Diverse Physiological Roles of Flavonoids in Plant Environmental Stress Responses and Tolerance
Abstract
:1. Introduction
2. Chemistry and Biosynthesis of Flavonoids
3. Antioxidant Properties of Flavonoids
Abiotic Stress | Plant Species | Antioxidant Response of Flavonoids | References |
---|---|---|---|
UV-B radiation | Medicago sativa | Increased content of flavonoid compound induces enhanced antioxidant capacity of the plant. | [57] |
UV-B radiation | Kalanchoe pinnata | Increases total flavonoid and quercitrin content, which have antioxidant properties to protect the plant. | [58] |
UV-B stress and drought | Populus tremula × P. tremuloides | Transgenic line of poplar with high proanthocyanidins content displayed lower hydrogen peroxide content. | [59] |
Salinity | Zea maize | Improved plant performance under salt stress through antioxidant activities. | [60] |
Salinity | Arabidopsis thaliana | CrUGT87A1, a UDP-sugar glycosyltransferases (UGTs) gene, improved salt tolerance by increasing antioxidant capacity resulting from the accumulation of flavonoids. | [61] |
Salinity | Amaranthus tricolor | Increases flavonoid content, which showed the potent antioxidant activity in scavenging ROS. | [62] |
Salinity | Amaranthus lividus | Increases flavonoid content and the antioxidant capacity of leaves, total flavonoid content scavenged ROS. | [63] |
Water stress | Chrysanthemum morifoilum | Increases flavonoids (rutin, quercetin, apigenin, and luteolin) and enhanced antioxidant activity. | [64] |
Drought | Arabidopsis thaliana | Increase in total flavonoid content followed by an increase in antioxidant activity. | [65] |
Drought | Cistus clusii | prevented oxidative damage. | [66] |
Drought | Swingle citrumelo | Proline accumulation was concomitant with an increase in antioxidant activity. | [67] |
Temperature stress | Solanum viarum Dunal | Flavonoids inhibited ROS-mediated oxidative damage. | [68] |
Heat and salinity | Solanum Lycopersicon | Lower antioxidative damage was observed following a high accumulation of flavonols. | [69] |
Cadmium stress | Trigonella foenum-graecum | H2S-induced polyamines accumulation was concomitant with an increase in ROS-detoxification capacity. | [70] |
Cadmium stress | Solanum Lycopersicon | Nitric oxide-induced increase in flavonols resulted in improved antioxidant capacity. | [71] |
Lead stress | Tritium aestivum | Accumulation of proline was concomitant with a lower level of lipid peroxidation. | [72] |
4. Flavonoids-Mediated Defenses against Abiotic Stress
Abiotic Stress | Concentration/Levels | Duration of Stress | Plant Species | Flavonoids Level under Stress | References |
---|---|---|---|---|---|
Salinity | 50 and 100 mM NaCl | 35 days | Amaranthus lividus | An increase was observed in total flavonoid content by 31%. | [77] |
Salinity | 200 mM NaCl | 3 weeks | Apocynum venetum L. | The total flavonoid content and dihydroquercetin decreased by 20.46% to 23.08%, but an increase in flavonols (quercetin and kaempferol) by 1.6-fold and 2.2-fold was detected in comparison to control. | [78] |
Drought | Stop watering | 5 days | Arabidopsis thaliana L. | Quercetin 3-O-glucoside and cyanidin 3-O-glucoside exhibited approximately10-fold higher activity than kaempferol 3-O-glucoside, whereas a slight reduction in total flavonoid content was observed. | [79] |
Drought | Osmotic potential of 0.49 MPa | 48 h | Triticum aestivum L. | Significant increase in total flavonoid content was detected by 143% in cultivars aikang 58 compared with Chinese spring (115%). | [80] |
Drought | Soil water content 25% (±2.5%) | At three-leaf seedling stage | Zea mays L. | Flavonol in guard cells was observed 1.7-fold higher compared to control. | [81] |
Copper | 200 mg L−1 | 35 days | Belamcanda chinensis | Increased generation of 11 kinds of flavonoids. | [82] |
Copper and Zinc | 200–500 ppm | 28 days | (Lycopersicon esculentum Mill | Accumulation of flavonoids increased (1.44, 0.93 mg QE/g DW) compared to the control (0.18, 0.13 mg QE/g DW) in roots and leaves, respectively. | [83] |
UV-B and drought | 40% drought-stressed | 8 weeks | Ligustrum vulgare L. | Increases in the biosynthesis of quercetin-3-O-rutinoside, luteolin 7-O-glucoside, and echinacosid were observed. | [53] |
Extreme temperature and high CO2 levels | Light intensity 700 PAR and ambient CO2 (400 µmol mol−1) | 35–39 days | Lactuca sativa L. | Increased accumulation of quercetin-3-O-glucoside, quercetin-3-O-glucuronide, luteolin7-O-glucoside, cyanidin derivatives (61%), and cyanidin-3-O-glucoside (28%), while lower accumulations of kaempferol, myricetin, quercitrin (99–94%), and rutin were found under high light condition. Total flavonoid content increased by 7.5-fold in comparison to control. | [84] |
Stress | Stress Level | Duration of Stress | Plant Species | Flavonoids Modulation | Function of Flavonoids | Reference |
---|---|---|---|---|---|---|
Drought | Drought (mild drought stress) | 24 h | Tea (Camellia sinensis) | Accumulation phenylalanine ammonia-lyase (PAL), cinnamic acid 4-hydroxylase (C4H), 4-coumarateCoA ligase (4CL), chalcone synthase (CHS), and dihydrofavonol 4-reductase (DFR). | Increase in flavonoid content was concomitant with stress tolerance in plant. | [85] |
Drought | 15–25% of soil water-holding capacity | 8 days | Tea (C. sinensis) | Accumulation of endogenous flavonoids, including: C4H, CHS, F3′5′H, F3H, kaempferol, quercetin, and myricetin triggered by fulvic acid. | Increase in flavonoid content took part in improved tolerance of plants against drought. | [86] |
Drought | 8% PEG 6000 | 7 days | Maize (Zea mays) Pigeon pea (Cajanus cajan) | Accumulation of endogenous flavonoids, including: genistein, genistin, and pterostilbene. | ABA and CcMYB114 improve drought tolerance by regulating the accumulation of flavonoids. | [81,87] |
Drought | Stopped watering | 3 weeks | Arabidopsis (A. thaliana) | Accumulation of endogenous flavonoids triggered by ectopic expression of Arabidopsis glycosyltransferase gene (UGT76E11). | Activation of stress-related transcription factors. | [88] |
Salt | 300 mM NaCl | 14 days | Arabidopsis (A. thaliana) | Accumulation of endogenous flavonoids including: chalcone, dihydrokaempferole, and quercetin. | Act in MYB111-regulated salt stress response. | [89] |
Salt | 100, 150, and 200 mM NaCl | 19 days | Maize (Z. mays) | Exogenous application of α-tocopherol in combination with selenium (Na2SeO4 (0.5 mM) + a-tocopherol (200 ppm)). | Improved plant performance under salt stress through antioxidant defense. | [60] |
Salt | 150 mM NaCl | 5 days | Tomato (Solanum Lycopersicon L.) | Exogenous application of vanillic acid (4- hydroxy-3-methoxy benzoic acid) (50 μM). | Increase in the activity of AsA-GSH cycle and glyoxalase system and a further increase in accumulation of osmolytes. Improved K+ accumulation and restricted Na+ accumulation. Increase in superoxide dismutase (SOD), catalase (CAT), and ascorbic acid (AsA). | [90] |
Salt | 100 mM NaCl | 8 days | Bean (Phaseolus vulgaris) | Exogenous application of naringenin (0.1–0.4 mM). | Regulation of cellular redox, chloroplast antioxidant system, and photosynthesis. | [91] |
Heavy metals | 150 mg L−1 of Pb2 þ (which corresponds to 724 μM Pb(NO3)2) | Incubated for 2 h | Lupin | Incubation of seedlings with catechin before exposure to lead stress (5, 10, and 20 μg mL−1 of catechin equivalents). | Increased root growth and reduced accumulation of ROS, lipid peroxidation, and cell death. | [92] |
Heavy metals | Wastewater | 100 days | Lettuce and turnip | Accumulation of endogenous flavonoids, including putrescine and spermidine. | Counteract the oxidative stress. | [93] |
High temperature | 37 °C (day), 25 °C (night) | During growth period | Tomato (Solanum Lycopersicon L.) | Accumulation of endogenous flavonoids. | Reducing the abundance of ROS, enhancing fertility. | [94] |
High temperature | Moderate (36 °C/24 °C day/night) or severe (42 °C/26 °C day/night) | During the growth period since the pod’s color changed to an individual level | Soybean (Glycine max) | Accumulation of endogenous flavonoids, including tocopherols, flavonoids, phenylpropanoids, and ascorbate precursors. | Scavenging of heat-induced ROS damage during seed maturity. | [95] |
Air pollutant | Sulfur dioxide (SO2), NO2, carbon monoxide (CO), hydrocarbons (HC), and airborne particulate material (APM) | During growth period | Spartium junceum L., Lagerstroemia indica L., Th uja orientalis L., and Petunia hybrida L. w | Accumulation of endogenous flavonoids. | Reduced ROS accumulation in pollen grain and improved development of pollen tube and germination. | [96] |
Air pollutant | O3 stress (300 nL L−1) | 6 h | Medicago truncatula | Accumulation of endogenous phenolic compounds. | Phenols were oxidized red/purple pigments and resulted in the accumulation of antioxidant compounds. | [97] |
4.1. Drought and Salinity
4.2. Toxic Metal/Metalloids
4.3. Extreme Temperature
4.4. Atmospheric Pollutants
4.5. Light Stress
4.6. Other Stresses
5. Flavonoids-Mediated Abiotic Stress Signaling
6. Molecular and Genetic Approaches in Tailoring Flavonoids Biosynthesis and Regulation under Abiotic Stress
7. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Genes, Transcript | Method | Plant Species | Stress | Results | Reference |
---|---|---|---|---|---|
GuCPKs | Induced expression of GuCPKs gene | Glycyrrhiza uralensis | NaCl (30 mM) and CaCl2 (2.5 mM) | Improved the accumulation of flavonoids biosynthesis and glycyrrhizic acid. | [175] |
flavanol 3-hydroxylase. | Induced expression of flavanol 3-hydroxylase gene | Rice | Salinity (150 mM) and heat stress (28–30 °C, light 16/8 h) | Improved biosynthesis of quercetin and kaempferol. Increased oxidative damage, which was mitigated with the accumulation of flavonoids content. | [176] |
AtMYB12 | Overexpression of AtMYB12 | Arabidopsis | Drought (25% PEG6000 for 2 weeks) and salinity stress (300 mM once every 2 days for 4 weeks) | Increased the flavonoids agglomeration by the upregulation of genes actively involved in flavonoid biosynthesis | [177] |
VvMyBF1 | VvMyBF1 gene cloned from grapevine induced into Arabidopsis | Arabidopsis | Drought (25% PEG6000 for 2 weeks) and salt stress (200 mM NaCl for 2 weeks) | Increased the accumulation of flavonoids. Higher activities of SOD, POD, pyrroline-5-carboxylate synthase, dihydroflavonol reductase, FLS, CHI, and PAL, as well as a significant reduction of MDA and H2O2 content. | [178] |
GmMyB12 | Overexpression of GmMyB12 | Arabidopsis | Salinity (200 mM NaCl, 2 weeks) and drought stress (25% PEG6000, 2 weeks) | Increased the downstream flavonoids by improving the expression of flavonoid biosynthesis-related genes. Increased the pyrroline-5-carboxylate synthase, SOD, and POD. | [179] |
Basic helix-loop-helix (bHLH) | Transcription factor gene of (bHLH) antirrhinum (AmDEL) induced in Arabidopsis | Arabidopsis | Drought (25% PEG6000 for 2 weeks) and salinity stress (300 mM 2 days for 4 week) | Higher activities of pyrrline-5-carboxylate synthase, dihydroflavonol reductase, chalcone isomerase, and phenylalanine ammonia lyase (PAL) in transgenic plants. Upregulated flavonoids biosynthesis genes. | [180] |
SIbHLH22 | Overexpression of SIbHLH22 | Tomato | Drought (100 mM mannitol) and slat stress (200 mM NaCl) | Transgenic plants showed enhanced vigor by improving ROS scavenging system. Showed small leaves, short height, and higher accumulation of flavonoids. | [181] |
Chalcone isomerase 2 (OsCHI2) | Induction of OsCHI2 | Rice | Heat (40 °C for 3 days), cold stress (2 °C; 16 h light/8 h dark for 12 days), salinity stresses (150 mM NaCl for 7 days), and drought stress (withholding water 7 days at 9 to 10 leave stage). | Abundant structural genes of flavonoid biosynthesis and modulation of flavonoid metabolism. | [118] |
AeCHS o in Arabidopsis plants | AeCHS gene isolated from Abelmosschus esculentus and induced in Arabidopsis. | Arabidopsis | Osmotic (300 mM mannitol for a week) and salt stress (200 mM NaCl for a week) | Increased flavonoid biosynthesis and abiotic stress tolerance. | [182] |
CHS gene by | Overexpression of CHS gene in Arabidopsis | Arabidopsis | High light stress (200 µmol m−2 s−1) | Increased the synthesis of anthocyanins that enhance the adaptability of plants against light stress. | [183] |
EkFLS gene | Overexpressed the EkFLS gene in Arabidopsis; isolated from Euphorbia kansui Liou | Arabidopsis | Drought stress (20% PEG600) and salinity stress (200 mM NaCl) | Increased flavonoids biosynthesis and gave a theoretical base for improving the phytoextracts of medicinal plants and their resistance against multiple stresses simultaneously. | [184] |
GSA1 gene | Overexpression of GSA1 in rice | Rice | Salinity stress (150 mM for 7 days), drought stress (16% PEG8000 for 2 to 3 weeks), and heat stress (42 °C for dozens of hours) | Redirected the metabolic flux from lignin synthesis toward flavonoids synthesis. Accumulated more glycosides and flavonoids. | [185] |
glycosyltransferase gene (UGT76E11) | Overexpression of UGT76E1 | Arabidopsis | H2O2 (0.4 mM), drought (200 mM mannitol), and salinity (100 mM NaCl for 10 days) stress | Showed substantially enhanced tolerance through producing of higher glucosylate quercetin by modulating flavonoid biosynthesis pathway. | [88] |
RtLDOX/RtLDOX2 | Expressed leucoanthocyanidin dioxygenase genes (RtLDOX/RtLDOX2) of Reaumuria trigyna in Arabidopsis | Arabidopsis | Drought (150 mM and 300 mM mannitol for 15 days), salinity (75 mM and 100 mM NaCl for 10 days), and ultraviolet-B-stress (30 min per day for 7 days) | Overexpression of RtLDOX2 showed a higher accumulation of flavonols and anthocyanin and converted dihydrokaempferol to kaempferol, scavenging ROS. | [186] |
UDP-sugar glycosyltransferase gene (CrUGT87A1) | CrUGT87A1 cloned form Carex rigescens in Arabidopsis | Arabidopsis | Salt stress (100 mM and 125 mM NaCl for 7 days) | Higher accumulation of antioxidants and flavonoids. | [61] |
R2R3-MYB (SbMYB2 and SbMYB7) | Overexpression of R2R3-MYB form Scutellaria baicalensis in tobacco | Tobacco | Salt stress (150 mM NaCl), drought (0.2 M mannitol), and ABA (100 µ M) for 3, 6, and 9 days, respectively | Higher fresh weight, lower flavonoid synthesis gene and antioxidants, and higher phenylpropanoid accumulation. | [187] |
PA1-type MYB transcription factor (MdMYBPA1) | MdbHLH33 directly binds to the cis element of the MdMYBPA1 responsive to low temperature | Apple (Malus x domestica) | Low temperature (14 °C) | Responded to flavonoid biosynthesis by synthesizing anthocyanin from proanthocyanin. | [188] |
Ethylene insensitive 2 (EIN2) | Overexpression of EIN2 | Rice | Cd stress (10 µM for 10 days) | Increased flavonoid and phenolics biosynthesis. | [189] |
Core apple autophagy-related gene (MdATG8i) | Overexpression of MdATG8i | Apple | Drought (withholding water for 6 days) | Higher photosynthesis, amino acids, flavonoids, and antioxidant activities, lower ROS and oxidized and insoluble proteins, higher roots hydraulic conductivity, and improved water uptake. | [190] |
AvFLS | Apocynum venetum gene overexpression in AvFLS induced in tobacco | Tobacco | Salinity stress (200 mM for 72 h) | Increased flavonoids synthesis, absorbed more K+, maintained Na+/K+ homeostasis, and increased K+/Na+ ratio. | [191] |
SbMYB8 | Overexpression of R2R3-MYB form Scutellaria baicalensis in tobacco | Tobacco | Salt stress (150 mM NaCl), drought (0.2 M mannitol), and ABA (100 µM) for 3, 6, and 9 days, respectively | Higher flavonoid biosynthesis and antioxidants, and improved tolerance against stress. | [192] |
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Shomali, A.; Das, S.; Arif, N.; Sarraf, M.; Zahra, N.; Yadav, V.; Aliniaeifard, S.; Chauhan, D.K.; Hasanuzzaman, M. Diverse Physiological Roles of Flavonoids in Plant Environmental Stress Responses and Tolerance. Plants 2022, 11, 3158. https://doi.org/10.3390/plants11223158
Shomali A, Das S, Arif N, Sarraf M, Zahra N, Yadav V, Aliniaeifard S, Chauhan DK, Hasanuzzaman M. Diverse Physiological Roles of Flavonoids in Plant Environmental Stress Responses and Tolerance. Plants. 2022; 11(22):3158. https://doi.org/10.3390/plants11223158
Chicago/Turabian StyleShomali, Aida, Susmita Das, Namira Arif, Mohammad Sarraf, Noreen Zahra, Vaishali Yadav, Sasan Aliniaeifard, Devendra Kumar Chauhan, and Mirza Hasanuzzaman. 2022. "Diverse Physiological Roles of Flavonoids in Plant Environmental Stress Responses and Tolerance" Plants 11, no. 22: 3158. https://doi.org/10.3390/plants11223158