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Wrack Composed by Fucus spp, Ascophyllum nodosum and Pelvetia canaliculata Limits Metal Uptake and Restores the Redox Homeostasis of Barley Plants Grown in Cu-Contaminated Soils

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Abstract

Since metal contamination compromises crop growth and food safety, eco-friendly responses to prevent this are needed. This study provided an integrative evaluation of the potential of wrack (macroalgae debris) to increase the tolerance of Hordeum vulgare L. (barley plant) to copper (Cu).Plants were grown in a soil mixed with 219 mg Cu kg−1 with/without 2% (m/m) wrack for 14 days. Copper impaired all growth-related parameters. Wrack application counteracted most of these negative impacts and lowered metal accumulation in roots. Metal exposure increased reactive oxygen species content [superoxide anion (O2•−) and hydrogen peroxide [H2O2]) and lipid peroxidation degree, which was evaluated through the quantification of malondialdehyde, while co-treatment with wrack partially reverted some of these effects. The non-enzymatic antioxidant (AOX) system was mainly activated by Cu, with accumulated glutathione (GSH), ascorbate (AsA) and phenols, mostly in roots, while proline content was reduced. Wrack protective action was through a modulation of GSH and AsA redox state and enhanced ascorbate peroxidase. The results suggest wrack’s potential to alleviate Cu-induced phytotoxicity, which probably relies on the reduction of Cu-induced oxidative stress through a more efficient activity of AOX metabolites and by limiting Cu absorption and bioaccumulation, especially in roots of barley plants.

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References

  • Adrees M, Ali S, Rizwan M, Ibrahim M, Abbas F, Farid M, Zia-Ur-Rehman M, Irshad MK, Bharwana SA (2015) The effect of excess copper on growth and physiology of important food crops: a review. Environ Sci Pollut Res 22:8148–8162

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Ahmad P, Sarwat M, Sharma S (2008) Reactive oxygen species, antioxidants and signaling in plants. J Plant Biol 51:167–173

    CAS  Google Scholar 

  • Ali MB, Singh N, Shohael AM, Hahn EJ, Paek K (2006) Phenolics metabolism and lignin synthesis in root suspension cultures of Panax ginseng in response to copper stress. Plant Sci 171:147–154

    CAS  Google Scholar 

  • Alobwede E, Leake JR, Pandhal J (2019) Circular economy fertilization: testing micro and macro algal species as soil improvers and nutrient sources for crop production in greenhouse and field conditions. Geoderma 334:113–123

    CAS  Google Scholar 

  • Anjos Neto APd, Oliveira GRF, Mello SdC, Silva MSd, Gomes-Junior FG, Novembre ADdLC, Azevedo RA (2020) Seed priming with seaweed extract mitigate heat stress in spinach: effect on germination, seedling growth and antioxidant capacity. Bragantia 79(4):502–511

    Google Scholar 

  • Anjum NA, Ahmad I, Mohmood I, Pacheco M, Duarte AC, Pereira E, Umar S, Ahmad A, Khan NA, Iqbal MJE (2012) Modulation of glutathione and its related enzymes in plants’ responses to toxic metals and metalloids—a review. J Exp Bot 75:307–324

    CAS  Google Scholar 

  • Arioli T, Mattner SW, Winberg PC (2015) Applications of seaweed extracts in Australian agriculture: past, present and future. J Appl Phycol 27:2007–2015

    PubMed  PubMed Central  Google Scholar 

  • Bates LS, Waldren RP, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    CAS  Google Scholar 

  • Battacharyya D, Babgohari MZ, Rathor P, Prithiviraj B (2015) Seaweed extracts as biostimulants in horticulture. Sci Hortic 196:39–48

    CAS  Google Scholar 

  • Beck R, Kalra Y, Vaughan B, Wolf A (2000) Soil analysis handbook of reference methods. Plant and Soil Analysis Council, 4th edn. CRC Press LLC, New York, p 109–115

  • Bielen A, Remans T, Vangronsveld J, Cuypers A (2013) The influence of metal stress on the availability and redox state of ascorbate, and possible interference with its cellular functions. J Mol Sci 14:6382–6413

    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 72:248–254

    CAS  PubMed  Google Scholar 

  • Branco-Neves S, Soares C, de Sousa A, Martins V, Azenha M, Gerós H, Fidalgo F (2017) An efficient antioxidant system and heavy metal exclusion from leaves make Solanum cheesmaniae more tolerant to Cu than its cultivated counterpart. Food Energy Secur 6:123–133

    Google Scholar 

  • Bulgari R, Franzoni G, Ferrante A (2019) Biostimulants application in horticultural crops under abiotic stress conditions. Agronomy 9:306

    CAS  Google Scholar 

  • Chen C-T, Chen T-H, Lo K-F, Chiu C (2004) Effects of proline on copper transport in rice seedlings under excess copper stress. Plant Sci 166:103–111

    CAS  Google Scholar 

  • Colombini I, Chelazzi L, Gibson R, Atkinson R (2003) Influence of marine allochthonous input on sandy beach communities. Oceanogr Mar Biol Annu Rev 41:115–159

    Google Scholar 

  • de Sousa A, Teixeira J, Regueiras MT, Azenha M, Silva F, Fidalgo F (2013) Metalaxyl-induced changes in the antioxidant metabolism of Solanum nigrum L. suspension cells. Pestic Biochem Physiol 107:235–243

    Google Scholar 

  • Dewis J, Freitas F (1970) Physical and chemical methods of soil and water analysis. FAO Soils Bulletin

  • Donahue JL, Okpodu CM, Cramer CL, Grabau EA, Alscher RG (1997) Responses of antioxidants to paraquat in pea leaves (relationships to resistance). Plant Physiol 113:249–257

    CAS  PubMed  PubMed Central  Google Scholar 

  • Duong HLS (2008) Investigating the ecological implications of wrack removal on South Australian sandy beaches. Flinders University, School of Biological Sciences, Australia

    Google Scholar 

  • Elansary HO, Skalicka-Woźniak K, King IW (2016) Enhancing stress growth traits as well as phytochemical and antioxidant contents of Spiraea and Pittosporum under seaweed extract treatments. Plant Physiol Biochem 105:310–320

    CAS  PubMed  Google Scholar 

  • European Commission (2020) Circular Economy Action Plan - for a cleaner and more competitive Europe. European Union Brussels, Belgium

  • European Union (2019) Regulation of the european parliament and of the council laying down rules on the making available on the market of EU fertilising products and amending regulations (EC) No 1069/2009 and (EC) No 1107/2009 and repealing regulation (EC) No 2003/2003. European Union Brussels, Belgium

    Google Scholar 

  • Fike J, Allen V, Schmidt R, Zhang X, Fontenot J, Bagley C, Ivy R, Evans R, Coelho R, Wester D (2001) Tasco-forage: I. Influence of a seaweed extract on antioxidant activity in tall fescue and in ruminants. J Anim Sci 79:1011–1021

    CAS  PubMed  Google Scholar 

  • Gajewska E, Skłodowska M (2007) Effect of nickel on ROS content and antioxidative enzyme activities in wheat leaves. Biometals 20:27–36

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Gillespie KM, Ainsworth EA (2007) Measurement of reduced, oxidized and total ascorbate content in plants. Nat Protoc 2:871

    CAS  PubMed  Google Scholar 

  • Gupta KJ, Igamberdiev AU, Manjunatha G, Segu S, Moran JF, Neelawarne B, Bauwe H, Kaiser W (2011) The emerging roles of nitric oxide (NO) in plant mitochondria. Plant Science 181:520-526

    CAS  PubMed  Google Scholar 

  • Gupta DK, Tohoyama H, Joho M, Inouhe M (2002) Possible role of phytochelatins and glutathione metabolism in cadmium tolerance in chickpea roots. J Plant Res 115:429–437

    CAS  PubMed  Google Scholar 

  • Handique G, Handique A (2009) Proline accumulation in lemongrass (Cymbopogon flexuosus Stapf.) due to heavy metal stress. J Environ Biol 30:299–302

    CAS  PubMed  Google Scholar 

  • Hasanuzzaman M, Nahar K, Anee TI, Fujita M (2017) Glutathione in plants: biosynthesis and physiological role in environmental stress tolerance. Physiol Mol Biol Plants 23:249–268

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Sci Behav 7:1456–1466

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • IPCC (2019) Climate change and land: an IPCC special report on climate change, desertification, land degradation, sustainable land management, food security, and greenhouse gas fluxes in terrestrial ecosystems. https://www.ipcc.ch/srccl/cite-report/

  • ISO (2008) Soil quality: effects of pollutants on earthworms (Eisenia fetida). Part 2. Determination of effects on reproduction. Annex C. ISO/Dis 11268-2.2. International Organization for Standardization, Geneva

    Google Scholar 

  • John R, Ahmad P, Gadgil K, Sharma S (2009) Heavy metal toxicity: effect on plant growth, biochemical parameters and metal accumulation by Brassica juncea L. Int J Plant Sci 3:66–75

    Google Scholar 

  • Khan W, Rayirath UP, Subramanian S, Jithesh MN, Rayorath P, Hodges DM, Critchley AT, Craigie JS, Norrie J, Prithiviraj B (2009) Seaweed extracts as biostimulants of plant growth and development. J Plant Growth Regul 28:386–399

    CAS  Google Scholar 

  • Khatun S, Ali MB, Hahn E-J, Paek K (2008) Copper toxicity in Withania somnifera: growth and antioxidant enzymes responses of in vitro grown plants. Enviorn Exp Bot 64:279–285

    CAS  Google Scholar 

  • Kono Y, Fridovich I (1982) Superoxide radical inhibits catalase. J Biol Chem 257:5751–5754

    CAS  PubMed  Google Scholar 

  • Li X, Ma H, Jia P, Wang J, Jia L, Zhang T, Yang Y, Chen H, Wei X (2012) Responses of seedling growth and antioxidant activity to excess iron and copper in Triticum aestivum L. Ecotoxicol Enviorn Saf 86:47–53

    CAS  Google Scholar 

  • Li D, Wu S, Liu L, Zhang Y, Li S (2018) Vulnerability of the global terrestrial ecosystems to climate change. Glob Change Biol 24:4095–4106

    Google Scholar 

  • Liang X, Zhang L, Natarajan SK, Becker DF (2013) Proline mechanisms of stress survival. Antioxid Redox Signal 19(9):998–1011

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lukatkin A, Egorova I, Michailova I, Malec P, Strzałka K (2014) Effect of copper on pro-and antioxidative reactions in radish (Raphanus sativus L.) in vitro and in vivo. J Trace Elem Med Biol 28:80–86

    CAS  PubMed  Google Scholar 

  • Macreadie PI, Bishop MJ, Booth DJ (2011) Implications of climate change for macrophytic rafts and their hitchhikers. Mar Ecol Prog Ser 443:285–292

    Google Scholar 

  • Macreadie PI, Trevathan-Tackett SM, Baldock JA, Kelleway JJ (2017) Converting beach-cast seagrass wrack into biochar: a climate-friendly solution to a coastal problem. Sci Total Environ 574:90–94

    CAS  PubMed  Google Scholar 

  • Mansori M, Chernane H, Latique S, Benaliat A, Hsissou D, El Kaoua M (2015) Seaweed extract effect on water deficit and antioxidative mechanisms in bean plants (Phaseolus vulgaris L.). J Appl Phycol 27:1689–1698

    Google Scholar 

  • Migocka M, Malas K (2018) Plant responses to copper: molecular and regulatory mechanisms of copper uptake, distribution and accumulation in plants. Plant micronutrient use efficiency. Elsevier, Amsterdam, pp 71–86

    Google Scholar 

  • Mittler R (2017) ROS are good. Trends Plant Sci 22:11–19

    CAS  PubMed  Google Scholar 

  • Mohanty D, Adhikary P, Chattopadhyay N (2013) Seaweed liquid fertilizer (SLF) and its role in agriculture productivity. Ecoscan 3:147–155

    Google Scholar 

  • Moore SK, Trainer VL, Mantua NJ, Parker MS, Laws EA, Backer LC, Fleming LE (2008) Impacts of climate variability and future climate change on harmful algal blooms and human health. Environ Health 7(Suppl 2):S4

    PubMed  PubMed Central  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Rastgoo L, Alemzadeh A (2011) Biochemical responses of Gouan (Aeluropus littoralis) to heavy metals stress. Aust J Plant Sci 5:375

    CAS  Google Scholar 

  • Rehman M, Liu L, Wang Q, Saleem MH, Bashir S, Ullah S, Peng D (2019) Copper environmental toxicology, recent advances, and future outlook: a review. Environ Sci Pollut Res 26:18003–18016

    CAS  Google Scholar 

  • Rice-Evans C, Miller N, Paganga G (1997) Antioxidant properties of phenolic compounds. Trends Plant Sci 2:152–159

    Google Scholar 

  • Rouphael Y, Colla G (2020) Biostimulants in agriculture. Front Plant Sci 11:40–47

    PubMed  PubMed Central  Google Scholar 

  • Rouphael Y, De Micco V, Arena C, Raimondi G, Colla G, De Pascale S (2017) Effect of Ecklonia maxima seaweed extract on yield, mineral composition, gas exchange, and leaf anatomy of zucchini squash grown under saline conditions. J Appl Phycol 29:459–470

    CAS  Google Scholar 

  • Santiago LJM, Louro RP, De Oliveira D (2000) Compartmentation of phenolic compounds and phenylalanine ammonia-lyase in leaves of Phyllanthus tenellus Roxb. and their induction by copper sulphate. Ann Bot 86:1023–1032

    CAS  Google Scholar 

  • Schutzendubel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365

    CAS  PubMed  Google Scholar 

  • Sgherri C, Milone MTA, Clijsters H, Navari-Izzo F (2001) Antioxidative enzymes in two wheat cultivars, differently sensitive to drought and subjected to subsymptomatic copper doses. J Plant Physiol 58:1439–1447

    Google Scholar 

  • Sharma HSS, Fleming C, Selby C, Rao JR, Martin T (2013) Plant biostimulants: a review on the processing of macroalgae and use of extracts for crop management to reduce abiotic and biotic stresses. J Appl Phycol 26:465–490

    Google Scholar 

  • Sharmila P, Kumari PK, Singh K, Prasad N, Pardha-Saradhi P (2017) Cadmium toxicity-induced proline accumulation is coupled to iron depletion. Protoplasma 254:763–770

    CAS  PubMed  Google Scholar 

  • Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319

    CAS  PubMed  Google Scholar 

  • Slima DF, Ahmed D (2020) Trace metals accumulated in pea plant (Pisum sativum L.) as a result of irrigation with wastewater. J Soil Sci Plant Nutr 20:2749–2760

    CAS  Google Scholar 

  • Soares C, de Sousa A, Pinto A, Azenha M, Teixeira J, Azevedo RA, Fidalgo F (2016) Effect of 24-epibrassinolide on ROS content, antioxidant system, lipid peroxidation and Ni uptake in Solanum nigrum L. under Ni stress. Enviorn Exp Bot 122:115–125

    CAS  Google Scholar 

  • Soares C, Carvalho ME, Azevedo RA, Fidalgo F (2019a) Plants facing oxidative challenges—a little help from the antioxidant networks. Environ Exp Bot 161:4–25

    CAS  Google Scholar 

  • Soares C, Pereira R, Spormann S, Fidalgo F (2019b) Is soil contamination by a glyphosate commercial formulation truly harmless to non-target plants?—evaluation of oxidative damage and antioxidant responses in tomato. Environ Pollut 247:256–265

    CAS  PubMed  Google Scholar 

  • Sousa B, Soares C, Oliveira F, Martins M, Branco-Neves S, Barbosa B, Ataíde I, Fidalgo F (2020) Foliar application of 24-epibrassinolide improves Solanum nigrum L. tolerance to high levels of Zn without affecting its remediation potential. Chemosphere 244:125579

    CAS  PubMed  Google Scholar 

  • Szabados L, Savoure A (2009) Proline: a multifunctional amino acid. Trends Plant Sci 15(2):89–98

    PubMed  Google Scholar 

  • Thounaojam TC, Panda P, Mazumdar P, Kumar D, Sharma G, Sahoo L, Sanjib P (2012) Excess copper induced oxidative stress and response of antioxidants in rice. Plant Physiol Biochem 53:33–39

    CAS  PubMed  Google Scholar 

  • Tripathi BN, Gaur J (2004) Relationship between copper-and zinc-induced oxidative stress and proline accumulation in Scenedesmus sp. Planta 219:397–404

    CAS  PubMed  Google Scholar 

  • US Environmental Protection Agency (1998) Method 3051a—microwave assisted acid digestion of sediments, sludges, soils, and oils. Z Für Anal Chem 111:362–366

    Google Scholar 

  • Van Oosten MJ, Pepe O, De Pascale S, Silletti S, Maggio A (2017) The role of biostimulants and bioeffectors as alleviators of abiotic stress in crop plants. Chem Biol Technol Agric 4:5–12

    Google Scholar 

  • Villares R, Fernández-Lema E, López-Mosquera ME (2016) Evaluation of beach wrack for use as an organic fertilizer: temporal survey in different areas. Thalassas: Int J Mar Sci 32:19–36

    Google Scholar 

  • Vinod K, Awasthi G, Chauhan PK (2012) Cu and Zn tolerance and responses of the biochemical and physiochemical system of wheat. J Stress Physiol Biochem 53:1227–1236

    Google Scholar 

  • Yamamoto Y, Hachiya A, Matsumoto H (1997) Oxidative damage to membranes by a combination of aluminum and iron in suspension-cultured tobacco cells. Plant Cell Physiol 38:1333–1339

    CAS  Google Scholar 

  • Yruela I (2005) Copper in plants. Braz J Plant Physiol 17:145–156

    CAS  Google Scholar 

  • Zafar H, Ali A, Ali JS, Haq IU, Zia M (2016) Effect of ZnO nanoparticles on Brassica nigra seedlings and stem explants: growth dynamics and antioxidative response. Front Plant Sci 7:535

    PubMed  PubMed Central  Google Scholar 

  • Zhang X (1997) Influence of plant growth regulators on turfgrass growth, antioxidant status, and drought tolerance. PhD thesis, Virginia Tech

  • Zhang X, Ervin EH (2008) Impact of seaweed extract-based cytokinins and zeatin riboside on creeping bentgrass heat tolerance. Crop Sci 48:364–370

    Google Scholar 

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Funding

This research was funded by GreenUPorto (UIDB/05748/2020 and UIDP/05748/2020) and ValWrack (POCI-01-0145-FEDER-029818) and PestBiocide (PCIF/GVB/0150/2018) projects. CS, MM and BS also acknowledge Fundação para a Ciência e para a Tecnologia (FCT) for providing PhD scholarships (CS: SFRH/BD/115643/2016; MM: SFRH/BD/143268/2019; BS: 2020/07826/BD).

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FS, MM, CS, RP and FF—conceptualization; FS, MM, BS, CS, MA—investigation; FS, MM, CS, RP—formal analysis; FF and RP—resources; FS, MM, CS—writing-original draft; FS, MM, CS, BS, FF, RP—writing—review and editing; FF and RP—supervision.

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Correspondence to Filipa Sousa.

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Sousa, F., Martins, M., Sousa, B. et al. Wrack Composed by Fucus spp, Ascophyllum nodosum and Pelvetia canaliculata Limits Metal Uptake and Restores the Redox Homeostasis of Barley Plants Grown in Cu-Contaminated Soils. J Plant Growth Regul 41, 3544–3555 (2022). https://doi.org/10.1007/s00344-021-10532-x

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