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

Response of Zebrina pendula leaves to enhanced UV-B radiation

Dan Wang A * , Yuchu Sun A * , Mei Tu A , Peipei Zhang A , Xiaoqiong Wang A , Taixia Wang A B C and Jingyuan Li https://orcid.org/0000-0002-0832-1701 A B C *
+ Author Affiliations
- Author Affiliations

A College of Life Science, Henan Normal University, Xinxiang, Henan 453007, China.

B Engineering Technology Research Center of Nursing and Utilisation of Genuine Chinese Crude Drugs in Henan Province, Xinxiang, Henan 453007, China.

C Corresponding author. Email: 041034@htu.edu.cn

Functional Plant Biology 48(9) 851-859 https://doi.org/10.1071/FP20274
Submitted: 9 September 2020  Accepted: 10 March 2021   Published: 3 May 2021

Abstract

Plants inevitably receive harmful UV-B radiation when exposed to solar energy, so they have developed a variety of strategies to protect against UV-B radiation damage during long-term evolution. In this study, Zebrina pendula Schnizl. was used to investigate the plant defence against UV-B radiation because of its strong adaptability to sunlight changes, and the colour of its leaves changes significantly under different sunlight intensities. The experiment was carried out to study the changes of Z. pendula leaves under three light conditions: artificial daylight (control check); shading 50%; and artificial daylight + UV-B, aiming to explore the mechanism of defence against UV-B radiation by observing changes in leaf morphological structure, anthocyanin content and distribution. Results showed that the single leaf area increased but leaves became thinner, and the anthocyanin content in the epidermal cells decreased under 50% shading. In contrast, under daylight + UV-B, the single leaf area decreased but thickness increased (mainly due to the increase of the thickness of the upper epidermis and the palisade tissue), the trichomes increased. In addition, the anthocyanin content in the epidermal cells and phenylalanine ammonia-lyase (PAL) activity increased, and the leaf colour became redder, also, the photosynthetic pigment content in mesophyll cells and the biomass per unit volume increased significantly under daylight + UV-B. Thus, when UV-B radiation was enhanced, Z. pendula leaves reduced the exposure to UV-B radiation by reducing the area, and reflect some UV-B radiation by growing trichomes. The UV-B transmittance was effectively reduced by increasing the single leaf thickness and anthocyanin content to block or absorb partial UV-B. Through the above comprehensive defence strategies, Z. pendula effectively avoided the damage of UV-B radiation to mesophyll tissue.

Keywords: UV-B radiation, light conditions, morphological structure, mesophyll, anthocyanin, defence strategy, defense strategy, Zebrina pendula.


References

Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S (2010) Roles of enzymatic and non-enzymatic antioxidants in plants during abiotic stress. Critical Reviews in Biotechnology 30, 161–175.
Roles of enzymatic and non-enzymatic antioxidants in plants during abiotic stress.Crossref | GoogleScholarGoogle Scholar | 20214435PubMed |

Ballaré CL, Caldwell MM, Flint SD, Robinson SA, Bornman JF (2011) Effects of solar ultraviolet radiation on terrestrial ecosystems. Patterns, mechanisms, and interactions with climate change. Photochemical & Photobiological Sciences 10, 226–241.
Effects of solar ultraviolet radiation on terrestrial ecosystems. Patterns, mechanisms, and interactions with climate change.Crossref | GoogleScholarGoogle Scholar |

Barnes PW, Flint SD, Slusser JR, Gao W, Ryel RJ (2008) Diurnal changes in epidermal UV transmittance of plants in naturally high UV environments. Physiologia Plantarum 133, 363–372.
Diurnal changes in epidermal UV transmittance of plants in naturally high UV environments.Crossref | GoogleScholarGoogle Scholar | 18346077PubMed |

Barnes PW, Flint SD, Tobler MA, Ryel RJ (2016) Diurnal adjustment in ultraviolet sunscreen protection is widespread among higher plants. Oecologia 181, 55–63.
Diurnal adjustment in ultraviolet sunscreen protection is widespread among higher plants.Crossref | GoogleScholarGoogle Scholar | 26809621PubMed |

Bernula P, Crocco CD, Arongaus AB, Ulm R, Nagy F, Viczian A (2017) Expression of the UVR8 photoreceptor in different tissues reveals tissue-autonomous features of UV-B signalling. Plant, Cell & Environment 40, 1104–1114.
Expression of the UVR8 photoreceptor in different tissues reveals tissue-autonomous features of UV-B signalling.Crossref | GoogleScholarGoogle Scholar |

Caldwell MM, Ballare CL, Bornman JF, Flint SD, Bjorn LO, Teramura AH, Kulandaivelu G, Tevini M (2003) Terrestrial ecosystems, increased solar ultraviolet radiation and interactions with other climatic change factors. Photochemical & Photobiological Sciences 2, 29–38.
Terrestrial ecosystems, increased solar ultraviolet radiation and interactions with other climatic change factors.Crossref | GoogleScholarGoogle Scholar |

Chen D-Q, Li Z-Y, Pan R-C, Wang X-J (2006) Anthocyanin accumulation mediated by blue light and cytokinin in Arabidopsis seedlings. Journal of Integrative Plant Biology 48, 420–425.
Anthocyanin accumulation mediated by blue light and cytokinin in Arabidopsis seedlings.Crossref | GoogleScholarGoogle Scholar |

Christie JM, Arvai AS, Baxter KJ, Heilmann M, Pratt AJ, O’Hara A, Kelly SM, Hothorn M, Smith BO, Hitomi K, Jenkins GI, Getzoff ED (2012) Plant UVR8 photoreceptor senses UV-B by tryptophan-mediated disruption of cross-dimer salt bridges. Science 335, 1492–1496.
Plant UVR8 photoreceptor senses UV-B by tryptophan-mediated disruption of cross-dimer salt bridges.Crossref | GoogleScholarGoogle Scholar | 22323738PubMed |

Davey MP, Susanti NI, Wargent JJ, Findlay JE, Quick WP, Paul ND, Jenkins GI (2012) The UV-B photoreceptor UVR8 promotes photosynthetic efficiency in Arabidopsis thaliana exposed to elevated levels of UV-B. Photosynthesis Research 114, 121–131.
The UV-B photoreceptor UVR8 promotes photosynthetic efficiency in Arabidopsis thaliana exposed to elevated levels of UV-B.Crossref | GoogleScholarGoogle Scholar | 23161229PubMed |

Dotto M, Casati P (2017) Developmental reprogramming by UV-B radiation in plants. Plant Science 264, 96–101.
Developmental reprogramming by UV-B radiation in plants.Crossref | GoogleScholarGoogle Scholar | 28969807PubMed |

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 |

Fukuda S, Satoh A, Kasahara H, Matsuyama H, Takeuchi Y (2008) Effects of ultraviolet-B irradiation on the cuticular wax of cucumber (Cucumis sativus) cotyledons. Journal of Plant Research 121, 179–189.
Effects of ultraviolet-B irradiation on the cuticular wax of cucumber (Cucumis sativus) cotyledons.Crossref | GoogleScholarGoogle Scholar | 18217194PubMed |

Gao L, Liu Y, Wang X, Li Y, Han R (2019) Lower levels of UV-B light trigger the adaptive responses by inducing plant antioxidant metabolism and flavonoid biosynthesis in Medicago sativa seedlings. Functional Plant Biology 46, 896–906.
Lower levels of UV-B light trigger the adaptive responses by inducing plant antioxidant metabolism and flavonoid biosynthesis in Medicago sativa seedlings.Crossref | GoogleScholarGoogle Scholar | 31196381PubMed |

Ghasemi S, Kumleh HH, Kordrostami M (2019) Changes in the expression of some genes involved in the biosynthesis of secondary metabolites in Cuminum cyminum L. under UV stress. Protoplasma 256, 279–290.
Changes in the expression of some genes involved in the biosynthesis of secondary metabolites in Cuminum cyminum L. under UV stress.Crossref | GoogleScholarGoogle Scholar | 30083789PubMed |

Jacobs JF, Koper GJM, Ursem WNJ (2007) UV protective coatings: A botanical approach. Progress in Organic Coatings 58, 166–171.
UV protective coatings: A botanical approach.Crossref | GoogleScholarGoogle Scholar |

Jan S, Kamili AN, Parray JA, Bedi YS, Ahmad P (2016) Microclimatic variation in UV perception and related disparity in tropane and quinolizidine alkaloid composition of Atropa acuminata, Lupinus polyphyllus and Hyoscyamus niger. Journal of Photochemistry and Photobiology. B, Biology 161, 230–235.
Microclimatic variation in UV perception and related disparity in tropane and quinolizidine alkaloid composition of Atropa acuminata, Lupinus polyphyllus and Hyoscyamus niger.Crossref | GoogleScholarGoogle Scholar | 27285814PubMed |

Jenkins GI (2014) The UV-B photoreceptor UVR8: from structure to physiology. The Plant Cell 26, 21–37.
The UV-B photoreceptor UVR8: from structure to physiology.Crossref | GoogleScholarGoogle Scholar | 24481075PubMed |

Kataria S, Jajoo A, Guruprasad KN (2014) Impact of increasing Ultraviolet-B (UV-B) radiation on photosynthetic processes. Journal of Photochemistry and Photobiology. B, Biology 137, 55–66.
Impact of increasing Ultraviolet-B (UV-B) radiation on photosynthetic processes.Crossref | GoogleScholarGoogle Scholar | 24725638PubMed |

Khudyakova AY, Kreslavski VD, Shirshikova GN, Zharmukhamedov SK, Kosobryukhov AA, Allakhverdiev SI (2017) Resistance of Arabidopsis thaliana L. photosynthetic apparatus to UV-B is reduced by deficit of phytochromes B and A. Journal of Photochemistry and Photobiology. B, Biology 169, 41–46.
Resistance of Arabidopsis thaliana L. photosynthetic apparatus to UV-B is reduced by deficit of phytochromes B and A.Crossref | GoogleScholarGoogle Scholar | 28273503PubMed |

Kohli SK, Khanna K, Bhardwaj R, Abd_Alla EF, Ahmad P, Corpas FJ (2019) Assessment of subcellular ROS and NO metabolism in higher plants: multifunctional signaling molecules. Antioxidants 8, 641
Assessment of subcellular ROS and NO metabolism in higher plants: multifunctional signaling molecules.Crossref | GoogleScholarGoogle Scholar |

Láposi R, Veres S, Lakatos G, Oláh V, Fieldsend A, Mészáros I (2009) Responses of leaf traits of European beech (Fagus sylvatica L.) saplings to supplemental UV-B radiation and UV-B exclusion. Agricultural and Forest Meteorology 149, 745–755.
Responses of leaf traits of European beech (Fagus sylvatica L.) saplings to supplemental UV-B radiation and UV-B exclusion.Crossref | GoogleScholarGoogle Scholar |

Larkum AWD, Karge M, Reifarth F, Eckert HJ, Post A, Renger G (2001) Effect of monochromatic UV-B radiation on electron transfer reactions of Photosystem II. Photosynthesis Research 68, 49–60.
Effect of monochromatic UV-B radiation on electron transfer reactions of Photosystem II.Crossref | GoogleScholarGoogle Scholar |

Lee SB, Suh MC (2015) Advances in the understanding of cuticular waxes in Arabidopsis thaliana and crop species. Plant Cell Reports 34, 557–572.
Advances in the understanding of cuticular waxes in Arabidopsis thaliana and crop species.Crossref | GoogleScholarGoogle Scholar | 25693495PubMed |

Liakopoulos G, Stavrianakou S, Karabourniotis G (2006) Trichome layers versus dehaired lamina of Olea europaea leaves: differences in flavonoid distribution, UV-absorbing capacity, and wax yield. Environmental and Experimental Botany 55, 294–304.
Trichome layers versus dehaired lamina of Olea europaea leaves: differences in flavonoid distribution, UV-absorbing capacity, and wax yield.Crossref | GoogleScholarGoogle Scholar |

Lidon FJC, Reboredo FH, Leitão AE, Silva MMA, Duarte MP, Ramalho JC (2012) Impact of UV-B radiation on photosynthesis. Emirates Journal of Food and Agriculture 24, 546–556.
Impact of UV-B radiation on photosynthesis.Crossref | GoogleScholarGoogle Scholar |

Lister CE, Lancaster JE, Walker JRL (1996) Developmental changes in enzymes of flavonoid biosynthesis in the skins of red and green apple cultivars. Journal of the Science of Food and Agriculture 71, 313–320.
Developmental changes in enzymes of flavonoid biosynthesis in the skins of red and green apple cultivars.Crossref | GoogleScholarGoogle Scholar |

Liu S, Wu C, Fand G, Li T, Ying R, Miao Y (2017) Effects of yeast strain on anthocyanin, color, and antioxidant activity of mulberry wines. Food Biochemistry 41, e12409
Effects of yeast strain on anthocyanin, color, and antioxidant activity of mulberry wines.Crossref | GoogleScholarGoogle Scholar |

Liu L, Gregan S, Winefield C, Jordan B (2018) 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 |

Lo Piccolo E, Landi M, Pellegrini E, Agati G, Giordano C, Giordani T, Lorenzini G, Malorgio F, Massai R, Nali C, Rallo G, Remorini D, Vernieri P, Guidi L (2018) Multiple consequences induced by epidermally-located anthocyanins in young, mature and senescent leaves of Prunus. Frontiers in Plant Science 9, 917
Multiple consequences induced by epidermally-located anthocyanins in young, mature and senescent leaves of Prunus.Crossref | GoogleScholarGoogle Scholar | 30013588PubMed |

Luengo Escobar A, Franklin MDOS, Acevedo P, Nunes-Nesi A, Alberdi M, Reyes-Díaz M (2017) Different levels of UV-B resistance in Vaccinium corymbosum cultivars reveal distinct backgrounds of phenylpropanoid metabolites. Plant Physiology and Biochemistry 118, 541–550.
Different levels of UV-B resistance in Vaccinium corymbosum cultivars reveal distinct backgrounds of phenylpropanoid metabolites.Crossref | GoogleScholarGoogle Scholar | 28779619PubMed |

Rezayian M, Niknam V, Ebrahimzadeh H (2020) Penconazole and calcium ameliorate drought stress in canola by upregulating the antioxidative enzymes. Functional Plant Biology 47, 825–839.
Penconazole and calcium ameliorate drought stress in canola by upregulating the antioxidative enzymes.Crossref | GoogleScholarGoogle Scholar | 32579878PubMed |

Robson TM, Klem K, Urban O, Jansen MA (2015) Re-interpreting plant morphological responses to UV-B radiation. Plant, Cell & Environment 38, 856–866.
Re-interpreting plant morphological responses to UV-B radiation.Crossref | GoogleScholarGoogle Scholar |

Saad KR, Kumar G, Giridhar P, Shetty NP (2018) Differential expression of anthocyanin biosynthesis genes in Daucus carota callus culture in response to ammonium and potassium nitrate ratio in the culture medium. 3 Biotech 8, 431
Differential expression of anthocyanin biosynthesis genes in Daucus carota callus culture in response to ammonium and potassium nitrate ratio in the culture medium.Crossref | GoogleScholarGoogle Scholar | 30306000PubMed |

Schultze M, Bilger W (2019) Acclimation of Arabidopsis thaliana to low temperature protects against damage of photosystem II caused by exposure to UV-B radiation at 9°C. Plant Physiology and Biochemistry 134, 73–80.
Acclimation of Arabidopsis thaliana to low temperature protects against damage of photosystem II caused by exposure to UV-B radiation at 9°C.Crossref | GoogleScholarGoogle Scholar | 30366738PubMed |

Singh S, Agrawal M, Agrawal SB (2013) Differential sensitivity of spinach and amaranthus to enhanced UV-B at varying soil nutrient levels: association with gas exchange, UV-B-absorbing compounds and membrane damage. Photosynthesis Research 115, 123–138.
Differential sensitivity of spinach and amaranthus to enhanced UV-B at varying soil nutrient levels: association with gas exchange, UV-B-absorbing compounds and membrane damage.Crossref | GoogleScholarGoogle Scholar | 23686471PubMed |

Sun M, Gobu FR, Pan D, Li Y, Gao K (2016) Acylphloroglucinol derivatives from Decaspermum gracilentum and their antiradical and cytotoxic activities. Journal of Asian Natural Products Research 18, 13–19.
Acylphloroglucinol derivatives from Decaspermum gracilentum and their antiradical and cytotoxic activities.Crossref | GoogleScholarGoogle Scholar | 26690508PubMed |

Teramura AH, Sullivan JH (1994) Effects of UV-B radiation on photosynthesis and growth of terrestrial plants. Photosynthesis Research 39, 463–473.
Effects of UV-B radiation on photosynthesis and growth of terrestrial plants.Crossref | GoogleScholarGoogle Scholar | 24311137PubMed |

Thomas DT, Puthur JT (2019) Amplification of abiotic stress tolerance potential in rice seedlings with a low dose of UV-B seed priming. Functional Plant Biology 46, 455–466.
Amplification of abiotic stress tolerance potential in rice seedlings with a low dose of UV-B seed priming.Crossref | GoogleScholarGoogle Scholar | 30940331PubMed |

Tossi VE, Regalado JJ, Iannicelli J, Laino LE, Pitta-Lvarez SI (2019) Beyond Arabidopsis: differential UV-B response mediated by UVR8 in diverse species. Frontiers in Plant Science 10, 780
Beyond Arabidopsis: differential UV-B response mediated by UVR8 in diverse species.Crossref | GoogleScholarGoogle Scholar | 31275337PubMed |

Trentin AR, Pivato M, Mehdi SM, Barnabas LE, Giaretta S, Fabrega-Prats M, Prasad D, Arrigoni G, Masi A (2015) Proteome readjustments in the apoplastic space of Arabidopsis thaliana ggt1 mutant leaves exposed to UV-B radiation. Frontiers in Plant Science 6, 128
Proteome readjustments in the apoplastic space of Arabidopsis thaliana ggt1 mutant leaves exposed to UV-B radiation.Crossref | GoogleScholarGoogle Scholar | 25852701PubMed |

Wang L, Jin P, Wang J, Jiang L, Shan T, Zheng Y (2015) Effect of β-aminobutyric acid on cell wall modification and senescence in sweet cherry during storage at 20 °C. Food Chemistry 175, 471–477.
Effect of β-aminobutyric acid on cell wall modification and senescence in sweet cherry during storage at 20 °C.Crossref | GoogleScholarGoogle Scholar | 25577108PubMed |

Wargent JJ, Jordan BR (2013) From ozone depletion to agriculture: understanding the role of UV radiation in sustainable crop production. New Phytologist 197, 1058–1076.
From ozone depletion to agriculture: understanding the role of UV radiation in sustainable crop production.Crossref | GoogleScholarGoogle Scholar |

Wargent JJ, Nelson BCW, McGhie TK, Barnes PW (2015) Acclimation to UV-B radiation and visible light in Lactuca sativa involves up-regulation of photosynthetic performance and orchestration of metabolome-wide responses. Plant, Cell & Environment 38, 929–940.
Acclimation to UV-B radiation and visible light in Lactuca sativa involves up-regulation of photosynthetic performance and orchestration of metabolome-wide responses.Crossref | GoogleScholarGoogle Scholar |

Wu D, Hu Q, Yan Z, Chen W, Yan C, Huang X, Zhang J, Yang P, Deng H, Wang J, Deng X, Shi Y (2012) Structural basis of ultraviolet-B perception by UVR8. Nature 484, 214–219.
Structural basis of ultraviolet-B perception by UVR8.Crossref | GoogleScholarGoogle Scholar | 22388820PubMed |

Xie Y, Zhang W, Duan X, Dai C, Zhang Y, Cui W, Wang R, Shen W (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 | 32480752PubMed |

Yan A, Pan J, An L, Gan Y, Feng H (2012) The responses of trichome mutants to enhanced ultraviolet-B radiation in Arabidopsis thaliana. Journal of Photochemistry and Photobiology. B, Biology 113, 29–35.
The responses of trichome mutants to enhanced ultraviolet-B radiation in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 22647943PubMed |

Zhang TJ, Chow WS, Liu XT, Zhang P, Liu N, Peng CL (2016) A magic red coat on the surface of young leaves: anthocyanins distributed in trichome layer protect Castanopsis fissa leaves from photoinhibition. Tree Physiology 36, 1296–1306.
A magic red coat on the surface of young leaves: anthocyanins distributed in trichome layer protect Castanopsis fissa leaves from photoinhibition.Crossref | GoogleScholarGoogle Scholar | 27614357PubMed |

Živanović B, Vidović M, Milić Komić S, Jovanović L, Kolarž P, Morina F, Veljović Jovanović S (2017) Contents of phenolics and carotenoids in tomato grown underpolytunnels with different UV-transmission rates. Turkish Journal of Agriculture and Forestry 41, 113–120.
Contents of phenolics and carotenoids in tomato grown underpolytunnels with different UV-transmission rates.Crossref | GoogleScholarGoogle Scholar |