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Differential physiological responses and tolerance to potentially toxic elements in Primula forbesii Franch

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Abstract

Environmental pollution caused by potentially toxic elements (PTEs) has become a global problem that endangers environmental sustainability due to industrial, agricultural, and urban pollution. Primula forbesii Franch. (a synonym of Primula filipes G. Watt.) is a biennial flower native to China with excellent stress resistance and ornamental value. In this study, we examined the phenotypic traits, growth indexes, and physiological properties of P. forbesii in response to five representative PTEs (Cd, Ni, Cr(III), Cu, and Zn) under hydroponic culture conditions. High concentrations of Zn and Cr had little effect on the growth and physiological properties of P. forbesii, indicating that the species has strong tolerance to Zn and Cr stress. Alternatively, high concentrations of Cd, Ni, and Cu seriously affected plant growth and development, resulting in leaf chlorosis and even death, and therefore may have a serious negative impact on the growth of P. forbesii. However, activity levels of some antioxidant enzymes and osmotic regulatory substances remained high, indicating that P. forbesii resisted PTE stress by regulating physiological and biochemical metabolism to a certain extent. Furthermore, principal component analysis and membership function were used to comprehensively evaluate P. forbesii resistance to PTEs. These analyses revealed that P. forbesii exhibits distinct sensitivities and physiological responses to different PTEs and suggested that the resistance to five PTEs in decreasing order is Zn > Cr > Cd > Cu > Ni. These results provide a theoretical basis for the future application of P. forbesii in environments with PTE pollution and may expand its practical utilization.

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References

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105(105):121–126

    Article  CAS  Google Scholar 

  • Ahmad P (2012) Salt-induced changes in photosynthetic activity and oxidative defense system of three cultivars of mustard (Brassica juncea L.). Afr J Biotechnol 11(11):2694–2703

    CAS  Google Scholar 

  • Ali MA, Asghar HN, Khan MY, Saleem M, Naveed M, Niazi NK (2015) Alleviation of nickel-induced stress in mungbean through application of gibberellic acid. Int J Agric Biol 17(05):990–994

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254

    Article  CAS  Google Scholar 

  • Feng J, Lin Y, Yang Y, Shen Q, Huang J, Wang S, Zhu X, Li Z (2018) Tolerance and bioaccumulation of Cd and Cu in Sesuvium portulacastrum. Ecotoxicol Environ Saf 147:306–312. https://doi.org/10.1016/j.ecoenv.2017.08.056

    Article  CAS  Google Scholar 

  • Ghori NH, Ghori T, Hayat MQ, Imadiet SR, Gul A, Altay V, Ozturk M (2019) Heavy metal stress and responses in plants. Int J Environ Sci Technol 16(3):1807–1828

    Article  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) ROS and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48(12):909–930

    Article  CAS  Google Scholar 

  • Gill PK, Sharma AD, Singh P, Bhullaret SS (2001) Effect of various abiotic stresses on the growth, soluble sugars and water relations of sorghum seedlings grown in light and darkness. Bulg J Plant Physiol 27:72–84

    CAS  Google Scholar 

  • Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53(366):1–11

    Article  CAS  Google Scholar 

  • He SY, Yang X, He ZL, Baligar VC (2017) Morphological and physiological responses of plants to cadmium toxicity: a review. Pedosphere 27(3):421–438

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125(1):189–198

    Article  CAS  Google Scholar 

  • Hess JL, Foster JG (1976) Superoxide-dismutase in higher-plants. Fed Proc 7:1553

    Google Scholar 

  • Hojati M, Modarres-Sanavy SAM, Enferadi ST, Majdi M, Ghanati F, Farzadfar S, Pazoki A (2017) Cadmium and copper induced changes in growth, oxidative metabolism and terpenoids of Tanacetum parthenium. Environ Sci Pollut Res 24(13):12261–12272

    Article  CAS  Google Scholar 

  • Hou WH, Chen X, Song GL, Wang QH, Chang CC (2007) Effects of copper and cadmium on heavy metal polluted waterbody restoration by duckweed (Lemna minor). Plant Physiol Biochem 45(1):62–69

    Article  CAS  Google Scholar 

  • Hu CM (1990) Primulaceae. In: Chen FH, Hu CM (eds) Flora Reipublicae Popularis Sinicae. Science Press, Beijing, pp 1–321

    Google Scholar 

  • Huang MY, Ai HL, Xu XX, Chen K, Niu H, Zhu HH, Sun J, Du DY, Chen L (2018) Nitric oxide alleviates toxicity of hexavalent chromium on tall fescue and improves performance of photosystem II. Ecotoxicol Environ Saf 164:32–40

    Article  CAS  Google Scholar 

  • Hussain MK, Aziz A, Ditta HMA, Azhar MF, El-Shehawi AM, Hussain S, Mehboob N, Hussain M, Farooq S (2021) Foliar application of seed water extract of Nigella sativa improved maize growth in cadmium-contaminated soil. PLoS One 16(7):e0254602. https://doi.org/10.1371/journal.pone.0254602

    Article  CAS  Google Scholar 

  • Jia Y, Zhao JL, Pan YZ, Xu Y, Sun LX, Liu QL (2014) Collection and evaluation of Primula species of western Sichuan in China. Genet Resour Crop Evol 61:1245–1262

    Article  Google Scholar 

  • Jia Y, Liu CL, Lan XY, Zhao J, Xiang YF, Pan YZ (2020) Effect of cadium stress on the growth and physiological characteristics of Primula forbesii seedlings. Acta Bot Boreal-Occident Sin 40(3):0454–0462

    Google Scholar 

  • Jia Y, Xiang YF, Wang LL, Zhao J, Liu CL, Pan YZ (2020b) Effects of salt stress on the growth and physiological characteristics of Primula forbesii. Acta Pratacul Sin 29(10):119–128

    Google Scholar 

  • Jin Y, Zhang B, Chen J, Mao W, Lou L, Shen C, Lin Q (2021) Biofertilizer-induced response to cadmium accumulation in Oryza sativa L. grains involving exogenous organic matter and soil bacterial community structure. Ecotoxicol Environ Saf 211:111952. https://doi.org/10.1016/j.ecoenv.2021.111952

    Article  CAS  Google Scholar 

  • Jozefczak M, Keunen E, Schat H, Bliek M, Hernandez LE, Carleer R, Remans T, Bohler S, Vangronsveld J, Cuypers A (2014) Differential response of Arabidopsis leaves and roots to cadmium: Glutathione-related chelating capacity vs antioxidant capacity. Plant Physiol Biochem 83:1–9

    Article  CAS  Google Scholar 

  • Khair KU, Farid M, Ashraf U, Zubair M, Ali S (2020) Citric acid enhanced phytoextraction of nickel (Ni) and alleviate Mentha piperita (L.) from Ni-induced physiological and biochemical damages. Environ Sci Pollut Res 27(21):27010–27022

    Article  CAS  Google Scholar 

  • Khan AHA, Kiyani A, Mirza CR, Butt TA, Barros R, Ali B, Iqbal M, Yousaf S (2021) Ornamental plants for the phytoremediation of heavy metals: Present knowledge and future perspectives. Environ Res. 195:110780. https://doi.org/10.1016/j.envres.2021.110780

    Article  CAS  Google Scholar 

  • Kopittke PM, Blamey FPC, Asher CJ, Menzies NW (2010) Trace metal phytotoxicity in solution culture: A review. J Exp Bot 61:945–954

    Article  CAS  Google Scholar 

  • Lagriffoul A, Mocquot B, Mench M, Vangronsveld J (1998) Cadmium toxicity effects on growth, mineral and chlorophyll contents, and activities of stress related enzymes in young maize plants (Zea mays L.). Plant Soil 200(2):241–250

    Article  CAS  Google Scholar 

  • Law MY, Charles SA, Halliwell B (1983) Glutathione and ascorbic acid in spinach Spinacia oleracea chloroplasts The effect of hydrogen peroxide and of paraquat. Biochem J 210(3):899–903

    Article  CAS  Google Scholar 

  • Li HS (2002) Experimental principle and techniques of plant physiology and biochemistry. Higher Education Press, Beijing, pp 194–197, 258–260

    Google Scholar 

  • Li M, Wang GX, Lin JS (2003) Application of external calcium in improving the PEG-induced water stress tolerance in liquorice cells. Bot Bullet Acad Sin 44(4):275–284

    CAS  Google Scholar 

  • Li X, Yang Y, Jia L, Chen H, Wei X (2013) Zinc-induced oxidative damage, antioxidant enzyme response and proline metabolism in roots and leaves of wheat plants. Ecotoxicol Environ Saf 89:150–157. https://doi.org/10.1016/j.ecoenv.2012.11.025

    Article  CAS  Google Scholar 

  • Li JT, Gurajala HK, Wu LH, van der Ent A, Qiu RL, Baker AJM, Tang YT, Yang XE, Shu WS (2018) Hyperaccumulator plants from China: A synthesis of the current state of knowledge. Environ Sci Technol 52(21):11980–11994. https://doi.org/10.1021/acs.est.8b01060

    Article  CAS  Google Scholar 

  • Lin HY, Sun T, Zhou Y, Zhang XM (2016) Anti-oxidative feedback and biomarkers in the intertidal seagrass Zostera japonica induced by exposure to copper, lead and cadmium. Mar Pollut Bull 109(1):325–333

    Article  CAS  Google Scholar 

  • Liu J, Yu G, Jiang P, Zhang X, Oiu R (2020) Interaction of Mn and Cd during their uptake in Celosia argentea differs between hydroponic and soil systems. Plant Soil 450(1–2):323–336

    Article  CAS  Google Scholar 

  • Madhava Rao KV, Sresty TVS (2000) Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Sci 157(1):113–128

    Article  CAS  Google Scholar 

  • Matés JM (2000) Effects of antioxidant enzymes in the molecular control of ROS toxicology. Toxicology 153(1):83–104

    Article  Google Scholar 

  • Matraszek R, Hawrylak-Nowak B, Chwil S, Chwil M (2016a) Macronutrient composition of nickel-treated wheat under different sulfur concentrations in the nutrient solution. Environ Sci Pollut Res 23(6):5902–5914

    Article  CAS  Google Scholar 

  • Matraszek R, Hawrylak-Nowak B, Chwil S, Chwil M (2016b) Interaction between cadmium stress and sulphur nutrition level on macronutrient status of Sinapis alba L. Water Air Soil Pollut 227(9):355

    Article  Google Scholar 

  • Nieboer E, Richardson DHS (1980) The replacement of the nondescript term “Heavy metals” by a biologically and chemically significant classification of metal ions. Environ Pollut Ser B 1(1):3–26

    Article  CAS  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: Keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49(1):249

    Article  CAS  Google Scholar 

  • Phusantisampan T, Meeinkuirt W, Saengwilai P, Pichtel J, Chaiyarat R (2016) Phytostabilization potential of two ecotypes of Vetiveria zizanioides in cadmium-contaminated soils: greenhouse and field experiments. Environ Sci Pollut Res Int 23(19):20027–38. https://doi.org/10.1007/s11356-016-7229-5

    Article  CAS  Google Scholar 

  • Radoti K, Dui T, Mutavdi D (2000) Changes in peroxidase activity and isoenzymes in spruce needles after exposure to different concentrations of cadmium. Environ Exp Bot 44(2):105–113

    Article  Google Scholar 

  • Reckova S, Tuma J, Dobrev P, Vankova R (2019) Influence of copper on hormone content and selected morphological, physiological and biochemical parameters of hydroponically grown Zea mays plants. Plant Growth Regul 89:11. https://doi.org/10.1007/s10725-019-00527-w

  • Richards AJ (2003) Primula, 2nd edn. Timber Press, Oregon

    Google Scholar 

  • Rouached H (2011) Multilevel coordination of phosphate and sulfate homeostasis in plants. Plant Signal Behav 6(7):952–955

    Article  CAS  Google Scholar 

  • Rouached H, Secco D, Arpat BA (2010) Regulation of ion homeostasis in plants: Current approaches and future challenges. Plant Signal Behav 5(5):501–502

    Article  Google Scholar 

  • Sarwar N, Imran M, Shaheen MR, Ishaque W, Kamran MA, Matloob A, Rehim A, Hussain S (2017) Phytoremediation strategies for soils contaminated with heavy metals: Modifications and future perspectives. Chemosphere 171:710–721. https://doi.org/10.1016/j.chemosphere.2016.12.116

    Article  CAS  Google Scholar 

  • Shah K, Kumar RG, Verma S, Dubey RS (2001) Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Sci 161:1135–1141. https://doi.org/10.1016/S01689452(01)00517-9

    Article  CAS  Google Scholar 

  • Shanker AK, Cervantes C, Loza-Tavera H, Avudainayagam S (2005) Chromium toxicity in plants. Environ Int 31(5):739–753. https://doi.org/10.1016/j.envint.2005.02.003

    Article  CAS  Google Scholar 

  • Sidhu GPS, Singh HP, Batish DR, Kohli RK (2017) Tolerance and hyperaccumulation of cadmium by a wild, unpalatable herb Coronopus didymus (L.) Sm. (Brassicaceae). Ecotoxicol Environ Saf 135:209–215

    Article  CAS  Google Scholar 

  • Singh PK, Tewari RK (2003) Cadmium toxicity induced changes in plant water relations and oxidative metabolism of Brassica juncea L. plants. J Environ Biol 24(1):107–112

    CAS  Google Scholar 

  • Singh H, Kumar D, Soni V (2020) Copper and mercury induced oxidative stresses and antioxidant responses of Spirodela polyrhiza (L) Schleid. Biochem Biophys Rep 23:100781

    Google Scholar 

  • Sricoth T, Meeinkuirt W, Saengwilai P, Pichtel J, Taeprayoon P (2018) Aquatic plants for phytostabilization of cadmium and zinc in hydroponic experiments. Environ Sci Pollut Res Int 25(15):14964–14976. https://doi.org/10.1007/s11356-018-1714-y

    Article  CAS  Google Scholar 

  • Srivastava S, Mishra S, Tripathi RD, Dwivedi S, Trivedi PK, Tandon PK (2007) Phytochelatins and antioxidant systems respond differentially during arsenite and arsenate stress in Hydrilla verticillata (L.f.) Royle. Environ Sci Technol 41(8):2930–2936

    Article  CAS  Google Scholar 

  • Su C, Jiang Y, Li F, Yang Y, Lu Q, Zhang T, Hu D, Xu Q (2017) Investigation of subcellular distribution, physiological, and biochemical changes in Spirodela polyrhiza as a function of cadmium exposure. Environ Exp Bot 142:24–33

    Article  CAS  Google Scholar 

  • Uddin MM, Chen Z, Huang L (2020) Cadmium accumulation, subcellular distribution and chemical fractionation in hydroponically grown Sesuvium portulacastrum [Aizoaceae]. PLoS ONE 15(12):e0244085

    Article  CAS  Google Scholar 

  • Wang SL, Liao WB, Yu FQ, Liao B, Shu WS (2009) Hyperaccumulation of lead, zinc, and cadmium in plants growing on a lead/zinc outcrop in Yunnan province, China. Environ Geol 58(3):471

    Article  CAS  Google Scholar 

  • Wang J, Zeng Q, Zhu J, Liu G, Tang H (2013) Dissimilarity of ascorbate–glutathione (AsA–GSH) cycle mechanism in two rice (Oryza sativa L.) cultivars under experimental free-air ozone exposure. Agr Ecosyst Environ 165:39–49. https://doi.org/10.1016/j.agee.2012.12.006

    Article  CAS  Google Scholar 

  • Wellburn AR, Lichtenthaler HK (1984) Formulae and program to determine total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Springer, Dordrecht, pp 9–12

    Google Scholar 

  • Woraharn S, Meeinkuirt W, Phusantisampan T, Avakul P (2021) Potential of ornamental monocot plants for rhizofiltration of cadmium and zinc in hydroponic systems. Environ Sci Pollut Res Int 28(26):35157–35170. https://doi.org/10.1007/s11356-021-13151-x

    Article  CAS  Google Scholar 

  • Wrzaczek M, Brosche M, Kangasjarvi J (2013) ROS signaling loops—production, perception, regulation. Curr Opin Plant Biol 16(5):575–582

    Article  CAS  Google Scholar 

  • Yamada M, Malambane G, Yamada S, Suharsono S, Tsujimoto H, Moseki B, Akashi K (2018) Differential physiological responses and tolerance to potentially toxic elements in biodiesel tree Jatropha curcas. Sci Rep 8(1):1635

    Article  Google Scholar 

  • Yang LP, Zhu J, Wang P, Zeng J, Tan R, Yang YZ, Liu ZM (2018) Effect of Cd on growth, physiological response, Cd subcellular distribution and chemical forms of Koelreuteria paniculata. Ecotoxicol Environ Saf 160:10–18. https://doi.org/10.1016/j.ecoenv.2018.05.026

    Article  CAS  Google Scholar 

  • Ye X, Ling T, Xue Y, Xu C, Zhou W, Hu L, Jian C, Shi Z (2016) Thymol mitigates cadmium stress by regulating glutathione levels and ROS homeostasis in tobacco seedlings. Molecules 21(10):1339

    Article  Google Scholar 

  • Yousaf B, Liu G, Wang R, Imtiaz M, Zia-Ur-Rehman M, Munir MA, Niu Z (2016) Bioavailability evaluation, uptake of heavy metals and potential health risks via dietary exposure in urban-industrial areas. Environ Sci Pollut Res Int 23(22):22443–22453. https://doi.org/10.1007/s11356-016-7449-8

    Article  CAS  Google Scholar 

  • Zhang XF, Zhang XH, Gao B, Li ZA, Xia HP, Li HF, Li J (2014) Effect of cadmium on growth, photosynthesis, mineral nutrition and metal accumulation of an energy crop, king grass (Pennisetum americanum × P. purpureum). Biomass Bioenergy 67:179–187

    Article  CAS  Google Scholar 

  • Zhou JH, Cheng K, Zheng JY, Liu ZQ, Shen WB, Fan HB, Jin ZN (2019) Physiological and biochemical characteristics of Cinnamomum camphora in response to Cu- and Cd-contaminated soil. Water Air Soil Pollut 230(1):15

    Article  Google Scholar 

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This work was supported by the National Natural Science Foundation of China (32001356).

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    1. College of Landscape Architecture, Sichuan Agricultural University, Chengdu, 611130, China

      Yin Jia, Xiancai Yin, Jian Zhao, Yuanzhi Pan, Beibei Jiang, Qinglin Liu & Yifeng Li

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    1. Yin Jia
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    2. Xiancai Yin
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    Contributions

    All authors contributed to the study conception and design. Material preparation and implementation of experiments were performed by Jian Zhao and Yifeng Li, and the data collection and analysis were performed by Yuanzhi Pan and Beibei Jiang. The manuscript was written by Yin Jia and Xiancai Yin, and Qinglin Liu made some modifications to the manuscript. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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    Jia, Y., Yin, X., Zhao, J. et al. Differential physiological responses and tolerance to potentially toxic elements in Primula forbesii Franch. Environ Sci Pollut Res 30, 67200–67216 (2023). https://doi.org/10.1007/s11356-023-27259-9

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