Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Lower levels of UV-B light trigger the adaptive responses by inducing plant antioxidant metabolism and flavonoid biosynthesis in Medicago sativa seedlings

Limei Gao https://orcid.org/0000-0002-4806-1449 A B D , Ying Liu B , Xiaofei Wang B , Yongfeng Li B C and Rong Han A B
+ Author Affiliations
- Author Affiliations

A Department of Biotechnology, College of Life Science, Shanxi Normal University, Linfen 041000, China.

B Cell Biology Laboratory, College of Life Science, Shanxi Normal University, Linfen 041000, China.

C Analysis and Testing Center, Shanxi Normal University, Linfen 041000, China.

D Corresponding author. Email: limeigao1122@126.com

Functional Plant Biology 46(10) 896-906 https://doi.org/10.1071/FP19007
Submitted: 16 January 2019  Accepted: 21 May 2019   Published: 14 June 2019

Abstract

Ultraviolet-B (UV-B) light, as an intrinsic part of sunlight, has more significant effects on plant growth and photomorphogenesis than other organisms due to plant’s sessile growth pattern. In our studies, we have observed that alfalfa (Medicago sativa L.) seedlings are very sensitive to UV-B performance. Seedlings have grown better at lower levels of UV-B light (UV-B irradiation dosage <17.35 μW cm–2 day–1), and have higher UV-resistance. However, the higher levels of UV-B light (UV-B irradiation dosage >17.35 μW cm–2 day–1) has caused severe stress injuries to alfalfa seedlings, and seriously inhibited its growth and development. Chlorophyll biosynthesis and chlorophyll fluorescence have been suppressed under all different dosage of UV-B light conditions. Plant antioxidant enzymes were induced by lower levels of UV-B, but greatly inhibited under higher levels of UV-B light. The contents of flavonoid compounds significantly increased under UV-B light compared with controls, and that was more significant under lower levels of UV-B than higher levels of UV-B. Therefore, we have assumed that the significant induction of plant antioxidant capacity and flavonoid excessive accumulation play a central role in alfalfa UV-B tolerance to lower levels of UV-B irradiation.

Additional keywords: flavonoid, plant antioxidant capacity, UV-B tolerance.


References

Brosché M, Strid Å (2003) Molecular events following perception of ultraviolet-B radiation by plants. Physiologia Plantarum 117, 1–10.
Molecular events following perception of ultraviolet-B radiation by plants.Crossref | GoogleScholarGoogle Scholar |

Cembrowska-Lech D, Koprowski M, Kepczyński J (2015) Germination induction of dormant Avena fatua aryopses by KAR1 and GA3 involving the control of reactive oxygen species (H2O2 and O2•–) and enzymatic antioxidants (superoxide dismutase and catalase) both in the embryo and the aleurone layers. Journal of Plant Physiology 176, 169–179.
Germination induction of dormant Avena fatua aryopses by KAR1 and GA3 involving the control of reactive oxygen species (H2O2 and O2•–) and enzymatic antioxidants (superoxide dismutase and catalase) both in the embryo and the aleurone layers.Crossref | GoogleScholarGoogle Scholar | 25618514PubMed |

Cornara L, Xiao J, Burlando B (2016) Therapeutic potential of temperate forage legumes: a review. Critical Reviews in Food Science and Nutrition 56, S149–S161.
Therapeutic potential of temperate forage legumes: a review.Crossref | GoogleScholarGoogle Scholar | 26507574PubMed |

Eichholz I, Rohn S, Gamm A, Beesk N, Herppich WB, Kroh LW, Ulrichs C, Huyskens-Keil S (2012) UV-B-mediated flavonoid synthesis in white asparagus (Asparagus officinalis L.). Food Research International 48, 196–201.
UV-B-mediated flavonoid synthesis in white asparagus (Asparagus officinalis L.).Crossref | GoogleScholarGoogle Scholar |

Fasano R, Gonzalez N, Tosco A, Dal Piaz F, Docimo T, Serrano R, Grillo S, Leone A, Inzé D (2014) Role of Arabidopsis UV resistance locus 8 in plant growth reduction under osmotic stress and low levels of UV-B. Molecular Plant 7, 773–791.
Role of Arabidopsis UV resistance locus 8 in plant growth reduction under osmotic stress and low levels of UV-B.Crossref | GoogleScholarGoogle Scholar | 24413416PubMed |

Frohnmeyer H, Staiger D (2003) Ultraviolet-B radiation-mediated responses in plants. Balancing damage and protection. Plant Physiology 133, 1420–1428.
Ultraviolet-B radiation-mediated responses in plants. Balancing damage and protection.Crossref | GoogleScholarGoogle Scholar | 14681524PubMed |

Gao LM, Li YF, Han R (2015) He-Ne laser preillumination improves the resistance of tall fescue (Festuca arundinacea Schreb.) seedlings to high saline conditions. Protoplasma 252, 1135–1148.
He-Ne laser preillumination improves the resistance of tall fescue (Festuca arundinacea Schreb.) seedlings to high saline conditions.Crossref | GoogleScholarGoogle Scholar | 25547962PubMed |

Gao LM, Li YF, Shen ZH, Han R (2018a) Responses of He-Ne laser on agronomic traits and the crosstalk between UVR8 signaling and phytochrome B signaling pathway in Arabidopsis thaliana subjected to supplementary ultraviolet-B (UV-B) stress. Protoplasma 255, 761–771.
Responses of He-Ne laser on agronomic traits and the crosstalk between UVR8 signaling and phytochrome B signaling pathway in Arabidopsis thaliana subjected to supplementary ultraviolet-B (UV-B) stress.Crossref | GoogleScholarGoogle Scholar |

Gao LM, Wang XF, Shen ZH, Li YF (2018b) The application of exogenous Gibberellic acid enhances wheat seedlings UV-B tolerance by ameliorating DNA damage and manipulating UV-absorbing compound biosynthesis in wheat seedling leaves. Pakistan Journal of Botany 50, 2167–2172.

Hadidi M, Ibarz A, Conde J, Pagan J (2019) Optimisation of steam blanching on enzymatic activity, color and protein degradation of alfalfa (Medicago sativa) to improve some quality characteristics of its edible protein. Food Chemistry 276, 591–598.
Optimisation of steam blanching on enzymatic activity, color and protein degradation of alfalfa (Medicago sativa) to improve some quality characteristics of its edible protein.Crossref | GoogleScholarGoogle Scholar | 30409637PubMed |

Henry-Kirk RA, Plunkett B, Hall M, McGhie T, Allan AC, Wargent JJ, Espley RV (2018) Solar UV light regulates flavonoid metabolism in apple (Malus × domestica). Plant, Cell & Environment 41, 675–688.
Solar UV light regulates flavonoid metabolism in apple (Malus × domestica).Crossref | GoogleScholarGoogle Scholar |

Huang Z, Liu Y, Cui Z, Fang Y, He HH, Liu BR, Wu GL (2018) Soil water storage deficit of alfalfa (Medicago sativa) grasslands along ages in arid area (China). Field Crops Research 221, 1–6.
Soil water storage deficit of alfalfa (Medicago sativa) grasslands along ages in arid area (China).Crossref | GoogleScholarGoogle Scholar |

Jansen MAK, Babu TS, Heller D, Gaba V, Mattoo AK, Edelman M (1996) Ultraviolet-B effects on Spirodela oligorrhiza: induction of different protection mechanisms. Plant Science 115, 217–223.
Ultraviolet-B effects on Spirodela oligorrhiza: induction of different protection mechanisms.Crossref | GoogleScholarGoogle Scholar |

Jenkins GI (2009) Signal transduction in responses to UV-B radiation. Annual Review of Plant Biology 60, 407–431.
Signal transduction in responses to UV-B radiation.Crossref | GoogleScholarGoogle Scholar | 19400728PubMed |

Kalaji HM, Schansker G, Ladle RJ, Goltsev V, Bosa K, Allakhverdiev SI, Brestic M, Bussotti F, Calatayud A, Dąbrowski P, et al (2014) Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. Photosynthesis Research 122, 121–158.
Frequently asked questions about in vivo chlorophyll fluorescence: practical issues.Crossref | GoogleScholarGoogle Scholar | 25119687PubMed |

Kreslavski VD, Los DA, Schmitt FJ, Zharmukhamedov SK, Kuznetsov VV, Allakhverdiev SI (2018a) The impact of the phytochromes on photosynthetic processes. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1859, 400–408.
The impact of the phytochromes on photosynthetic processes.Crossref | GoogleScholarGoogle Scholar |

Kreslavski VD, Shmarev AN, Lyubimov VY, Semenova GA, Zharmukhamedov SK, Shirshikova GN, Khudyakova AY, Allakhverdiev SI (2018b) Response of photosynthetic apparatus in Arabidopsis thaliana L. mutant deficient in phytochrome A and B to UV-B. Photosynthetica 56, 418–426.
Response of photosynthetic apparatus in Arabidopsis thaliana L. mutant deficient in phytochrome A and B to UV-B.Crossref | GoogleScholarGoogle Scholar |

Li F, Jin Z, Qu W, Zhao D, Ma F (2006) Cloning of cDNA encoding the Saussurea medusa chalcone isomerase and its expression in transgenic tobacco. Plant Physiology and Biochemistry 44, 455–461.
Cloning of cDNA encoding the Saussurea medusa chalcone isomerase and its expression in transgenic tobacco.Crossref | GoogleScholarGoogle Scholar | 17010632PubMed |

Li Y, Gao L, Han R (2016) A combination of He-Ne laser irradiation and exogenous NO application efficiently protect wheat seedling from oxidative stress caused by elevated UV-B stress. Environmental Science and Pollution Research International 23, 23675–23682.
A combination of He-Ne laser irradiation and exogenous NO application efficiently protect wheat seedling from oxidative stress caused by elevated UV-B stress.Crossref | GoogleScholarGoogle Scholar | 27619371PubMed |

Liang T, Mei SL, Shi C, Yang Y, Peng Y, Ma LB, Wang F, Li X, Huang X, Yin YH, Liu HT (2018) UVR8 interacts with BES1 and BIM1 to regulate transcription and photomorphogenesis in Arabidopsis. Developmental Cell 44, 512–523.e5.
UVR8 interacts with BES1 and BIM1 to regulate transcription and photomorphogenesis in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 29398622PubMed |

Liu L, Gregan SM, Winefield C, Jordan B (2018a) Comparisons of controlled environment and vineyard experiments in Sauvignon blanc grapes reveal similar UV-B signal transduction pathways for flavonol biosynthesis. Plant Science 276, 44–53.
Comparisons of controlled environment and vineyard experiments in Sauvignon blanc grapes reveal similar UV-B signal transduction pathways for flavonol biosynthesis.Crossref | GoogleScholarGoogle Scholar | 30348327PubMed |

Liu L, Li Y, She G, Zhang X, Jordan B, Chen Q, Zhao J, Wan X (2018b) Metabolite profiling and transcriptomic analyses reveal an essential role of UVR8-mediated signal transduction pathway in regulating flavonoid biosynthesis in tea plants (Camellia sinensis) in response to shading. BMC Plant Biology 18, 233
Metabolite profiling and transcriptomic analyses reveal an essential role of UVR8-mediated signal transduction pathway in regulating flavonoid biosynthesis in tea plants (Camellia sinensis) in response to shading.Crossref | GoogleScholarGoogle Scholar | 30314466PubMed |

Ma M, Wang P, Yang RQ, Gu ZX (2018) Effects of UV-B radiation on the isoflavone accumulation and physiological-biochemical changes of soybean during germination: Physiological-biochemical change of germinated soybean induced by UV-B. Food Chemistry 250, 259–267.
Effects of UV-B radiation on the isoflavone accumulation and physiological-biochemical changes of soybean during germination: Physiological-biochemical change of germinated soybean induced by UV-B.Crossref | GoogleScholarGoogle Scholar | 29412920PubMed |

Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplast. Plant & Cell Physiology 22, 867–880.
Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplast.Crossref | GoogleScholarGoogle Scholar |

Porra RJ, Thompson WA, Kriedmann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Acta Biochimica et Biophysica Sinica 975, 384–394.
Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy.Crossref | GoogleScholarGoogle Scholar |

Rafińska K, Pomastowski P, Wrona O, Górecki R, Buszewski B (2017) Medicago sativa as a source of secondary metabolites for agriculture and pharmaceutical industry. Phytochemistry Letters 20, 520–539.
Medicago sativa as a source of secondary metabolites for agriculture and pharmaceutical industry.Crossref | GoogleScholarGoogle Scholar |

Rao KVM, Sresty TVS (2000) Antioxidant parameters in the seedlings of pigeon pea (Cajanus cajan L. Millspaugh) in response to Zn and Ni stress. Plant Science 157, 113–128.
Antioxidant parameters in the seedlings of pigeon pea (Cajanus cajan L. Millspaugh) in response to Zn and Ni stress.Crossref | GoogleScholarGoogle Scholar |

Reyes TH, Scartazza A, Castagna A, Cosio EG, Ranieri A, Guglielminetti L (2018) Physiological effects of short acute UVB treatments in Chenopodium quinoa Willd. Scientific Reports 8, 371
Physiological effects of short acute UVB treatments in Chenopodium quinoa Willd.Crossref | GoogleScholarGoogle Scholar |

Righini S, Rodriguez EJ, Berosich C, Grotewold E, Casati P, Falcone Ferreyra ML (2019) Apigenin produced by maize flavone synthase I and II protects plants against UV-B-induced damage. Plant, Cell & Environment 42, 495–508.
Apigenin produced by maize flavone synthase I and II protects plants against UV-B-induced damage.Crossref | GoogleScholarGoogle Scholar |

Strasser RJ, Tsimilli-Michael M, Srivastava A (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In ‘Probing photosynthesis: mechanisms, regulation and adaptation’. (Eds M Yunus, U Pather, P Mohanly) pp. 445–483. (Taylor and Francis: London)

Su JC, Zhang YH, Nie Y, Cheng D, Wang R, Hu HL, Chen J, Zhang JF, Du YW, Shen WB (2018) Hydrogen-induced osmotic tolerance is associated with nitric oxide-mediated proline accumulation and reestablishment of redox balance in alfalfa seedlings. Environmental and Experimental Botany 147, 249–260.
Hydrogen-induced osmotic tolerance is associated with nitric oxide-mediated proline accumulation and reestablishment of redox balance in alfalfa seedlings.Crossref | GoogleScholarGoogle Scholar |

Tohidfar M, Zare N, Jouzani GS, Eftekhari SM (2013) Agrobacterium-mediated transformation of alfalfa (Medicago sativa) using a synthetic cry3a gene to enhance resistance against alfalfa weevil. Plant Cell, Tissue and Organ Culture 113, 227–235.
Agrobacterium-mediated transformation of alfalfa (Medicago sativa) using a synthetic cry3a gene to enhance resistance against alfalfa weevil.Crossref | GoogleScholarGoogle Scholar |

Tossi V, Lombardo C, Cassia R, Lamattina L (2012) Nitric oxide and flavonoids are systemically induced by UV-B in maize leaves. Plant Science 193–194, 103–109.
Nitric oxide and flavonoids are systemically induced by UV-B in maize leaves.Crossref | GoogleScholarGoogle Scholar | 22794923PubMed |

Wang Y, Ren HJ, Pan HY, Liu JL, Zhang LY (2015) Enhanced tolerance and remediation to mixed contaminates of PCBs and 2,4-DCP by transgenic alfalfa plants expressing the 2,3-dihydroxybiphenyl-1,2-dioxygenase. Journal of Hazardous Materials 286, 269–275.
Enhanced tolerance and remediation to mixed contaminates of PCBs and 2,4-DCP by transgenic alfalfa plants expressing the 2,3-dihydroxybiphenyl-1,2-dioxygenase.Crossref | GoogleScholarGoogle Scholar | 25590820PubMed |

Wu Q, Su N, Zhang X, Liku Y, Cui J, Liang Y (2016) Hydrogen peroxide, nitric oxide and UV RESISTANCE LOCUS8 interact to mediate UV-B-induced anthocyanin biosynthesis in radish sprouts. Scientific Reports 6, 29164
Hydrogen peroxide, nitric oxide and UV RESISTANCE LOCUS8 interact to mediate UV-B-induced anthocyanin biosynthesis in radish sprouts.Crossref | GoogleScholarGoogle Scholar | 27404993PubMed |

Xie YJ, Zhang W, Duan XL, Dai C, Zhang YH, Cui WT, Wang R, Shen WB (2015) Hydrogen-rich water-alleviated ultraviolet-B-triggered oxidative damage is partially associated with the manipulation of the metabolism of (iso) flavonoids and antioxidant defence in Medicago sativa. Functional Plant Biology 42, 1141–1157.
Hydrogen-rich water-alleviated ultraviolet-B-triggered oxidative damage is partially associated with the manipulation of the metabolism of (iso) flavonoids and antioxidant defence in Medicago sativa.Crossref | GoogleScholarGoogle Scholar |

Yang Y, Liang T, Zhang LB, Shao K, Gu XX, Shang RX, Shi N, Li X, Zhang P, Liu HT (2018) UVR8 interacts with WRKY36 to regulate HY5 transcription and hypocotyl elongation in Arabidopsis. Nature Plants 4, 98–107.
UVR8 interacts with WRKY36 to regulate HY5 transcription and hypocotyl elongation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 29379156PubMed |

Yin R, Ulm R (2017) How plants cope with UV-B: from perception to response. Current Opinion in Plant Biology 37, 42–48.
How plants cope with UV-B: from perception to response.Crossref | GoogleScholarGoogle Scholar | 28411583PubMed |

Zhang JX, Kirham MB (1994) Drought stress-induced changes in activities of superoxide dismutase, catalase and peroxidase in wheat species. Plant & Cell Physiology 35, 785–791.
Drought stress-induced changes in activities of superoxide dismutase, catalase and peroxidase in wheat species.Crossref | GoogleScholarGoogle Scholar |

Zhang C, Shi S (2018) Physiological and proteomic responses of contrasting alfalfa (Medicago sativa L.) varieties to PEG-induced osmotic stress. Frontiers in Plant Science 9, 242
Physiological and proteomic responses of contrasting alfalfa (Medicago sativa L.) varieties to PEG-induced osmotic stress.Crossref | GoogleScholarGoogle Scholar | 29541085PubMed |

Zhang WJ, Wang T (2015) Enhanced salt tolerance of alfalfa (Medicago sativa) by rstB gene transformation. Plant Science 234, 110–118.
Enhanced salt tolerance of alfalfa (Medicago sativa) by rstB gene transformation.Crossref | GoogleScholarGoogle Scholar | 25804814PubMed |

Zhang JY, Duan Z, Zhang DY, Zhang JQ, Di HY, Wu F, Wang YR (2016) Co-transforming bar and CsLEA enhanced tolerance to drought and salt stress in transgenic alfalfa (Medicago sativa L.). Biochemical and Biophysical Research Communications 472, 75–82.
Co-transforming bar and CsLEA enhanced tolerance to drought and salt stress in transgenic alfalfa (Medicago sativa L.).Crossref | GoogleScholarGoogle Scholar |

Zlobin IE, Ivanov YV, Kartashov AV, Sarvin BA, Stavrianidi AN, Kreslavski VD, Kuznetsov VV (2019) Impact of weak water deficit on growth, photosynthetic primary processes and storage processes in pine and spruce seedlings. Photosynthesis Research 139, 307–323.
Impact of weak water deficit on growth, photosynthetic primary processes and storage processes in pine and spruce seedlings.Crossref | GoogleScholarGoogle Scholar | 29779192PubMed |