Investigating Phragmites australis response to copper exposure using physiologic, Fourier Transform Infrared and metabolomic approaches†
Jieting Wu A * , Tian Gao A , Lei Zhao B , Hongxu Bao A , Chang Yu A , Jianing Hu C and Fang Ma B *A School of Environmental Science, Liaoning University, Shenyang 110036, People’s Republic of China.
B State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of Technology, Harbin 150090, People’s Republic of China.
C Dalian Neusoft University of Information, Dalian 116032, People’s Republic of China.
Functional Plant Biology 49(4) 365-381 https://doi.org/10.1071/FP21258
Submitted: 3 September 2021 Accepted: 19 January 2022 Published: 21 February 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Phragmites australis (Cav.) Trin. ex Steud is a landscape plant with resistance to heavy metals that has significance in phytoremediation. However, little is known about the metabolomic background of the heavy metal resistance mechanisms of Phragmites. We studied copper stress on Phragmites and monitored physiological indicators such as malondialdehyde (MDA) and electrolyte leakage (EL). In addition, Fourier Transform Infrared (FTIR) was used to study the related chemical composition in the roots, stems, and leaves under copper stress. Furthermore, LC–MS technology was used to analyse the plants metabolic profile. Results showed that increased copper concentration in Phragmites led to the accumulation of MDA and EL. FTIR spectrum detected the presence of O–H and C=O stretching. O–H stretching was related to the presence of flavonoids, while C=O stretching reflected the presence of protein amide I. The latter was related to the change of amino acid composition. Both flavonoids and amino acids are regarded as contributors to the antioxidant of Phragmites under copper stress. Metabolomics analysis revealed that arginine and ayarin were accumulated and Phragmites leaves responded to copper stress with changes in the pool size of arginine and ayarin. It is speculated that they could improve resistance. Arginine is accumulated through two pathways: the citrulline decomposition and conversion pathway; and the circular pathway composed of ornithine, citrulline, l-argininosuccinate and arginine. Ayarin is synthesised through the quercetin methylation pathway. This study elucidates the antioxidant mechanisms for enhancing its resistance to heavy metal stress, thus improving of phytoremediation efficiency.
Keywords: arginine, ayarin, copper, FTIR, metabolomics, Phragmites australis, phytoremediation, plant resistance.
References
Agati G, Brunetti C, Fini A, Gori A, Guidi L, Landi M, Sebastiani F, Tattini M (2020) Are flavonoids effective antioxidants in plants? twenty years of our investigation. Antioxidants 9, 1098| Are flavonoids effective antioxidants in plants? twenty years of our investigation.Crossref | GoogleScholarGoogle Scholar |
Akhtar S, Shoaib A (2020) The counter defence system of antioxidants in Coelomycetous emerging human and plant pathogenic fungus Macrophomina phaseolina against copper toxicity. Environmental Science and Pollution Research 27, 597–606.
| The counter defence system of antioxidants in Coelomycetous emerging human and plant pathogenic fungus Macrophomina phaseolina against copper toxicity.Crossref | GoogleScholarGoogle Scholar | 31808087PubMed |
Ali F Ali F Ali F (2017) Health functionality of apigenin: a review. International Journal of Food Properties 20, 1197–1238.
| Health functionality of apigenin: a review.Crossref | GoogleScholarGoogle Scholar |
Arbona V, Manzi M, Ollas CD, Gómez-Cadenas A (2013) Metabolomics as a tool to investigate abiotic stress tolerance in plants. International Journal of Molecular Sciences 14, 4885–4911.
| Metabolomics as a tool to investigate abiotic stress tolerance in plants.Crossref | GoogleScholarGoogle Scholar | 23455464PubMed |
Balasundram N, Sundram K, Samman S (2006) Phenolic compounds in plants and agri-industrial by-products: antioxidant activity, occurrence, and potential uses. Food Chemistry 99, 191–203.
| Phenolic compounds in plants and agri-industrial by-products: antioxidant activity, occurrence, and potential uses.Crossref | GoogleScholarGoogle Scholar |
Bartošová A, Blinová L, Gerulová K (2015) Characterisation of polysacharides and lipids from selected green algae species by FTIR-ATR spectroscopy. Research Papers Faculty of Materials Science and Technology Slovak University of Technology 23, 97–102.
| Characterisation of polysacharides and lipids from selected green algae species by FTIR-ATR spectroscopy.Crossref | GoogleScholarGoogle Scholar |
Bonanno G (2013) Comparative performance of trace element bioaccumulation and biomonitoring in the plant species Typha domingensis, Phragmites australis and Arundo donax. Ecotoxicology and Environmental Safety 97, 124–130.
| Comparative performance of trace element bioaccumulation and biomonitoring in the plant species Typha domingensis, Phragmites australis and Arundo donax.Crossref | GoogleScholarGoogle Scholar | 23932595PubMed |
Breuillard C, Cynober L, Moinard C (2015) Citrulline and nitrogen homeostasis: an overview. Amino Acids 47, 685–691.
| Citrulline and nitrogen homeostasis: an overview.Crossref | GoogleScholarGoogle Scholar | 25676932PubMed |
Bukhari SB, Memon S, Mahroof-Tahir M, Bhanger MI (2009) Synthesis, characterization and antioxidant activity copper–quercetin complex. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 71, 1901–1906.
| Synthesis, characterization and antioxidant activity copper–quercetin complex.Crossref | GoogleScholarGoogle Scholar |
Carricondo JM, Oliver-Villanueva JV, Turégano JV, González JA, Mengual J (2021) Use of Phragmites australis for controlling phosphorus contamination in anthropogenic wetland ecosystems. Environmental Technology 42, 3055–3064.
| Use of Phragmites australis for controlling phosphorus contamination in anthropogenic wetland ecosystems.Crossref | GoogleScholarGoogle Scholar | 31986998PubMed |
Chen D, Shao Q, Yin L, Younis A, Zheng B (2019) Polyamine function in plants: metabolism, regulation on development, and roles in abiotic stress responses. Frontiers in Plant Science 9, 1945
| Polyamine function in plants: metabolism, regulation on development, and roles in abiotic stress responses.Crossref | GoogleScholarGoogle Scholar | 30687350PubMed |
Clark TC, Tinsley J, Sigholt T, Macqueen DJ, Martin SAM (2020) Supplementation of arginine, ornithine and citrulline in rainbow trout (Oncorhynchus mykiss): effects on growth, amino acid levels in plasma and gene expression responses in liver tissue. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 241, 110632
| Supplementation of arginine, ornithine and citrulline in rainbow trout (Oncorhynchus mykiss): effects on growth, amino acid levels in plasma and gene expression responses in liver tissue.Crossref | GoogleScholarGoogle Scholar |
Deng S-P, Yang Y-L, Cheng X-X, Li W-R, Cai J-Y (2019) Synthesis, spectroscopic study and radical scavenging activity of Kaempferol derivatives: enhanced water solubility and antioxidant activity. International Journal of Molecular Sciences 20, 975
| Synthesis, spectroscopic study and radical scavenging activity of Kaempferol derivatives: enhanced water solubility and antioxidant activity.Crossref | GoogleScholarGoogle Scholar |
Dixon RA, Strack D (2003) Phytochemistry meets genome analysis, and beyond………. Phytochemistry 62, 815–816.
| Phytochemistry meets genome analysis, and beyond……….Crossref | GoogleScholarGoogle Scholar | 12590109PubMed |
Dogan Y, Baslar S, Ugulu I (2014) A study on detecting heavy metal accumulation through biomonitoring: content of trace elements in plants at Mount Kazdagi in Turkey. Applied Ecology and Environmental Research 12, 627–636.
| A study on detecting heavy metal accumulation through biomonitoring: content of trace elements in plants at Mount Kazdagi in Turkey.Crossref | GoogleScholarGoogle Scholar |
Domingos P, Prado AM, Wong A, Gehring C, Feijo JA (2015) Nitric oxide: a multitasked signaling gas in plants. Molecular Plant 8, 506–520.
| Nitric oxide: a multitasked signaling gas in plants.Crossref | GoogleScholarGoogle Scholar | 25680232PubMed |
Dong N-Q, Lin H-X (2021) Contribution of phenylpropanoid metabolism to plant development and plant–environment interactions. Journal of Integrative Plant Biology 63, 180–209.
| Contribution of phenylpropanoid metabolism to plant development and plant–environment interactions.Crossref | GoogleScholarGoogle Scholar | 33325112PubMed |
Dou X, Zhou Z, Ren R, Xu M (2020) Apigenin, flavonoid component isolated from Gentiana veitchiorum flower suppresses the oxidative stress through LDLR-LCAT signaling pathway. Biomedicine & Pharmacotherapy 128, 110298
| Apigenin, flavonoid component isolated from Gentiana veitchiorum flower suppresses the oxidative stress through LDLR-LCAT signaling pathway.Crossref | GoogleScholarGoogle Scholar |
Farid M, Ali S, Rizwan M, Yasmeen T, Salim M Farid M, Ali S, Rizwan M, Yasmeen T, Salim M Farid M, Ali S, Rizwan M, Yasmeen T, Salim M Farid M, Ali S, Rizwan M, Yasmeen T, Salim M Farid M, Ali S, Rizwan M, Yasmeen T, Salim M (2020) Combined effects of citric acid and 5-aminolevulinic acid in mitigating chromium toxicity in sunflower (Helianthus annuus L.) grown in Cr spiked soil. Pakistan Journal of Agricultural Sciences 57, 477–488.
| Combined effects of citric acid and 5-aminolevulinic acid in mitigating chromium toxicity in sunflower (Helianthus annuus L.) grown in Cr spiked soil.Crossref | GoogleScholarGoogle Scholar |
Farooq MA, Islam F, Ali B, Najeeb U, Mao B, Gill RA, Yan G, Siddique KHM, Zhou W (2016) Arsenic toxicity in plants: cellular and molecular mechanisms of its transport and metabolism. Environmental and Experimental Botany 132, 42–52.
| Arsenic toxicity in plants: cellular and molecular mechanisms of its transport and metabolism.Crossref | GoogleScholarGoogle Scholar |
Fragkos K (2018) Citrulline and the intestine. pp. 1–313. Doctoral thesis, UCL (University College London).
Gautam V, Sharma P, Bakshi P, Arora S, Bhardwaj R, Paray BA, Alyemeni MN, Ahmad P (2020) Effect of Rhododendron arboreum leaf extract on the antioxidant defense system against chromium (VI) stress in Vigna radiata plants. Plants 9, 164
| Effect of Rhododendron arboreum leaf extract on the antioxidant defense system against chromium (VI) stress in Vigna radiata plants.Crossref | GoogleScholarGoogle Scholar |
Guo L, Gao L, Ma X, Guo F, Ruan H, Bao Y, Xia T, Wang Y (2019) Functional analysis of flavonoid 3′-hydroxylase and flavonoid 3′,5′-hydroxylases from tea plant (Camellia sinensis), involved in the B-ring hydroxylation of flavonoids. Gene 717, 144046
| Functional analysis of flavonoid 3′-hydroxylase and flavonoid 3′,5′-hydroxylases from tea plant (Camellia sinensis), involved in the B-ring hydroxylation of flavonoids.Crossref | GoogleScholarGoogle Scholar | 31434006PubMed |
Gupta D, Gupta RK (2011) Bioprotective properties of Dragon’s blood resin: in vitro evaluation of antioxidant activity and antimicrobial activity. BMC Complementary and Alternative Medicine 11, 13
| Bioprotective properties of Dragon’s blood resin: in vitro evaluation of antioxidant activity and antimicrobial activity.Crossref | GoogleScholarGoogle Scholar | 21329518PubMed |
Halliwell B (1991) Reactive oxygen species in living systems: source, biochemistry, and role in human disease. The American Journal of Medicine 91, S14–S22.
| Reactive oxygen species in living systems: source, biochemistry, and role in human disease.Crossref | GoogleScholarGoogle Scholar |
Harborne JB, Williams CA (2000) Advances in flavonoid research since 1992. Phytochemistry 55, 481–504.
| Advances in flavonoid research since 1992.Crossref | GoogleScholarGoogle Scholar | 11130659PubMed |
Hartman JL, Wehner TC, Ma G, Perkins-Veazie P (2019) Citrulline and arginine content of taxa of Cucurbitaceae. Horticulturae 5, 22
| Citrulline and arginine content of taxa of Cucurbitaceae.Crossref | GoogleScholarGoogle Scholar |
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125, 189–198.
| Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation.Crossref | GoogleScholarGoogle Scholar | 5655425PubMed |
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 |
Hou Q, Ufer G, Bartels D (2016) Lipid signalling in plant responses to abiotic stress. Plant, Cell & Environment 39, 1029–1048.
| Lipid signalling in plant responses to abiotic stress.Crossref | GoogleScholarGoogle Scholar |
Huang X, Wang L, Zhu S, Ho S-H, Wu J, Kalita PK, Ma F (2018) Unraveling the effects of arbuscular mycorrhizal fungus on uptake, translocation, and distribution of cadmium in Phragmites australis (Cav.) Trin. ex Steud. Ecotoxicology and Environmental Safety 149, 43–50.
| Unraveling the effects of arbuscular mycorrhizal fungus on uptake, translocation, and distribution of cadmium in Phragmites australis (Cav.) Trin. ex Steud.Crossref | GoogleScholarGoogle Scholar | 29149661PubMed |
Ishige K, Schubert D, Sagara Y (2001) Flavonoids protect neuronal cells from oxidative stress by three distinct mechanisms. Free Radical Biology and Medicine 30, 433–446.
| Flavonoids protect neuronal cells from oxidative stress by three distinct mechanisms.Crossref | GoogleScholarGoogle Scholar | 11182299PubMed |
Iwashina T (2003) Flavonoid function and activity to plants and other organisms. Biological Sciences in Space 17, 24–44.
| Flavonoid function and activity to plants and other organisms.Crossref | GoogleScholarGoogle Scholar | 12897458PubMed |
Jia L, Wu Q, Ye N, Liu R, Shi L, Xu W, Zhi H, Rahman ANMRB, Xia Y, Zhang J (2012) Proanthocyanidins inhibit seed germination by maintaining a high level of abscisic acid in Arabidopsis thaliana. Journal of Integrative Plant Biology 54, 663–673.
| Proanthocyanidins inhibit seed germination by maintaining a high level of abscisic acid in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 22765383PubMed |
Jortzik E, Fritz-Wolf K, Sturm N, Hipp M, Rahlfs S, Becker K (2010) Redox regulation of Plasmodium falciparum ornithine δ-aminotransferase. Journal of Molecular Biology 402, 445–459.
| Redox regulation of Plasmodium falciparum ornithine δ-aminotransferase.Crossref | GoogleScholarGoogle Scholar | 20673832PubMed |
Joshi V, Fernie AR (2017) Citrulline metabolism in plants. Amino Acids 49, 1543–1559.
| Citrulline metabolism in plants.Crossref | GoogleScholarGoogle Scholar | 28741223PubMed |
Ju W, Liu L, Fang L, Cui Y, Duan C, Wu H (2019) Impact of co-inoculation with plant-growth-promoting rhizobacteria and rhizobium on the biochemical responses of alfalfa-soil system in copper contaminated soil. Ecotoxicology and Environmental Safety 167, 218–226.
| Impact of co-inoculation with plant-growth-promoting rhizobacteria and rhizobium on the biochemical responses of alfalfa-soil system in copper contaminated soil.Crossref | GoogleScholarGoogle Scholar | 30342354PubMed |
Kalaichelvi K, Dhivya SM (2017) Screening of phytoconstituents, UV-VIS Spectrum and FTIR analysis of Micrococca mercurialis (L.) Benth. International Journal of Herbal Medicine 5, 40–44.
Kapoor D, Singh S, Kumar V, Romero R, Prasad R, Singh J (2019) Antioxidant enzymes regulation in plants in reference to reactive oxygen species (ROS) and reactive nitrogen species (RNS). Plant Gene 19, 100182
| Antioxidant enzymes regulation in plants in reference to reactive oxygen species (ROS) and reactive nitrogen species (RNS).Crossref | GoogleScholarGoogle Scholar |
Kato K, Ninomiya M, Tanaka K, Koketsu M (2016) Effects of functional groups and sugar composition of Quercetin derivatives on their radical scavenging properties. Journal of Natural Products 79, 1808–1814.
| Effects of functional groups and sugar composition of Quercetin derivatives on their radical scavenging properties.Crossref | GoogleScholarGoogle Scholar | 27314621PubMed |
Keurentjes JJB (2009) Genetical metabolomics: closing in on phenotypes. Current Opinion in Plant Biology 12, 223–230.
| Genetical metabolomics: closing in on phenotypes.Crossref | GoogleScholarGoogle Scholar |
Khan ZI, Ahmad K, Rehman S, Ashfaq A, Mehmood N, Ugulu I, Dogan Y (2019) Effect of sewage water irrigation on accumulation of metals in soil and wheat in Punjab, Pakistan. Pakistan Journal of Analytical & Environmental Chemistry 20, 60–66.
| Effect of sewage water irrigation on accumulation of metals in soil and wheat in Punjab, Pakistan.Crossref | GoogleScholarGoogle Scholar |
Koilraj P, Kalusulingam R, Sasaki K (2019) Arginine and lysine-functionalized layered double hydroxides as efficient sorbents for radioactive Co2+ removal by chelate-facilitated immobilization. Chemical Engineering Journal 374, 359–369.
| Arginine and lysine-functionalized layered double hydroxides as efficient sorbents for radioactive Co2+ removal by chelate-facilitated immobilization.Crossref | GoogleScholarGoogle Scholar |
Kováčik J, Klejdus B, Bačkor M (2009) Phenolic metabolism of Matricaria chamomilla plants exposed to nickel. Journal of Plant Physiology 166, 1460–1464.
| Phenolic metabolism of Matricaria chamomilla plants exposed to nickel.Crossref | GoogleScholarGoogle Scholar | 19380176PubMed |
Kováčik J, Klejdus B, Hedbavny J, Bačkor M (2010) Effect of copper and salicylic acid on phenolic metabolites and free amino acids in Scenedesmus quadricauda (Chlorophyceae). Plant Science 178, 307–311.
| Effect of copper and salicylic acid on phenolic metabolites and free amino acids in Scenedesmus quadricauda (Chlorophyceae).Crossref | GoogleScholarGoogle Scholar |
Kumar A, Dubey AK, Kumar V, Ansari MA, Narayan S Kumar A, Dubey AK, Kumar V, Ansari MA, Narayan S Kumar A, Dubey AK, Kumar V, Ansari MA, Narayan S (2020) Over-expression of chickpea glutaredoxin (CaGrx) provides tolerance to heavy metals by reducing metal accumulation and improved physiological and antioxidant defence system. Ecotoxicology and Environmental Safety 192, 110252
| Over-expression of chickpea glutaredoxin (CaGrx) provides tolerance to heavy metals by reducing metal accumulation and improved physiological and antioxidant defence system.Crossref | GoogleScholarGoogle Scholar | 32014725PubMed |
Kumar V, Roy BK (2018) Population authentication of the traditional medicinal plant Cassia tora L. based on ISSR markers and FTIR analysis. Scientific Reports 8, 10714
| Population authentication of the traditional medicinal plant Cassia tora L. based on ISSR markers and FTIR analysis.Crossref | GoogleScholarGoogle Scholar | 30013159PubMed |
Kusano M, Yang Z, Okazaki Y, Nakabayashi R, Fukushima A, Saito K (2015) Using metabolomic approaches to explore chemical diversity in rice. Molecular Plant 8, 58–67.
| Using metabolomic approaches to explore chemical diversity in rice.Crossref | GoogleScholarGoogle Scholar | 25578272PubMed |
Lee WJ, Kim J, Lee D, Hong S-W, Lee H (2017) Arabidopsis UDP-glycosyltransferase 78D1-overexpressing plants accumulate higher levels of kaempferol 3-O-β-d-glucopyranoside than wild-type plants. Applied Biological Chemistry 60, 647–652.
| Arabidopsis UDP-glycosyltransferase 78D1-overexpressing plants accumulate higher levels of kaempferol 3-O-β-d-glucopyranoside than wild-type plants.Crossref | GoogleScholarGoogle Scholar |
Li J, Hossain MS, Ma H, Yang Q, Gong X, Yang P, Feng B (2020a) Comparative metabolomics reveals differences in flavonoid metabolites among different coloured buckwheat flowers. Journal of Food Composition and Analysis 85, 103335
| Comparative metabolomics reveals differences in flavonoid metabolites among different coloured buckwheat flowers.Crossref | GoogleScholarGoogle Scholar |
Li M-Y, Feng K, Hou X-L, Jiang Q, Xu Z-S, Wang G-L, Liu J-X, Wang F, Xiong A-S (2020b) The genome sequence of celery (Apium graveolens L.), an important leaf vegetable crop rich in apigenin in the Apiaceae family. Horticulture Research 7, 9
| The genome sequence of celery (Apium graveolens L.), an important leaf vegetable crop rich in apigenin in the Apiaceae family.Crossref | GoogleScholarGoogle Scholar | 31934340PubMed |
Li Q, Song W, Sun M, Li J, Yu Z (2020c) Response of Bacillus vallismortis sp. EPS to exogenous sulfur stress/induction and its adsorption performance on Cu(II). Chemosphere 251, 126343
| Response of Bacillus vallismortis sp. EPS to exogenous sulfur stress/induction and its adsorption performance on Cu(II).Crossref | GoogleScholarGoogle Scholar | 32155492PubMed |
Lin Y-F, Aarts MGM (2012) The molecular mechanism of zinc and cadmium stress response in plants. Cellular and Molecular Life Sciences 69, 3187–3206.
| The molecular mechanism of zinc and cadmium stress response in plants.Crossref | GoogleScholarGoogle Scholar | 22903262PubMed |
Liu C, Xue Z, Tang D, Shen Y, Shi W, Ren L, Du G, Li Y, Cheng Z (2018b) Ornithine δ-aminotransferase is critical for floret development and seed setting through mediating nitrogen reutilization in rice. The Plant Journal 96, 842–854.
| Ornithine δ-aminotransferase is critical for floret development and seed setting through mediating nitrogen reutilization in rice.Crossref | GoogleScholarGoogle Scholar | 30144334PubMed |
Liu J, Wang J, Lee S, Wen R (2018a) Copper-caused oxidative stress triggers the activation of antioxidant enzymes via ZmMPK3 in maize leaves. PLoS ONE 13, e0203612
| Copper-caused oxidative stress triggers the activation of antioxidant enzymes via ZmMPK3 in maize leaves.Crossref | GoogleScholarGoogle Scholar | 30222757PubMed |
Liu N, Zhong G, Zhou J, Liu Y, Pang Y, Cai H, Wu Z (2019) Separate and combined effects of glyphosate and copper on growth and antioxidative enzymes in Salvinia natans (L.) All. Science of the Total Environment 655, 1448–1456.
| Separate and combined effects of glyphosate and copper on growth and antioxidative enzymes in Salvinia natans (L.) All.Crossref | GoogleScholarGoogle Scholar |
Łopusiewicz Ł, Mazurkiewicz-Zapałowicz K, Tkaczuk C (2020) Chemical changes in spores of the entomopathogenic fungus Metarhizium robertsii after exposure to heavy metals, studied through the use of FTIR spectroscopy. Journal of Elementology 25, 487–499.
| Chemical changes in spores of the entomopathogenic fungus Metarhizium robertsii after exposure to heavy metals, studied through the use of FTIR spectroscopy.Crossref | GoogleScholarGoogle Scholar |
Maestri E, Marmiroli M, Marmiroli N (2016) Bioactive peptides in plant-derived foodstuffs. Journal of Proteomics 147, 140–155.
| Bioactive peptides in plant-derived foodstuffs.Crossref | GoogleScholarGoogle Scholar | 27079980PubMed |
Maurya AK, Rani A (2017) Nitric oxide (NO) and physio-biochemical adaptation in plants against stress. In ‘Plant adaptation strategies in changing environment’. (Eds V Shukla, S Kumar, N Kumar) pp. 347–386. (Springer Singapore)
| Crossref |
Meenakshi S, Gnanambigai D, Tamil mozhi S, Arumugam M, Balasubramanian T (2009) Total flavanoid and in vitro antioxidant activity of two seaweeds of Rameshwaram coast. Global Journal of Pharmacology 3, 59–62.
Meyer H, Bolarinwa A, Wolfram G, Linseisen J (2006) Bioavailability of apigenin from apiin-rich parsley in humans. Annals of Nutrition and Metabolism 50, 167–172.
| Bioavailability of apigenin from apiin-rich parsley in humans.Crossref | GoogleScholarGoogle Scholar | 16407641PubMed |
Monné M, Miniero DV, Daddabbo L, Palmieri L, Porcelli V, Palmieri F (2015) Mitochondrial transporters for ornithine and related amino acids: a review. Amino Acids 47, 1763–1777.
| Mitochondrial transporters for ornithine and related amino acids: a review.Crossref | GoogleScholarGoogle Scholar | 26002808PubMed |
Nasibi F, Heidari T, Asrar Z, Mansoori H (2013) Effect of arginine pre-treatment on nickel accumulation and alleviation of the oxidative stress in Hyoscyamus niger. Journal of Soil Science and Plant Nutrition 13, 680–689.
| Effect of arginine pre-treatment on nickel accumulation and alleviation of the oxidative stress in Hyoscyamus niger.Crossref | GoogleScholarGoogle Scholar |
Nazir F, Hussain A, Fariduddin Q (2019) Hydrogen peroxide modulate photosynthesis and antioxidant systems in tomato (Solanum lycopersicum L.) plants under copper stress. Chemosphere 230, 544–558.
| Hydrogen peroxide modulate photosynthesis and antioxidant systems in tomato (Solanum lycopersicum L.) plants under copper stress.Crossref | GoogleScholarGoogle Scholar | 31125883PubMed |
Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxidation in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry 95, 351–358.
| Assay for lipid peroxidation in animal tissues by thiobarbituric acid reaction.Crossref | GoogleScholarGoogle Scholar |
Pandey N (2018) Role of plant nutrients in plant growth and physiology. In ‘Plant nutrients and abiotic stress tolerance’. (Eds M Hasanuzzaman, M Fujita, H Oku, K Nahar, B Hawrylak-Nowak) pp. 1–31. (Springer Singapore)
Pang J, Chan GSY, Zhang J, Liang J, Wong MH (2003) Physiological aspects of vetiver grass for rehabilitation in abandoned metalliferous mine wastes. Chemosphere 52, 1559–1570.
| Physiological aspects of vetiver grass for rehabilitation in abandoned metalliferous mine wastes.Crossref | GoogleScholarGoogle Scholar | 12867189PubMed |
Patle TK, Shrivas K, Kurrey R, Upadhyay S, Jangde R, Chauhan R (2020) Phytochemical screening and determination of phenolics and flavonoids in Dillenia pentagyna using UV–vis and FTIR spectroscopy. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 242, 118717
| Phytochemical screening and determination of phenolics and flavonoids in Dillenia pentagyna using UV–vis and FTIR spectroscopy.Crossref | GoogleScholarGoogle Scholar |
Pękal A, Biesaga M, Pyrzynska K (2011) Interaction of quercetin with copper ions: complexation, oxidation and reactivity towards radicals. BioMetals 24, 41–49.
| Interaction of quercetin with copper ions: complexation, oxidation and reactivity towards radicals.Crossref | GoogleScholarGoogle Scholar | 20835752PubMed |
Peng H, Wang Y, Tan TL, Chen Z (2020) Exploring the phytoremediation potential of water hyacinth by FTIR spectroscopy and ICP-OES for treatment of heavy metal contaminated water. International Journal of Phytoremediation 22, 939–951.
| Exploring the phytoremediation potential of water hyacinth by FTIR spectroscopy and ICP-OES for treatment of heavy metal contaminated water.Crossref | GoogleScholarGoogle Scholar | 32529840PubMed |
Peng X, Zheng Z, Cheng K-W, Shan F, Ren G-X, Chen F, Wang M (2008) Inhibitory effect of mung bean extract and its constituents vitexin and isovitexin on the formation of advanced glycation endproducts. Food Chemistry 106, 475–481.
| Inhibitory effect of mung bean extract and its constituents vitexin and isovitexin on the formation of advanced glycation endproducts.Crossref | GoogleScholarGoogle Scholar |
Petukhov A, Kremleva T, Petukhova G, Khritokhin N (2021) Biochemical responses of medicinal plant Tussilago farfara L. to elevated heavy metal concentrations in soils of urban areas. Toxics 9, 171
| Biochemical responses of medicinal plant Tussilago farfara L. to elevated heavy metal concentrations in soils of urban areas.Crossref | GoogleScholarGoogle Scholar | 34357914PubMed |
Pisoschi AM, Pop A (2015) The role of antioxidants in the chemistry of oxidative stress: a review. European Journal of Medicinal Chemistry 97, 55–74.
| The role of antioxidants in the chemistry of oxidative stress: a review.Crossref | GoogleScholarGoogle Scholar | 25942353PubMed |
Rafi M, Septaningsih DA, Karomah AH Rafi M, Septaningsih DA, Karomah AH Rafi M, Septaningsih DA, Karomah AH (2021) Inhibition of α-glucosidase activity, metals content, and phytochemical profiling of Andrographis paniculata from different geographical origins based on FTIR and UHPLC-Q-Orbitrap HRMS metabolomics. Biodiversitas 22, 1535–1542.
| Inhibition of α-glucosidase activity, metals content, and phytochemical profiling of Andrographis paniculata from different geographical origins based on FTIR and UHPLC-Q-Orbitrap HRMS metabolomics.Crossref | GoogleScholarGoogle Scholar |
Rani S, Pooja K, Pal GK (2018) Exploration of rice protein hydrolysates and peptides with special reference to antioxidant potential: computational derived approaches for bio-activity determination. Trends in Food Science & Technology 80, 61–70.
| Exploration of rice protein hydrolysates and peptides with special reference to antioxidant potential: computational derived approaches for bio-activity determination.Crossref | GoogleScholarGoogle Scholar |
Riaz M, Kamran M, Fang Y, Wang Q, Cao H, Yang G, Deng L, Wang Y, Zhou Y, Anastopoulos I, Wang X (2021) Arbuscular mycorrhizal fungi-induced mitigation of heavy metal phytotoxicity in metal contaminated soils: a critical review. Journal of Hazardous Materials 402, 123919
| Arbuscular mycorrhizal fungi-induced mitigation of heavy metal phytotoxicity in metal contaminated soils: a critical review.Crossref | GoogleScholarGoogle Scholar | 33254825PubMed |
Roubeau Dumont E, Elger A, Azéma C, Castillo Michel H, Surble S, Larue C (2022) Cutting-edge spectroscopy techniques highlight toxicity mechanisms of copper oxide nanoparticles in the aquatic plant Myriophyllum spicatum. Science of the Total Environment 803, 150001
| Cutting-edge spectroscopy techniques highlight toxicity mechanisms of copper oxide nanoparticles in the aquatic plant Myriophyllum spicatum.Crossref | GoogleScholarGoogle Scholar |
Sahin I, Akcicek E, Guner O, Dogan Y, Ugulu I (2016) An investigation on determining heavy metal accumulation in plants growing at Kumalar Mountain in Turkey. Eurasian Journal of Biosciences 10, 22–29.
| An investigation on determining heavy metal accumulation in plants growing at Kumalar Mountain in Turkey.Crossref | GoogleScholarGoogle Scholar |
Saleem MH, Fahad S, Khan SU, Din M, Ullah A, Sabagh AE, Hossain A, Llanes A, Liu L (2020a) Copper-induced oxidative stress, initiation of antioxidants and phytoremediation potential of flax (Linum usitatissimum L.) seedlings grown under the mixing of two different soils of China. Environmental Science and Pollution Research 27, 5211–5221.
| Copper-induced oxidative stress, initiation of antioxidants and phytoremediation potential of flax (Linum usitatissimum L.) seedlings grown under the mixing of two different soils of China.Crossref | GoogleScholarGoogle Scholar | 31848948PubMed |
Saleem MH, Fahad S, Rehman M, Saud S, Jamal Y, Khan S, Liu L (2020b) Morpho-physiological traits, biochemical response and phytoextraction potential of short-term copper stress on kenaf (Hibiscus cannabinus L.) seedlings. PeerJ 8, e8321
| Morpho-physiological traits, biochemical response and phytoextraction potential of short-term copper stress on kenaf (Hibiscus cannabinus L.) seedlings.Crossref | GoogleScholarGoogle Scholar | 32030320PubMed |
Samaras L, Sicilia M-A, García-Barriocanal E (2021) Predicting epidemics using search engine data: a comparative study on measles in the largest countries of Europe. BMC Public Health 21, 100
| Predicting epidemics using search engine data: a comparative study on measles in the largest countries of Europe.Crossref | GoogleScholarGoogle Scholar | 33472589PubMed |
Sharma A, Shahzad B, Rehman A, Bhardwaj R, Landi M, Zheng B (2019) Response of phenylpropanoid pathway and the role of polyphenols in plants under abiotic stress. Molecules 24, 2452
| Response of phenylpropanoid pathway and the role of polyphenols in plants under abiotic stress.Crossref | GoogleScholarGoogle Scholar |
Siano F, Moccia S, Picariello G, Russo GL, Sorrentino G, Di Stasio M, La Cara F, Volpe MG (2019) Comparative study of chemical, biochemical characteristic and ATR-FTIR analysis of seeds, oil and flour of the edible fedora cultivar Hemp (Cannabis sativa L.). Molecules 24, 83
| Comparative study of chemical, biochemical characteristic and ATR-FTIR analysis of seeds, oil and flour of the edible fedora cultivar Hemp (Cannabis sativa L.).Crossref | GoogleScholarGoogle Scholar |
Singh A, Singh NB, Hussain I, Singh H (2017) Effect of biologically synthesized copper oxide nanoparticles on metabolism and antioxidant activity to the crop plants Solanum lycopersicum and Brassica oleracea var. botrytis. Journal of Biotechnology 262, 11–27.
| Effect of biologically synthesized copper oxide nanoparticles on metabolism and antioxidant activity to the crop plants Solanum lycopersicum and Brassica oleracea var. botrytis.Crossref | GoogleScholarGoogle Scholar | 28962841PubMed |
Singh S, Kumar V, Kapoor D, Kumar S, Singh S, Dhanjal DS, Datta S, Samuel J, Dey P, Wang S, Prasad R, Singh J (2020) Revealing on hydrogen sulfide and nitric oxide signals co-ordination for plant growth under stress conditions. Physiologia Plantarum 168, 301–317.
| Revealing on hydrogen sulfide and nitric oxide signals co-ordination for plant growth under stress conditions.Crossref | GoogleScholarGoogle Scholar | 31264712PubMed |
Slater TF (1984a) Free-radical mechanisms in tissue injury. Biochemical Journal 222, 1–15.
| Free-radical mechanisms in tissue injury.Crossref | GoogleScholarGoogle Scholar |
Slater TF (1984b) [33] Overview of methods used for detecting lipid peroxidation. In ‘Methods in enzymology. Vol. 105’. (Ed. L Packer) pp. 283–293. (Academic Press)
| Crossref |
Ugulu I (2015) Determination of heavy metal accumulation in plant samples by spectrometric techniques in Turkey. Applied Spectroscopy Reviews 50, 113–151.
| Determination of heavy metal accumulation in plant samples by spectrometric techniques in Turkey.Crossref | GoogleScholarGoogle Scholar |
Ugulu I, Dogan Y, Baslar S, Varol O (2012) Biomonitoring of trace element accumulation in plants growing at Murat Mountain. International Journal of Environmental Science and Technology 9, 527–534.
| Biomonitoring of trace element accumulation in plants growing at Murat Mountain.Crossref | GoogleScholarGoogle Scholar |
Ugulu I, Unver MC, Dogan Y (2016) Determination and comparison of heavy metal accumulation level of Ficus carica bark and leaf samples in Artvin, Turkey. Oxidation Communications 39, 765–775.
Unver MC, Ugulu I, Durkan N, Baslar S, Dogan Y (2015) Heavy metal contents of Malva sylvestris sold as edible greens in the local markets of Izmir. Ekoloji 24, 13–25.
| Heavy metal contents of Malva sylvestris sold as edible greens in the local markets of Izmir.Crossref | GoogleScholarGoogle Scholar |
Villiers F, Ducruix C, Hugouvieux V, Jarno N, Ezan E, Garin J, Junot C, Bourguignon J (2011) Investigating the plant response to cadmium exposure by proteomic and metabolomic approaches. Proteomics 11, 1650–1663.
| Investigating the plant response to cadmium exposure by proteomic and metabolomic approaches.Crossref | GoogleScholarGoogle Scholar | 21462346PubMed |
Vitalini S, Flamini G, Valaguzza A, Rodondi G, Iriti M, Fico G (2011) Primula spectabilis Tratt. aerial parts: morphology, volatile compounds and flavonoids. Phytochemistry 72, 1371–1378.
| Primula spectabilis Tratt. aerial parts: morphology, volatile compounds and flavonoids.Crossref | GoogleScholarGoogle Scholar | 21612805PubMed |
Wang S, He T, Xu F, Li X, Yuan L, Wang Q, Liu H (2021) Analysis of physiological and metabolite response of Celosia argentea to copper stress. Plant Biology 23, 391–399.
| Analysis of physiological and metabolite response of Celosia argentea to copper stress.Crossref | GoogleScholarGoogle Scholar | 32722892PubMed |
Watkins JM, Hechler PJ, Muday GK (2014) Ethylene-induced flavonol accumulation in guard cells suppresses reactive oxygen species and moderates stomatal aperture. Plant Physiology 164, 1707–1717.
| Ethylene-induced flavonol accumulation in guard cells suppresses reactive oxygen species and moderates stomatal aperture.Crossref | GoogleScholarGoogle Scholar | 24596331PubMed |
Winter G, Todd CD, Trovato M, Forlani G, Funck D (2015) Physiological implications of arginine metabolism in plants. Frontiers in Plant Science 6, 534
| Physiological implications of arginine metabolism in plants.Crossref | GoogleScholarGoogle Scholar | 26284079PubMed |
Wu J, Wang L, Ma F, Yang J, Li S, Li Z (2013) Effects of vegetative-periodic-induced rhizosphere variation on the uptake and translocation of metals in Phragmites australis (Cav.) Trin ex. Steudel growing in the Sun Island Wetland. Ecotoxicology 22, 608–618.
| Effects of vegetative-periodic-induced rhizosphere variation on the uptake and translocation of metals in Phragmites australis (Cav.) Trin ex. Steudel growing in the Sun Island Wetland.Crossref | GoogleScholarGoogle Scholar | 23455898PubMed |
Wu J, Wang L, Ma F, Zhao L, Huang X (2019) The speciation and distribution characteristics of Cu in Phragmites australis (Cav.) Trin ex. Steudel. Plant Biology 21, 873–881.
| The speciation and distribution characteristics of Cu in Phragmites australis (Cav.) Trin ex. Steudel.Crossref | GoogleScholarGoogle Scholar | 30929304PubMed |
Yadav P, Kaur R, Kanwar MK, Sharma A, Verma V, Sirhindi G, Bhardwaj R (2018) Castasterone confers copper stress tolerance by regulating antioxidant enzyme responses, antioxidants, and amino acid balance in B. juncea seedlings. Ecotoxicology and Environmental Safety 147, 725–734.
| Castasterone confers copper stress tolerance by regulating antioxidant enzyme responses, antioxidants, and amino acid balance in B. juncea seedlings.Crossref | GoogleScholarGoogle Scholar | 28942275PubMed |
Yan J, Yu L, Xu S, Gu W, Zhu W (2014) Apigenin accumulation and expression analysis of apigenin biosynthesis relative genes in celery. Scientia Horticulturae 165, 218–224.
| Apigenin accumulation and expression analysis of apigenin biosynthesis relative genes in celery.Crossref | GoogleScholarGoogle Scholar |
Ye ZH, Baker AJM, Wong MH, Willis AJ (2003) Copper tolerance, uptake and accumulation by Phragmites australis. Chemosphere 50, 795–800.
| Copper tolerance, uptake and accumulation by Phragmites australis.Crossref | GoogleScholarGoogle Scholar | 12688493PubMed |
Yu S, Sheng L, Mao H, Huang X, Luo L, Li Y (2020) Physiological response of Conyza Canadensis to cadmium stress monitored by Fourier transform infrared spectroscopy and cadmium accumulation. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 229, 118007
| Physiological response of Conyza Canadensis to cadmium stress monitored by Fourier transform infrared spectroscopy and cadmium accumulation.Crossref | GoogleScholarGoogle Scholar |
Zeng W, Zhang S, Xia M, Wu X, Qiu G, Shen L (2020) Insights into the production of extracellular polymeric substances of Cupriavidus pauculus 1490 under the stimulation of heavy metal ions. RSC Advances 10, 20385–20394.
| Insights into the production of extracellular polymeric substances of Cupriavidus pauculus 1490 under the stimulation of heavy metal ions.Crossref | GoogleScholarGoogle Scholar |
Zhang X, Herger AG, Ren Z, Li X, Cui Z (2020) Resistance effect of flavonols and toxicology analysis of hexabromocyclododecane based on soil-microbe-plant system. Chemosphere 257, 127248
| Resistance effect of flavonols and toxicology analysis of hexabromocyclododecane based on soil-microbe-plant system.Crossref | GoogleScholarGoogle Scholar | 32526471PubMed |
Zhao L, Huang Y, Paglia K, Vaniya A, Wancewicz B, Keller AA (2018) Metabolomics reveals the molecular mechanisms of copper induced cucumber leaf (Cucumis sativus) senescence. Environmental Science & Technology 52, 7092–7100.
| Metabolomics reveals the molecular mechanisms of copper induced cucumber leaf (Cucumis sativus) senescence.Crossref | GoogleScholarGoogle Scholar |
Zhu Y, Wang H, Lv X, Zhang Y, Wang W (2020) Effects of biochar and biofertilizer on cadmium-contaminated cotton growth and the antioxidative defense system. Scientific Reports 10, 20112
| Effects of biochar and biofertilizer on cadmium-contaminated cotton growth and the antioxidative defense system.Crossref | GoogleScholarGoogle Scholar | 33208871PubMed |
Zimmermann B, Bağcioğlu M, Tafinstseva V, Kohler A, Ohlson M, Fjellheim S (2017) A high-throughput FTIR spectroscopy approach to assess adaptive variation in the chemical composition of pollen. Ecology and Evolution 7, 10839–10849.
| A high-throughput FTIR spectroscopy approach to assess adaptive variation in the chemical composition of pollen.Crossref | GoogleScholarGoogle Scholar | 29299262PubMed |