYB protein of Pyrus betulaefolia, functions in drought tolerance and modulates polyamine levels by regulating arginine decarboxylase gene. Plant Biotechnol. J. 2017;15:1186-1203.
Not in our library10.1111/pbi.12708
128.
Qin W., Xie L., Li Y., Liu H., Fu X., Chen T., Hassani D., Li L., Sun X., Tang K. An R2R3-MYB transcription factor positively regulates the glandular secretory trichome initiation in Artemisia annua L. Front. Plant Sci. 2021;12:657156.
Not in our library10.3389/fpls.2021.657156
129.
Czemmel S., Heppel S.C., Bogs J. R2R3 MYB transcription factors: Key regulators of the flavonoid biosynthetic pathway in grapevine. Protoplasma. 2012;249:109-118.
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130.
Anwar M., Yu W., Yao H., Zhou P., Allan A.C., Zeng L. NtMYB3, an R2R3-MYB from narcissus, regulates flavonoid biosynthesis. Int. J. Mol. Sci. 2019;20:5456.
Not in our library10.3390/ijms20215456
131.
Xu F., Ning Y., Zhang W., Liao Y., Li L., Cheng H., Cheng S. An R2R3-MYB transcription factor as a negative regulator of the flavonoid biosynthesis pathway in Ginkgo biloba. Funct. Integr. Genom. 2014;14:177-189.
Not in our library10.1007/s10142-013-0352-1
132.
Yan J., Wang B., Zhong Y., Yao L., Cheng L., Wu T. The soybean R2R3 MYB transcription factor GmMYB100 negatively regulates plant flavonoid biosynthesis. Plant Mol. Biol. 2015;89:35-48.
Not in our library10.1007/s11103-015-0349-3
133.
Premathilake A.T., Ni J., Bai S., Tao R., Ahmad M., Teng Y. R2R3-MYB transcription factor PpMYB17 positively regulates flavonoid biosynthesis in pear fruit. Planta. 2020;252:59.
Not in our library10.1007/s00425-020-03473-4
134.
Sun Z., Linghu B., Hou S., Liu R., Wang L., Hao Y., Han Y., Zhou M., Liu L., Li H. Tartary buckwheat FtMYB31 gene encoding an R2R3-MYB transcription factor enhances flavonoid accumulation in Tobacco. J. Plant Growth Regul. 2020;39:564-574.
Not in our library10.1007/s00344-019-10000-7
135.
Yuan Y., Qi L., Yang J., Wu C., Liu Y., Huang L. A Scutellaria baicalensis R2R3-MYB gene, SbMYB8, regulates flavonoid biosynthesis and improves drought stress tolerance in transgenic tobacco. Plant Cell Tissue Organ Cult. 2015;120:961-972.
Not in our library10.1007/s11240-014-0650-x
136.
Cultrone A., Cotroneo P.S., Reforgiato Recupero G. Cloning and molecular characterization of R2R3-MYB and bHLH-MYC transcription factors from Citrus sinensis. Tree Genet. Genomes. 2010;6:101-112.
Not in our library10.1007/s11295-009-0232-y
137.
Qi Y., Zhou L., Han L., Zou H., Miao K., Wang Y. PsbHLH1, a novel transcription factor involved in regulating anthocyanin biosynthesis in tree peony (Paeonia suffruticosa). Plant Physiol. Biochem. 2020;154:396-408.
Not in our library10.1016/j.plaphy.2020.06.015
138.
Li S. Transcriptional control of flavonoid biosynthesis: Fine-tuning of the MYB-bHLH-WD40 (MBW) complex. Plant Signal. Behav. 2014;9:e27522.
Not in our library10.4161/psb.27522
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Mano H., Ogasawara F., Sato K., Higo H., Minobe Y. Isolation of a regulatory gene of anthocyanin biosynthesis in tuberous roots of purple-fleshed sweet potato. Plant Physiol. 2007;143:1252-1268.
Not in our library10.1104/pp.106.094425
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Zhao L., Gao L., Wang H., Chen X., Wang Y., Yang H., Wei C., Wan X., Xia T. The R2R3-MYB, bHLH, WD40, and related transcription factors in flavonoid biosynthesis. Funct. Integr. Genom. 2013;13:75-98.
Not in our library10.1007/s10142-012-0301-4
141.
Ding B., Patterson E.L., Holalu S.V., Li J., Johnson G.A., Stanley L.E., Greenlee A.B., Peng F., Bradshaw H.D., Blinov M.L., et al. Two MYB proteins in a self-organizing activator-inhibitor system produce spotted pigmentation patterns. Curr. Biol. 2020;30:802-814.
Not in our library10.1016/j.cub.2019.12.067
142.
Regulatory Mechanisms of bHLH Transcription Factors in Plant Adaptive Responses to Various Abiotic Stresses · 2021
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143.
Li C.F., Zhu Y., Yu Y., Zhao Q.Y., Wang S.J., Wang X.C., Yao M.Z., Luo D., Li X., Chen L. Global transcriptome and gene regulation network for secondary metabolite biosynthesis of tea plant (Camellia sinensis). BMC Genom. 2015;16:560.
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144.
Qiu Z., Wang H., Li D., Yu B., Hui Q., Yan S., Huang Z., Cui X., Cao B. Identification of candidate HY5-dependent and-independent regulators of anthocyanin biosynthesis in tomato. Plant Cell Physiol. 2019;60:643-656.
Not in our library10.1093/pcp/pcy236
145.
Outchkourov N.S., Karlova R., Hölscher M., Schrama X., Blilou I., Jongedijk E., Simon C.D., van Dijk A.D.J., Bosch D., Hall R.D. Transcription factor-mediated control of anthocyanin biosynthesis in vegetative tissues. Plant Physiol. 2018;176:1862-1878.
Not in our library10.1104/pp.17.01662
146.
Malacarne G., Coller E., Czemmel S., Vrhovsek U., Engelen K., Goremykin V., Bogs J., Moser C. The grapevine VvibZIPC22 transcription factor is involved in the regulation of flavonoid biosynthesis. J. Exp. Bot. 2016;67:3509-3522.
Not in our library10.1093/jxb/erw181
147.
Singh D., Singh H., Singh N., Dwivedi S., Trivedi T.P. Tobacco HY5, NtHY5, positively regulates flavonoid biosynthesis and enhances salt stress tolerance. bioRxiv. 2022;1.
Not in our library10.1101/2022.01.05.475064
148.
Morishita T., Kojima Y., Maruta T., Nishizawa-Yokoi A., Yabuta Y., Shigeoka S. Arabidopsis NAC transcription factor, ANAC078, regulates flavonoid biosynthesis under high-light. Plant Cell Physiol. 2009;50:2210-2222.
Not in our library10.1093/pcp/pcp159
149.
An X.H., Tian Y., Chen K.Q., Liu X.J., Liu D.D., Xie X.B., Cheng C.G., Cong P.H., Hao Y.J. MdMYB9 and MdMYB11 are involved in the regulation of the JA-induced biosynthesis of anthocyanin and proanthocyanidin in apples. Plant Cell Physiol. 2015;56:650-662.
Not in our library10.1093/pcp/pcu205
150.
Skirycz A., Jozefczuk S., Stobiecki M., Muth D., Zanor M.I., Witt I., Mueller-Roeber B. Transcription factor AtDOF4; 2 affects phenylpropanoid metabolism in Arabidopsis thaliana. New Phytol. 2007;175:425-438.
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151.
Wang N., Liu W., Zhang T., Jiang S., Xu H., Wang Y., Zhang Z., Wang C., Chen X. Transcriptomic analysis of red-fleshed apples reveals the novel role of MdWRKY11 in flavonoid and anthocyanin biosynthesis. J Agric. Food Chem. 2018;66:7076-7086.
Not in our library10.1021/acs.jafc.8b01273
152.
Liu S., Wang L., Cao M., Pang S., Li W., Kato-Noguchi H., Jin B. Identification and characterization of long non-coding RNAs regulating flavonoid biosynthesis in Ginkgo biloba leaves. Ind. Crop. Prod. 2020;158:112980.
Not in our library10.1016/j.indcrop.2020.112980
153.
Liu X., Tang N., Xu F., Chen Z., Zhang X., Ye J., Liao Y., Zhang W., Kim S., Wu P., et al. SMRT and Illumina RNA sequencing reveal the complexity of terpenoid biosynthesis in Zanthoxylum armatum. Tree Physiol. 2022;42:664-683.
Not in our library10.1093/treephys/tpab114
154.
Ma X., Zhang X., Traore S.M., Xin Z., Yin D. Genome-wide identification and analysis of long noncoding RNAs (lncRNAs) during seed development in peanut (Arachis hypogaea L.). BMC Plant Biol. 2020;20:192.
Not in our library10.1186/s12870-020-02405-4
155.
Sharma A., Badola P.K., Bhatia C., Sharma D., Trivedi P.K. Primary transcript of miR858 encodes regulatory peptide and controls flavonoid biosynthesis and development in Arabidopsis. Nat. Plants. 2020;6:1262-1274.
Not in our library10.1038/s41477-020-00769-x
156.
Shen N., Wang T., Gan Q., Liu S., Wang L., Jin B. Plant flavonoids: Classification, distribution, biosynthesis, and antioxidant activity. Food Chem. 2022;383:132531.
Not in our library10.1016/j.foodchem.2022.132531
157.
Heat Shock Proteins: Dynamic Biomolecules to Counter Plant Biotic and Abiotic Stresses · 2019
No notice
158.
Bajaj R., Huang Y., Gebrechristos S., Mikolajczyk B., Brown H., Prasad R., Varma A., Kathryn E., Bushley. Transcriptional responses of soybean roots to colonization with the root endophytic fungus Piriformospora indica reveals altered phenylpropanoid and secondary metabolism. Sci. Rep. 2018;8:10227.
Not in our library10.1038/s41598-018-26809-3
159.
Rodziewicz P., Swarcewicz B., Chmielewska K., Wojakowska A., Stobiecki M. Influence of abiotic stresses on plant proteome and metabolome changes. Acta Physiol. Plant. 2014;36:1-19.
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160.
Ramakrishna A., Ravishankar G.A. Role of plant metabolites in abiotic stress tolerance under changing climatic conditions with special reference to secondary compounds. Clim. Change Plant Abiotic Stress Toler. 2013;26:705-726.
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161.
Mareri L., Parrotta L., Cai G. Environmental Stress and Plants. Int. J. Mol. Sci. 2022;23:5416.
Not in our library10.3390/ijms23105416
162.
Ahmed E., Arshad M., Khan M.Z., Amjad M.S., Ahmad S. Secondary metabolites and their multidimensional prospective in plant life. J. Pharm. Phytochem. 2017;6:205-214.
Not in our library
163.
Gupta A., Bano A., Rai S., Dubey P., Khan F., Pathak N., Sharma S. Plant Growth Promoting Rhizobacteria (PGPR): A sustainable agriculture to rescue the vegetation from the effect of biotic stress: A Review. Lett. Appl. NanoBiosci. 2021;10:2459-2465.
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164.
Singh V.K., Upadhyay R.S. The hypersensitive response: A case of cell death induction in plants. Int. J. Eng. Res. Technol. 2013;2:1828-1832.
Not in our library
165.
Thakker J.N., Patel S., Dhandhukia P.C. Induction of defense-related enzymes in banana plants: Effect of live and dead pathogenic strain of Fusarium oxysporum f. sp. cubense. Int. Schol. Res. Not. 2013;2013:601303.
Not in our library10.5402/2013/601303
166.
Sindhu S.S., Sehrawat A., Sharma R., Dahiya A. Biopesticides: Use of rhizosphere bacteria for biological control of plant pathogens. Def. Sci. J. 2016;1:135-148.
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167.
Molinari S. Natural genetic and induced plant resistance, as a control strategy to plant-parasitic nematodes alternative to pesticides. Plant Cell Rep. 2011;30:311-323.
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168.
Tuncsoy B. Nematicidal activity of silver nanomaterials against plant-parasitic nematodes. Silver Nanomaterials for Agri-Food Applications. 2021;527-548.
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169.
Oka Y., Koltai H., Bar-Eyal M., Mor M., Sharon E., Chet I., Spiegel Y. New strategies for the control of plant-parasitic nematodes. Pest Manag. Sci. 2000;56:983-988.
Not in our library10.1002/1526-4998(200011)56:11<983::aid-ps233>3.0.co;2-x
170.
Lindell K.J., Riley I.T., Davies K.A., Oldach K.H. Characterization of resistance to Pratylenus thorni (Nematoda) in wheat (Triticum aestivum): Attraction, tension, utility, and reproduction. Phytopathology. 2014;104:174-187.
Not in our library10.1094/phyto-12-12-0345-r
171.
A Phytochemical Perspective on Plant Defense Against Nematodes · 2020
Not checked
172.
Makhwedzhana M.M. Nematode Resistance and Resistance Mechanism in Sweet Potato Cultivars ‘Bophelo’, ‘Bosbok’ and Mvuvhelo’ to Meloidogyne incognita. Master’s Thesis. 2018.
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173.
Chin S., Behm C.A., Mathesius U. Functions of flavonoids in plant–nematode interactions. Plants. 2018;7:85.
Not in our library10.3390/plants7040085
174.
Lozano J., Smant G. Survival of plant-parasitic nematodes inside the host. Mol. Physiol. Basis Nematode Surviv. 2011;13:697-701.
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175.
Al-Muwayhi M.A.R. Biotic stress as a defense mechanism in soybean (Glycine max L.) toward microbial pathogen: Biochemical and physiological pathways study. Life Sci. J. 2020;17:24-36.
Not in our library
176.
Hammerschmidt R. How glyphosate affects plant disease development: It is more than enhanced susceptibility. Pest Manag. Sci. 2018;74:1054-1063.
Not in our library10.1002/ps.4521
177.
Walters D. Plant defense: Warding off attack by pathogens, herbivores and parasitic plants. Q. Rev. Biol. 2011;86:356-357.
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178.
Smant G., Jones J. Suppression of plant defences by nematodes. Genomics and Molecular Genetics of Plant-Nematode Interactions. 2011;273-286.
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179.
González-Fernández R., Prats E., Jorrín-Novo J.V. Proteomics of plant pathogenic fungi. J. Biomed. Biotechnol. 2010;2010:932527.
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180.
Suprapta D.N. Potential of microbial antagonists as biocontrol agents against plant fungal pathogens. J. ISSAAS. 2012;18:1-8.
Not in our library
181.
Parmar N., Singh K.H., Sharma D., Singh L., Kumar P., Nanjundan J., Khan Y.J., Chauhan D.K., Thakur A.K. Genetic engineering strategies for biotic and abiotic stress tolerance and quality enhancement in horticultural crops: A comprehensive review. 3 Biotech. 2017;7:1-35.
Not in our library10.1007/s13205-017-0870-y
182.
Saddique M., Kamran M., Shahbaz M. Differential responses of plants to biotic stress and the role of metabolites. Plant Metabolites and Regulation under Environmental Stress. 2018;69-87.
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183.
Meena M., Yadav G., Sonigra P., Nagda A., Mehta T., Swapnil P., Harish, Marwal A. Role of elicitors to initiate the induction of systemic resistance in plants to biotic stress. Plant Stress. 2022;5:100103.
Not in our library10.1016/j.stress.2022.100103
184.
Alkahtani M., Omer S.A., El-Naggar M.A., Abdelkareem E.M., Mahmoud M.A. Pathogenesis-related protein and phytoalexin induction against cucumber powdery mildew by elicitors. Int. J. Plant Pathol. 2011;2:63-71.
Not in our library10.3923/ijpp.2011.63.71
185.
Farahat G. Potential Impacts of Copper Sulfate and Sodium Silicate Salts of Maize Late Wilt Disease and Synthase of Anti-defense Compounds. Environ. Biodivers. Soil Secur. 2019;3:269-282.
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186.
Ortuño A., Díaz L., Alvarez N., Porras I., Garcia-Lidon A., Del Rio J.A. Comparative study of flavonoid and scoparone accumulation in different Citrus species and their susceptibility to Penicillium digitatum. Food Chem. 2011;125:232-239.
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187.
François G.A., de Moraes Pontes J.G., Pereira A.K., Fill T.P. Exploring the Citrus Sour Rot pathogen: Biochemical aspects, virulence factors, and strategies for disease management-a review. Fungal Biol. Rev. 2022;41:70-83.
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188.
Del Río J.A., Gómez P., Baidez A.G., Arcas M.C., Botía J.M., Ortuño A. Changes in the levels of polymethoxyflavones and flavanones as part of the defense mechanism of Citrussinensis (cv. Valencia Late) fruits against Phytophthora citrophthora. J. Agric. Food Chem. 2004;52:1913-1917.
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189.
Ortuno A., Arcas M.C., Botia J.M., Fuster M.D., Del Río J.A. Increasing resistance against Phytophthora citrophthora in tangelo Nova fruits by modulating polymethoxyflavones levels. J. Agric. Food Chem. 2002;50:2836-2839.
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Boué S.M., Carter C.H., Ehrlich K.C., Cleveland T.E. Induction of the soybean phytoalexins coumestrol and glyceollin by Aspergillus. J. Agric. Food Chem. 2000;48:2167-2172.
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Xie Y., Yang W., Tang F., Chen X.Q., Ren L.C. Antibacterial activities of flavonoids: Structure-activity relationship and mechanism. Curr. Med. Chem. 2015;22:132-149.
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192.
Górniak I., Bartoszewski R., Króliczewski J. Comprehensive review of antimicrobial activities of plant flavonoids. Phytochem. Rev. 2019;18:241-272.
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193.
Tiku A.R. Antimicrobial compounds (phytoanticipins and phytoalexins) and their role in plant defense. Co-Evolution of Secondary Metabolites. 2020;845-868.
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194.
Sharma I., Thakur A., Sharma A., Singh N., Kumar R., Sharma A. Phytoalexins: Implications in Plant Defense and Human Health. Plant Secondary Metabolites. 2022;329-353.
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195.
Gnanamanickam S.S., Smith D.A. Selective toxicity of isoflavonoid phytoalexins to gram-positive bacteria. Phytopathology. 1980;70:894.
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196.
Lyon F.M., Wood R.K.S. Production of phaseollin, coumestrol and related compounds in bean leaves inoculated with Pseudomonas spp. Physiol. Plant Pathol. 1975;6:117-124.
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197.
Li P., Ruan Z., Fei Z., Yan J., Tang G. Integrated transcriptome and metabolome analysis revealed that flavonoid biosynthesis may dominate the resistance of Zanthoxylum bungeanum against stem canker. J. Agric. Food Chem. 2021;69:6360-6378.
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198.
Sato M., Tanaka H., Tani N., Nagayama M., Yamaguchi R. Different antibacterial actions of isoflavones isolated from Erythrina poeppigiana against methicillin-resistant Staphylococcus aureus. Lett. Appl. Microbiol. 2006;43:243-248.
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199.
de Barros K.M.A., Sardi J.C.O., Maria-Neto S., Macedo A.J., Ramalho S.R. A new Kunitz trypsin inhibitor from Erythrina poeppigiana exhibits antimicrobial and antibiofilm properties against bacteria. Biomed. Pharmacother. 2021;144:112198.
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200.
Native Mass Spectrometry: What is in the Name? · 2016
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201.
Pisoschi A.M., Pop A. The role of antioxidants in the chemistry of oxidative stress: A review. Eur. J. Medi. Chem. 2015;97:55-74.
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202.
Saewan N., Jimtaisong A. Photoprotection of natural flavonoids. J. Appl. Pharm. Sci. 2013;3:129-141.
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203.
Ferreyra M.L.F., Serra P., Casati P. Recent advances on the roles of flavonoids as plant protective molecules after UV and high light exposure. Physiol. Plant. 2021;173:736-749.
Not in our library10.1111/ppl.13543
204.
Flavonoids as Antioxidants and Developmental Regulators: Relative Significance in Plants and Humans · 2013
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205.
Ferdinando M.D., Brunetti C., Fini A., Brunetti C., Di Ferdinando M. Flavonoids as antioxidants in plants under abiotic stresses. Abiotic Stress Responses Plants. 2012;159-179.
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206.
Casati P., Walbot V. Differential accumulation of maysin and rhamnosylisoorientin in leaves of high-altitude landraces of maize after UV-B exposure. Plant Cell Environ. 2005;28:788-799.
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207.
Casasa M.I., Falcone-Ferreyrac M.L., Nan J., Mejía-Guerra M.K., Rodríguez E., Wilson T., Engelmeier J., Casati P., Grotewold E. Identification and characterization of maize salmon silks genes involved in 1 insecticidal maysin biosynthesis. Plant Cell. 2016;28:1297-1309.
Not in our library10.1105/tpc.16.00003
208.
Righini S., Rodriguez E.J., Berosich C., Grotewold E., Casati P., Ferreyra M.L.F. Apigenin produced by maize flavone synthase I and II protects plants against UV-B-induced damage. Plant Cell Environ. 2019;42:495-508.
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209.
Honda C., Moriya S. Anthocyanin biosynthesis in apple fruit. Horticult. J. 2018;87:305-314.
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210.
Tohge T., de Souza L.P., Fernie A.R. On the natural diversity of phenylacylated-flavonoid and their in planta function under conditions of stress. Phytochem. Rev. 2018;17:279-290.
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Benavente-Garcıa O., Castillo J., Lorente J., Ortuño A., Del Rio J.A. Antioxidant activity of phenolics extracted from Olea europaea L. leaves. Food Chem. 2000;68:457-462.
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212.
Galvez-Valdivesio G., Mullineaux P. The role of reactive oxygen species in signalling from chloroplasts to the nucleus. Physiol. Plant. 2010;138:430-439.
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213.
Pourcel L., Routaboul J.M., Cheynier V., Lepiniec L., Debeaujon I. Debeaujon, Flavonoid oxidation in plants: From biochemical properties to physiological functions. Trends Plant Sci. 2006;12:29-36.
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214.
Laoué J., Fernandez C., Ormeño E. Plant flavonoids in mediterranean species: A focus on flavonols as protective metabolites under climate stress. Plants. 2022;11:172.
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215.
Li W., Tan L., Zou Y., Tan X.Q., Huang J.C., Chen W., Tang Q. The effects of ultraviolet A/B treatments on anthocyanin accumulation and gene expression in dark-purple tea cultivar ‘Ziyan’(Camellia sinensis). Molecules. 2020;25:354.
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216.
Dong N.Q., Lin H.X. Contribution of phenylpropanoid metabolism to plant development and plant–environment interactions. J. Integr. Plant Biol. 2021;63:180-209.
Not in our library10.1111/jipb.13054
217.
Chinnusamy V., Zhu J.K., Sunkar R. Gene regulation during cold stress acclimation in plants. Plant Stress Tolerance: Methods and Protocols. 2010;39-55.
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218.
Song X., Diao J., Ji J., Wang G., Guan C., Jin C., Wang Y. Molecular cloning and identification of a flavanone 3-hydroxylase gene from Lycium chinense, and its overexpression enhances drought stress in tobacco. Plant Physiol. Biochem. 2016;98:89-100.
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219.
Li H., Li D., Yang Z., Zeng Q., Luo Y., He N. Flavones produced by mulberry flavone synthase type I constitute a defense line against the ultraviolet-B stress. Plants. 2020;9:215.
Not in our library10.3390/plants9020215
220.
Kim J., Lee W.J., Vu T.T., Jeong C.Y., Hong S.W., Lee H. High accumulation of anthocyanins via the ectopic expression of AtDFR confers significant salt stress tolerance in Brassica napus L. Plant Cell Rep. 2017;36:1215-1224.
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221.
Ma D., Sun D., Wang C., Li Y., Guo T. Expression of flavonoid biosynthesis genes and accumulation of flavonoid in wheat leaves in response to drought stress. Plant Physiol. Biochem. 2014;80:60-66.
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222.
Transcriptional Factors Regulate Plant Stress Responses Through Mediating Secondary Metabolism · 2020
No notice
223.
Li H., Yue H., Xie J., Bu J., Li L., Xin X., Zhao Y., Zhang H., Yang L., Wang J., et al. Transcriptomic profiling of the high-vigour maize (Zea mays L.) hybrid variety response to cold and drought stresses during seed germination. Sci. Rep. 2021;11:19345.
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224.
Song Z., Yang Q., Dong B., Li N., Wang M., Du T., Liu N., Niu L., Jin H., Meng D. Melatonin enhances stress tolerance in pigeon pea by promoting flavonoid enrichment, particularly luteolin in response to salt stress. J. Exp. Bot. 2022;73:5992-6008.
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225.
Fang H., Qi X., Li Y., Yu X., Liu X. De novo transcriptomic analysis of light-induced flavonoid pathway, transcription factors in the flower buds of Lonicera japonica. Trees. 2020;34:267-283.
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226.
Babitha K.C., Vemanna R.S., Nataraja K.N., Udayakumar M. Overexpression of EcbHLH57 transcription factor from Eleusine coracana L. in tobacco confers tolerance to salt, oxidative and drought stress. PLoS ONE. 2015;10:e0137098.
Not in our library10.1371/journal.pone.0137098
227.
Li F., Guo S., Zhao Y., Chen D., Chong K., Xu Y. Overexpression of a homopeptide repeat-containing bHLH protein gene (OrbHLH001) from Dongxiang Wild Rice confers freezing and salt tolerance in transgenic Arabidopsis. Plant Cell Rep. 2010;29:977-986.
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228.
Salehi-Lisar S.Y., Bakhshayeshan-Agdam H. Drought stress in plants: Causes, consequences, and tolerance. Drought Stress Tolerance in Plants. 2016;1-16.
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229.
Chalker-Scott L. Environmental significance of anthocyanins in plant stress responses. Photochem. Photobiol. 1999;70:1-9.
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230.
Aloui A., Dumas-Gaudot E., Daher Z., van Tuinen D., Aschi-Smit S., Morandi D. Influence of arbuscular mycorrhizal colonisation on cadmium induced Medicago truncatula root isoflavonoid accumulation. Plant Physiol. Biochem. 2012;60:233-239.
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231.
Shin D.H., Choi M.G., Kang C.S., Par C.S., Choi S.B., Park Y.I. Overexpressing the wheat dihydroflavonol 4-reductase gene TaDFR increases anthocyanin accumulation in an Arabidopsis dfr mutant. Genes Genom. 2016;38:333-340.
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232.
Li C., Liu S., Yao X., Wang J., Wang T., Zhang Z., Zhang P., Chen K. PnF3H, a flavanone 3-hydroxylase from the Antarctic moss Pohlia nutans, confers tolerance to salt stress and ABA treatment in transgenic Arabidopsis. Plant Growth Regul. 2017;83:489-500.
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233.
Jeon J., Kim J.K., Wu Q., Park S.U. Effects of cold stress on transcripts and metabolites in tartary buckwheat (Fagopyrum tataricum). Environ. Exp. Bot. 2018;155:488-496.
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234.
Song Y., Feng J., Liu D., Long C. Different Phenylalanine Pathway Responses to Cold Stress Based on Metabolomics and Transcriptomics in Tartary Buckwheat Landraces. J. Agric. Food Chem. 2022;70:687-698.
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235.
Seleiman M.F., Aslam M.T., Alhammad B.A., Hassan M.U., Maqbool R., Chattha M.U., Khan I., Gitari H.I., Uslu O.S., Roy R. Salinity stress in wheat: Effects, mechanisms and management strategies. Phyton. 2022;91:667.
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236.
Hu J., Fang H., Wang J., Yue X., Chen X. Ultraviolet B-induced MdWRKY72 expression promotes anthocyanin synthesis in apple. Plant Sci. 2020;292:110377.
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237.
Hussain S.S., Kayani M.A., Amjad M. Transcription factors as tools to engineer enhanced drought stress tolerance in plants. Biotechnol. Progr. 2011;27:297-306.
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238.
Wang C.T., Ru J.N., Liu Y.W., Yang J.F., Li M., Xu Z.S., Fu J.D. The maize WRKY transcription factor ZmWRKY40 confers drought resistance in transgenic Arabidopsis. Int. J. Mol. Sci. 2018;19:2580.
Not in our library10.3390/ijms19092580
239.
Li X.D., Zhuang K.Y., Liu Z.M., Yang D.Y., Ma N.N., Meng Q.W. Overexpression of a novel NAC-type tomato transcription factor, SlNAM1, enhances the chilling stress tolerance of transgenic tobacco. J. Plant Physiol. 2016;204:54-65.
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240.
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 Tissue Organ Cul. 2016;125:387-398.
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241.
Jiao X., Teng Y., Zhan Y., Wu J., Lin X. Soil heavy metal pollution and risk assessment in Shenyang industrial district, Northeast China. PLoS ONE. 2015;10:e0127736.
Not in our library10.1371/journal.pone.0127736
242.
Kumar M., Chauhan A.S., Yusuf M.A., Sanyal I., Chauhan P. Transcriptome sequencing of chickpea (Cicer arietinum L.) genotypes for identification of drought-responsive genes under drought stress condition. Plant Mol. Biol. Rep. 2019;37:186-203.
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243.
Lijuan C., Huiming G., Yi L., Hongmei C. Chalcone synthase EaCHS1 from Eupatorium adenophorum functions in salt stress tolerance in tobacco. Plant Cell Rep. 2015;34:885-894.
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244.
Shi H., Chan Z. The cysteine2/histidine2-type transcription factor ZINC FINGER of ARABIDOPSIS THALIANA 6-activated C-REPEAT-BINDING FACTOR pathway is essential for melatonin-mediated freezing stress resistance in Arabidopsis. J. Pineal Res. 2014;57:185-191.
Not in our library10.1111/jpi.12155
245.
Thakur P., Kumar S., Malik J.A., Berger J.D., Nayyar H. Cold stress effects on reproductive development in grain crops: An overview. Environ. Exp. Bot. 2010;67:429-443.
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246.
Bhattacharya A. Effect of low-temperature stress on germination, growth, and phenology of plants: A review. Physiological Processes in Plants Under Low Temperature Stress. 2022;1-106.
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247.
Liu X., Zhou Y., Xiao J., Bao F. Effects of chilling on the structure, function and development of chloroplasts. Front. Plant Sci. 2018;9:1715.
Not in our library10.3389/fpls.2018.01715
248.
Chloroplast RNA-Binding Protein RBD1 Promotes Chilling Tolerance through 23S rRNA Processing in Arabidopsis. · 2016
Not checked
249.
Gan P., Liu F., Li R., Wang S., Luo J., Pearce R.S. Plant freezing and damage. Ann. Bot. 2001;87:417-424.
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250.
Puyaubert J., Baudouin E. New clues for a cold case: Nitric oxide response to low temperature. Plant Cell Environ. 2014;37:2623-2630.
Not in our library10.1111/pce.12329
251.
Ding Y., Shi Y., Yang S. Advances and challenges in uncovering cold tolerance regulatory mechanisms in plants. New Phytol. 2019;222:1690-1704.
Not in our library10.1111/nph.15696
252.
Mayr S., Ameglio T. Freezing stress in tree xylem. Prog. Bot. 2016;77:381-414.
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253.
Flavonoids are determinants of freezing tolerance and cold acclimation in Arabidopsis thaliana · 2016
No notice
254.
Zhang Y., Yang L., Hu H., Yang J., Cui J., Wei G., Xu J. Transcriptome and metabolome changes in Chinese cedar during cold acclimation reveal the roles of flavonoids in needle discoloration and cold resistance. Tree Physiol. 2022;9:1858-1875.
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255.
Li S.J., Bai Y.C., Li C.L., Yao H.P., Chen H., Zhao H.X., Wu Q. Anthocyanins accumulate in tartary buckwheat (Fagopyrum tataricum) sprout in response to cold stress. Acta Physiol. Plant. 2015;37:159.
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256.
Chen H., Jiang J.G. Osmotic adjustment and plant adaptation to environmental changes related to drought and salinity. Environ. Rev. 2010;18:309-319.
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257.
Regulation of Reactive Oxygen Species and Antioxidant Defense in Plants under Salinity · 2021
No notice
258.
Qadir M., Tubeileh A., Akhtar J., Larbi A., Khan M.A. Productivity enhancement of salt-affected environments through crop diversification. Land Degrad. Dev. 2008;19:429-453.
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259.
Shrivastava P., Kumar R. Soil salinity: A serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J. Biol. Sci. 2015;22:123-131.
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260.
Safdar H., Amin A., Shafiq Y., Ali A. A review: Impact of salinity on plant growth. Nat. Sci. 2019;17:34-40.
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261.
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.
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262.
Integrated de novo Analysis of Transcriptional and Metabolic Variations in Salt-Treated Solenostemma argel Desert Plants · 2021
Not checked
263.
Wang X., Dai W.W., Liu C., Yangchen Y.C., Gao R.F., Chen Y.Y., Yan H. Evaluation of physiological coping strategies and quality substances in purple sweetpotato under different salinity levels. Genes. 2022;13:1350.
Not in our library10.3390/genes13081350
264.
Jia T., An J., Liu Z., Chen J., Yu B. Salt stress induced soybean GmIFS1 expression and isoflavone accumulation and salt tolerance in transgenic soybean cotyledon hairy roots and tobacco. Plant Cell Tissue Organ Cul. 2017;128:469-477.
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265.
Farooq M., Wahid A., Kobayashi N., Fujita D., Basra S.M.A. Plant drought stress: Effects, mechanisms and management. Sustainable Agriculture. 2009;153-188.
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266.
Nabi R.B.S., Tayade R., Hussain A., Kulkarni K.P., Imran Q.M., Mun B.G., Yun B.W. Nitric oxide regulates plant responses to drought, salinity, and heavy metal stress. Environ. Exp. Bot. 2019;161:120-133.
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267.
Chaudhry S., Sidhu G.P.S. Climate change regulated abiotic stress mechanisms in plants: A comprehensive review. Plant Cell Rep. 2021;41:1-31.
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268.
Drought Resistance by Engineering Plant Tissue-Specific Responses · 2020
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269.
Iqbal A., Fahad S., Iqbal M., Alamzeb M., Ahmad A., Anwar S., Khan A.A., Arif M., Saeed M., Song M. Special adaptive features of plant species in response to drought. Salt and Drought Stress Tolerance in Plants. 2020;77-118.
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270.
Amnan M.A.M., Aizat W.M., Khaidizar F.D., Tan B.C. Drought stress induces morpho-physiological and proteome changes of Pandanus amaryllifolius. Plants. 2022;11:221.
Not in our library10.3390/plants11020221
271.
Salsinha Y.C.F., Indradewa D., Purwestri Y.A., Rachmawati D. Leaf physiological and anatomical characters contribute to drought tolerance of Nusa Tenggara Timur local rice cultivars. J. Crops Sci. Biotechnol. 2021;24:337-348.
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272.
Lv Z., Zhang C., Shao C., Liu B., Shen C. Research progress on the response of tea catechins to drought stress. J. Sci. Food Agric. 2021;101:5305-5313.
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273.
Hinojosa-Gómez J., Martín-Hernández C.S., Heredia J.B., León-Félix J., Osuna-Enciso T., Muy-Rangel M.D. Anthocyanin induction by drought stress in the calyx of roselle cultivars. Molecules. 2020;25:1555.
Not in our library10.3390/molecules25071555
274.
Gholamreza A., Shokrpour M., Karami L., Salami S.A. Prolonged water deficit stress and methyl jasmonate-mediated changes in metabolite profile, flavonoid concentrations and antioxidant activity in peppermint (Mentha piperita L.). Not. Bot. Horti Agrobo. 2019;47:70-80.
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275.
Mechri B., Tekaya M., Hammami M., Chehab H. Effects of drought stress on phenolic accumulation in greenhouse-grown olive trees (Olea europaea). Biochem. Syst. Ecol. 2020;92:104112.
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276.
Li X., Zhang X., Liu G., Tang Y., Lv J. The spike plays important roles in the drought tolerance as compared to the flag leaf through the phenylpropanoid pathway in wheat. Plant Physiol. Biochem. 2020;152:100-111.
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277.
Kalaivanan D., Ganeshamurthy A.N. Mechanisms of heavy metal toxicity in plants. Abiotic Stress Physiology of Horticultural Crops. 2016;85-102.
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278.
Ghori N.H., Ghori T., Hayat M.Q., Imadi S.R., Gul A., Altay V., Ozturk M. Heavy metal stress and responses in plants. Int. J. Environ. Sci. Technol. 2019;16:1807-1828.
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279.
Nagajyoti P.C., Lee K.D., Sreekanth T.V.M. Heavy metals, occurrence and toxicity for plants: A review. Environ. Chem. Lett. 2010;8:199-216.
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280.
Asati A., Pichhode M., Nikhil K. Effect of heavy metals on plants: An overview. Int. J. Appl. Innov. Eng. Manag. 2016;5:56-66.
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281.
Khan M., Aymen U., Mir A.H., Tiwari A., Prasad S.M., Singh J., Ramamurthy P.C., Singh R., Singh S., Parihar P. Understanding Heavy Metal Stress in Plants Through Mineral Nutrients. Heavy Metals in Plants Physiological to Molecular Approach. 2022;281-309.
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282.
Bhaduri A.M., Fulekar M.H. Antioxidant enzyme responses of plants to heavy metal stress. Rev. Environ. Sci. Bio/Technol. 2012;11:55-69.
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283.
Mahmud J.A., Bhuyan M.H.M., Anee T.I., Nahar K., Fujita M., Hasanuzzaman M. Reactive oxygen species metabolism and antioxidant defense in plants under metal/metalloid stress. Plant Abiotic Stress Tolerance. 2019;221-257.
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284.
Pisoschi A.M., Pop A., Iordache F., Stanca L., Predoi G., Serban A.I. Oxidative stress mitigation by antioxidants-an overview on their chemistry and influences on health status. Eur. J. Med. Chem. 2021;209:112891.
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285.
Jamla M., Khare T., Joshi S., Patil S., Kumar V. Omics approaches for understanding heavy metal responses and tolerance in plants. Curr. Plant Biol. 2021;27:100213.
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286.
Zhang X., Yang H., Schaufelberger M., Li X., Ren Z. Role of flavonol synthesized by nucleus FLS1 in Arabidopsis resistance to Pb stress. J. Agric. Food Chem. 2020;68:9646-9653.
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287.
Dai L.P., Dong X.J., Ma H.H. Molecular mechanism for cadmium-induced anthocyanin accumulation in Azolla imbricata. Chemospher. 2012;87:319-325.
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288.
Barrows G., Sexton S., Zilberman D. Agricultural biotechnology: The promise and prospects of genetically modified crops. J. Econ. Perspect. 2014;28:99-120.
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289.
Sedeek K.E.M., Mahas A., Mahfouz M. Plant genome engineering for targeted improvement of crop traits. Front. Plant Sci. 2019;10:114.
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290.
Basu S.K., Dutta M., Goyal A., Bhowmik P.K., Kumar J., Nandy S., Scagliusi S.M., Prasad R. Is genetically modified crop the answer for the next green revolution? GM Crops. 2010;1:68-79.
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291.
Wani S.H., Sah S.K., Hossain M.A., Kumar V., Balachandran S.M. Transgenic approaches for abiotic stress tolerance in crop plants. Advances in Plant Breeding Strategies: Agronomic, Abiotic and Biotic Stress Traits. 2016;345-396.
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292.
Zhang X.H., Zheng X.T., Sun B.Y., Peng C.L., Chow W.S. Over-expression of the CHS gene enhances resistance of Arabidopsis leaves to high light. Environ. Exp. Bot. 2018;154:33-43.
Not in our library10.1016/j.envexpbot.2017.12.011
293.
A Moss 2-Oxoglutarate/Fe(II)-Dependent Dioxygenases (2-ODD) Gene of Flavonoids Biosynthesis Positively Regulates Plants Abiotic Stress Tolerance · 2022
Not checked
294.
Zheng X.T., Chen Y.-H.L., Zhang X.H., Cai M.L., Yu Z.C., Peng C.L. ANS-deficient Arabidopsis is sensitive to high light due to impaired anthocyanin photoprotection. Funct. Plant Biol. 2019;46:756-765.
Not in our library10.1071/fp19042
295.
Li X.-J.W., Wang Y., Yan F., Li J.W., Zhao Y., Zhao X., Zhai Y., Wang Q.Y. Overexpression of soybean R2R3-MYB transcription factor, GmMYB12B2, and tolerance to UV radiation and salt stress in transgenic Arabidopsis. Genet. Mol. Res. 2016;15:gmr.15026573.
Not in our library10.4238/gmr.15026573
296.
Chen S., Li D., Chen S., He J., Wang Z., Yang G., Lu Z. Identifying and expression analysis of WD40 transcription factors in walnut. Plant Genom. 2022;15:e20229.
Not in our library10.1002/tpg2.20229
297.
Wang A., Zhu M., Luo Y., Liu Y., Li R., Kou M., Wang X., Zhang Y., Meng X., Zheng Y., et al. A sweet potato cinnamate 4-hydroxylase gene, IbC4H, increases phenolics content and enhances drought tolerance in tobacco. Acta Physiol. Plant. 2017;39:276.
Not in our library10.1007/s11738-017-2551-1
298.
Ku Y.S., Ng M.S., Cheng S.S., Lo A.W.Y., Xiao Z., Shin T.S., Chung G., Lam H.M. Understanding the composition, biosynthesis, accumulation and transport of flavonoids in crops for the promotion of crops as healthy sources of flavonoids for human consumption. Nutrients. 2020;12:1717.
Not in our library10.3390/nu12061717
299.
Meng C., Zhang S., Deng Y.S., Wang G.D., Kong F.Y. Overexpression of a tomato flavanone 3-hydroxylase-like protein gene improves chilling tolerance in tobacco. Plant Physiol. Biochem. 2015;96:388-400.
Not in our library10.1016/j.plaphy.2015.08.019
300.
Ai T.N., Naing A.H., Yun B.W., Lim S., Kim C.K. Overexpression of RsMYB1 enhances anthocyanin accumulation and heavy metal stress tolerance in transgenic petunia. Front. Plant Sci. 2018;9:1388.
Not in our library10.3389/fpls.2018.01388

Cited by papers we hold 1

A Review of Classification, Biosynthesis, Biological Activities and Potential Applications of Flavonoids · 2023
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