Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE (Open Access)

Metabolic programming of Rhododendron chrysanthum leaves following exposure to UVB irradiation

Xiaofu Zhou A , Jie Lyu B , Li Sun C , Jiawei Dong A and Hongwei Xu https://orcid.org/0000-0002-1721-7527 A *
+ Author Affiliations
- Author Affiliations

A Faculty of Jilin Provincial Key Laboratory of Plant Spectral Regions Science and Green Production, Jilin Normal University, Siping 136000, China.

B Faculty of Biological Science and Technology, Baotou Teachers’ College, Baotou 014030, China.

C Faculty of Siping Central People’s Hospital, Siping 136000, China.

* Correspondence to: xuhongwei@jlnu.edu.cn

Handling Editor: Suleyman Allakhverdiev

Functional Plant Biology 48(11) 1175-1185 https://doi.org/10.1071/FP20386
Submitted: 9 June 2020  Accepted: 7 August 2021   Published: 4 October 2021

© 2021 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Excessive UVB reaching the earth is a cause for concern. To decipher the mechanism concerning UVB resistance of plants, we studied the effects of UVB radiation on photosynthesis and metabolic profiling of Rhododendron chrysanthum Pall. by applying 2.3 W m−2 of UVB radiation for 2 days. Results showed that maximum quantum yield of PSII (Fv/Fm) and effective quantum yield of PSII (φPSII) decreased by 7.95% and 8.36%, respectively, following UVB exposure. Twenty five known metabolites were identified as most important by two different methods, including univariate and multivariate statistical analyses. Treatment of R. chrysanthum with UVB increased the abundance of flavonoids, organic acids, and amino acids by 62%, 22%, and 5%, respectively. UVB irradiation also induced about 1.18-fold increase in 11 top-ranked metabolites identified: five organic acids (d-2,3-dihydroxypropanoic acid, maleic acid, glyceric acid, fumaric acid and suberic acid), four amino acids (l-norleucine, 3-oxoalanine, l-serine and glycine), and two fatty acids (pelargonic acid and myristoleic acid). In addition, UVB irradiation increased the intermediate products of arginine biosynthesis and the TCA cycle. Taken together, the accumulation of flavonoids, organic acids, amino acids and fatty acids, accompanied by enhancement of TCA cycle and arginine biosynthesis, may protect R. chrysanthum plants against UVB deleterious effects.

Keywords: amino acids, arginine biosynthesis, chlorophyll fluorescence, fatty acids, flavonoids, metabolic profile, organic acids, photosynthesis, Rhododendron chrysanthum, TCA cycle, UVB irradiation.


References

Abdelrahman M, Burritt DJ, Tran L-SP (2018) The use of metabolomic quantitative trait locus mapping and osmotic adjustment traits for the improvement of crop yields under environmental stresses. Seminars in Cell & Developmental Biology 83, 86–94.
The use of metabolomic quantitative trait locus mapping and osmotic adjustment traits for the improvement of crop yields under environmental stresses.Crossref | GoogleScholarGoogle Scholar |

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

Ahmad P, Tripathi DK, Deshmukh R, Singh VP, Corpas FJ (2019) Revisiting the role of ROS and RNS in plants under changing environment. Environmental and Experimental Botany 161, 1–3.
Revisiting the role of ROS and RNS in plants under changing environment.Crossref | GoogleScholarGoogle Scholar |

Berli FJ, Moreno D, Piccoli P, Hespanhol-Viana L, Silva MF, Bressan-Smith R, Cavagnaro JB, Bottini R (2010) Abscisic acid is involved in the response of grape (Vitis vinifera L.) cv. Malbec leaf tissues to ultraviolet-B radiation by enhancing ultraviolet-absorbing compounds, antioxidant enzymes and membrane sterols. Plant, Cell & Environment 33, 1–10.
Abscisic acid is involved in the response of grape (Vitis vinifera L.) cv. Malbec leaf tissues to ultraviolet-B radiation by enhancing ultraviolet-absorbing compounds, antioxidant enzymes and membrane sterols.Crossref | GoogleScholarGoogle Scholar |

Blasco H, Błaszczyński J, Billaut JC, Nadal-Desbarats L, Pradat PF, Devos D, Moreau C, Andres CR, Emond P, Corcia P, Słowiński R (2015) Comparative analysis of targeted metabolomics: dominance-based rough set approach versus orthogonal partial least square-discriminant analysis. Journal of Biomedical Informatics 53, 291–299.
Comparative analysis of targeted metabolomics: dominance-based rough set approach versus orthogonal partial least square-discriminant analysis.Crossref | GoogleScholarGoogle Scholar | 25499899PubMed |

Casati P, Campi M, Morrow DJ, Fernandes JF, Walbot V (2011) Transcriptomic, proteomic and metabolomic analysis of UV-B signaling in maize. BMC Genomics 12, 321
Transcriptomic, proteomic and metabolomic analysis of UV-B signaling in maize.Crossref | GoogleScholarGoogle Scholar | 21679461PubMed |

Demkura PV, Ballaré CL (2012) UVR8 mediates UV-B-induced Arabidopsis defense responses against Botrytis cinerea by controlling sinapate accumulation. Molecular Plant 5, 642–652.
UVR8 mediates UV-B-induced Arabidopsis defense responses against Botrytis cinerea by controlling sinapate accumulation.Crossref | GoogleScholarGoogle Scholar | 22447155PubMed |

Dias MC, Pinto DCGA, Correia C, Moutinho-Pereira J, Oliveira H, Freitas H, Silva AMS, Santos C (2018) UV-B radiation modulates physiology and lipophilic metabolite profile in Olea europaea. Journal of Plant Physiology 222, 39–50.
UV-B radiation modulates physiology and lipophilic metabolite profile in Olea europaea.Crossref | GoogleScholarGoogle Scholar |

Dias MC, Santos C, Silva S, Pinto DCGA, Silva AM (2020) Physiological and metabolite reconfiguration of Olea europaea to cope and recover from a heat or high UV-B shock. Journal of Agricultural and Food Chemistry 68, 11339–11349.
Physiological and metabolite reconfiguration of Olea europaea to cope and recover from a heat or high UV-B shock.Crossref | GoogleScholarGoogle Scholar | 32955863PubMed |

Emiliani J, Grotewold E, Falcone F, María L, Casati P (2013) Flavonols protect Arabidopsis plants against UV-B deleterious effects. Molecular Plant 6, 1376–1379.
Flavonols protect Arabidopsis plants against UV-B deleterious effects.Crossref | GoogleScholarGoogle Scholar | 23371934PubMed |

Farooq M, Basra SMA, Wahid A, Ahmad N, Saleem BA (2009a) Improving the drought tolerance in rice (Oryza sativa L.) by exogenous application of salicylic acid. Journal of Agronomy and Crop Science 195, 237–246.
Improving the drought tolerance in rice (Oryza sativa L.) by exogenous application of salicylic acid.Crossref | GoogleScholarGoogle Scholar |

Farooq M, Wahid A, Ito O, Lee D-J, Siddique KHM (2009b) Advances in drought resistance of rice. Critical Reviews in Plant Sciences 28, 199–217.
Advances in drought resistance of rice.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 |

Guyon I, Elisseeff A (2003) An introduction to variable and feature selection. Journal of Machine Learning Research 3, 1157–1182.
An introduction to variable and feature selection.Crossref | GoogleScholarGoogle Scholar |

Hamid A, Singh S, Agrawal M, Agrawal SB (2018) Heteropogon contortus BL-1 (Pilli Grass) and elevated UV-B radiation: the role of growth, physiological and biochemical traits in determining forage productivity and quality. Photochemistry and Photobiology 95, 572–580.
Heteropogon contortus BL-1 (Pilli Grass) and elevated UV-B radiation: the role of growth, physiological and biochemical traits in determining forage productivity and quality.Crossref | GoogleScholarGoogle Scholar | 30066951PubMed |

Hamid A, Singh S, Agrawal M, Agrawal SB (2020) Effects of plant age on performance of the tropical perennial fodder grass, Cenchrus ciliaris L. subjected to elevated ultraviolet-B radiation. Plant Biology 22, 805–812.
Effects of plant age on performance of the tropical perennial fodder grass, Cenchrus ciliaris L. subjected to elevated ultraviolet-B radiation.Crossref | GoogleScholarGoogle Scholar | 32219978PubMed |

Hong J, Yang L, Zhang D, Shi J (2016) Plant metabolomics: an indispensable system biology tool for plant science. International Journal of Molecular Sciences 17, 767
Plant metabolomics: an indispensable system biology tool for plant science.Crossref | GoogleScholarGoogle Scholar |

Hugly S, Kunst L, Browse J, Somerville C (1989) Enhanced thermal tolerance of photosynthesis and altered chloroplast ultrastructure in a mutant Arabidopsis deficient in lipid peroxidation. Plant Physiology 90, 1134–1142.
Enhanced thermal tolerance of photosynthesis and altered chloroplast ultrastructure in a mutant Arabidopsis deficient in lipid peroxidation.Crossref | GoogleScholarGoogle Scholar | 16666863PubMed |

Jan S, Alyemeni MN, Wijaya L, Alam P, Siddique KH, Ahmad P (2018) Interactive effect of 24-epibrassinolide and silicon alleviates cadmium stress via the modulation of antioxidant defense and glyoxalase systems and macronutrient content in Pisum sativum L. seedlings. BMC Plant Biology 18, 146
Interactive effect of 24-epibrassinolide and silicon alleviates cadmium stress via the modulation of antioxidant defense and glyoxalase systems and macronutrient content in Pisum sativum L. seedlings.Crossref | GoogleScholarGoogle Scholar | 30012086PubMed |

Kasote DM, Katyare SS, Hegde MV, Bae H (2015) Significance of antioxidant potential of plants and its relevance to therapeutic applications. International Journal of Biological Sciences 11, 982–991.
Significance of antioxidant potential of plants and its relevance to therapeutic applications.Crossref | GoogleScholarGoogle Scholar | 26157352PubMed |

Kaya C, Okant M, Ugurlar F, Alyemeni MN, Ashraf M, Ahmad P (2019) Melatonin-mediated nitric oxide improves tolerance to cadmium toxicity by reducing oxidative stress in wheat plants. Chemosphere 225, 627–638.
Melatonin-mediated nitric oxide improves tolerance to cadmium toxicity by reducing oxidative stress in wheat plants.Crossref | GoogleScholarGoogle Scholar | 30901656PubMed |

Kim S, Yun EJ, Hossain MA, Lee H, Kim KH (2012) Global profiling of ultraviolet-induced metabolic disruption in Melissa officinalis by using gas chromatography-mass spectrometry. Analytical and Bioanalytical Chemistry 404, 553–562.
Global profiling of ultraviolet-induced metabolic disruption in Melissa officinalis by using gas chromatography-mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 22729379PubMed |

Kim S, Lee H, Kim KH (2018) Metabolomic elucidation of recovery of Melissa officinalis from UV-B irradiation stress. Industrial Crops and Products 121, 428–433.
Metabolomic elucidation of recovery of Melissa officinalis from UV-B irradiation stress.Crossref | GoogleScholarGoogle Scholar |

Knox PP, Lukashev EP, Gorokhov VV, Grishanova NP, Paschenko VZ (2019) Hybrid complexes of photosynthetic reaction centers and quantum dots in various matrices: resistance to UV irradiation and heating. Photosynthesis Research 139, 295–305.
Hybrid complexes of photosynthetic reaction centers and quantum dots in various matrices: resistance to UV irradiation and heating.Crossref | GoogleScholarGoogle Scholar | 29948749PubMed |

Kohli SK, Khanna K, Bhardwaj R, Abd_Allah 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 |

Kramer GF, Norman HA, Krizek DT, Mirecki RM (1991) Influence of UV-B radiation on polyamines, lipid peroxidation and membrane lipids in cucumber. Phytochemistry 30, 2101–2108.
Influence of UV-B radiation on polyamines, lipid peroxidation and membrane lipids in cucumber.Crossref | GoogleScholarGoogle Scholar |

Kreslavski VD, Shmarev AN, Lyubimov VY, Semenova GA, Zharmukhamedov SK, Shirshikova GN, Khudyakova AY, Allakhverdiev SI (2018) 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 |

Kusano M, Tohge T, Fukushima A, Kobayashi M, Hayashi N, Otsuki H, Kawashima M, Matsuda F, Niida R (2011) Metabolomics reveals comprehensive reprogramming involving two independent metabolic responses of Arabidopsis to UV-B light. The Plant Journal 67, 354–369.
Metabolomics reveals comprehensive reprogramming involving two independent metabolic responses of Arabidopsis to UV-B light.Crossref | GoogleScholarGoogle Scholar | 21466600PubMed |

Lyu J, Wang C, Liang DY, Liu L, Pandey LK, Xu HW, Zhou XF (2019) Sensitivity of wild and domesticated Rhododendron chrysanthum to different light regime (UVA, UVB, and PAR). Photosynthetica 57, 841–849.
Sensitivity of wild and domesticated Rhododendron chrysanthum to different light regime (UVA, UVB, and PAR).Crossref | GoogleScholarGoogle Scholar |

Machado F, Dias MC, de Pinho PG, Araújo AM, Pinto D, Silva A, Correia C, Moutinho-Pereira J, Santos C (2017) Photosynthetic performance and volatile organic compounds profile in Eucalyptus globulus after UVB radiation. Environmental and Experimental Botany 140, 141–149.
Photosynthetic performance and volatile organic compounds profile in Eucalyptus globulus after UVB radiation.Crossref | GoogleScholarGoogle Scholar |

Moorthy K, Kathiresan P (1998) UV-B induced alterations in composition of thylakoid membrane and amino acids in leaves of Rhizophora apiculata Blume. Photosynthetica 35, 321–328.
UV-B induced alterations in composition of thylakoid membrane and amino acids in leaves of Rhizophora apiculata Blume.Crossref | GoogleScholarGoogle Scholar |

Obata T, Fernie AR (2012) The use of metabolomics to dissect plant responses to abiotic stresses. Cellular and Molecular Life Sciences 69, 3225–3243.
The use of metabolomics to dissect plant responses to abiotic stresses.Crossref | GoogleScholarGoogle Scholar | 22885821PubMed |

Parida AK, Panda A, Rangani J (2018) Metabolomics-guided elucidation of abiotic stress tolerance mechanisms in plants. In ‘Plant metabolites and regulation under environmental stress’. (Eds P Ahmad, MA Ahanger, VP Singh, DK Tripathi, P Alam, MN Alyemeni) pp. 89–131. (Academic Press: London, UK) 10.1016/B978-0-12-812689-9.00005-4

Peng M, Shahzad R, Gul A, Subthain H, Shen S, Lei L, Zheng Z, Zhou J, Lu D, Wang S, Nishawy E, Liu X, Tohge T, Fernie AR, Luo J (2017) Differentially evolved glucosyltransferases determine natural variation of rice flavone accumulation and UV-tolerance. Nature Communications 8, 1975
Differentially evolved glucosyltransferases determine natural variation of rice flavone accumulation and UV-tolerance.Crossref | GoogleScholarGoogle Scholar | 29213047PubMed |

Pfündel EE (2003) Action of UV and visible radiation on chlorophyll fluorescence from dark-adapted grape leaves (Vitis vinifera L.). Photosynthesis Research 75, 29–39.
Action of UV and visible radiation on chlorophyll fluorescence from dark-adapted grape leaves (Vitis vinifera L.).Crossref | GoogleScholarGoogle Scholar | 16245091PubMed |

Popescu R, Kopp B (2013) The genus Rhododendron: an ethnopharmacological and toxicological review. Journal of Ethnopharmacology 147, 42–62.
The genus Rhododendron: an ethnopharmacological and toxicological review.Crossref | GoogleScholarGoogle Scholar | 23454683PubMed |

Qiu Y, Cai G, Zhou B, Li D, Zhao A, Xie G, Li H, Cai S, Xie D, Huang C, Ge W, Zhou Z, Xu LX, Jia W, Zheng S, Yen Y, Jia W (2014) A distinct metabolic signature of human colorectal cancer with prognostic potential. Clinical Cancer Research 20, 2136–2146.
A distinct metabolic signature of human colorectal cancer with prognostic potential.Crossref | GoogleScholarGoogle Scholar | 24526730PubMed |

Rama PG, Vinutha T (2019) Metabolomic profiling of plants to understand reasons for plant stress resilience to abiotic stress. In ‘Recent approaches in omics for plant resilience to climate change’. (Ed. S Wani) pp. 57–74. (Springer: Cham, Switzerland) 10.1007/978-3-030-21687-0_3

Rostami-Hodjegan A, Nurminen S, Jackson PR, Tucker GT (1996) Caffeine urinary metabolite ratios as markers of enzyme activity: a theoretical assessment. Pharmacogenetics 6, 121–149.
Caffeine urinary metabolite ratios as markers of enzyme activity: a theoretical assessment.Crossref | GoogleScholarGoogle Scholar | 9156692PubMed |

Rostami-Hodjegan A, Kroemer HK, Tucker GT (1999) In-vivo indices of enzyme activity: the effect of renal impairment on the assessment of CYP2D6 activity. Pharmacogenetics 9, 277–286.
In-vivo indices of enzyme activity: the effect of renal impairment on the assessment of CYP2D6 activity.Crossref | GoogleScholarGoogle Scholar | 10471059PubMed |

Takshak S, Agrawal SB (2019) Defense potential of secondary metabolites in medicinal plants under UV-B stress. Journal of Photochemistry and Photobiology B: Biology 193, 51–88.
Defense potential of secondary metabolites in medicinal plants under UV-B stress.Crossref | GoogleScholarGoogle Scholar |

Tang H, Zhang X, Gong B, Yan Y, Shi Q (2020) Proteomics and metabolomics analysis of tomato fruit at different maturity stages and under salt treatment. Food Chemistry 311, 126009
Proteomics and metabolomics analysis of tomato fruit at different maturity stages and under salt treatment.Crossref | GoogleScholarGoogle Scholar | 31887558PubMed |

Xie Z, Wang J, Wang W, Wang Y, Xu J, Li Z, Zhao X, Fu B (2021) Integrated analysis of the transcriptome and metabolome revealed the molecular mechanisms underlying the enhanced salt tolerance of rice due to the application of exogenous melatonin. Frontiers in Plant Science 11, 618680
Integrated analysis of the transcriptome and metabolome revealed the molecular mechanisms underlying the enhanced salt tolerance of rice due to the application of exogenous melatonin.Crossref | GoogleScholarGoogle Scholar | 33519878PubMed |

Yadav A, Lingwan M, Yadukrishnan P, Masakapalli SK, Datta S (2019) BBX31 promotes hypocotyl growth, primary root elongation and UV-B tolerance in Arabidopsis. Plant Signaling & Behavior 14, e1588672
BBX31 promotes hypocotyl growth, primary root elongation and UV-B tolerance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Zhou X, Chen S, Wu H, Yang Y, Xu H (2017) Biochemical and proteomics analyses of antioxidant enzymes reveal the potential stress tolerance in Rhododendron chrysanthum Pall. Biology Direct 12, 10
Biochemical and proteomics analyses of antioxidant enzymes reveal the potential stress tolerance in Rhododendron chrysanthum Pall.Crossref | GoogleScholarGoogle Scholar | 28476175PubMed |