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Fullerenol can Ameliorate Iron Deficiency in Cucumber Grown Hydroponically

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Abstract

Among engineered nanomaterials designed for sustainable crop production, water-soluble fullerene derivatives offer unique properties with broad biological applications. In this paper, the role of fullerenol in amelioration of iron (Fe) deficiency (the most common and widespread nutrition disorder) in Cucumis sativus (a Strategy I plant) was investigated. Cucumber plants were grown hydroponically, either with [+FeII (ferrous) and +FeIII (ferric)] or in Fe-free (−FeII and −FeIII) nutrient solution, with (+ F) or without (−F) a fullerenol supply. Being higher in root apoplastic Fe, the –FeII plants became less chlorotic and were more tolerant to Fe deficiency, as compared with –FeIII plants. Although fullerenol did not affect the root apoplastic Fe in Fe-fed plants, it significantly lowered the root apoplastic Fe in –FeII-starved plants, in turn, increasing the leaf active-Fe concentration and successful suppression of plant Fe-deficiency symptoms. The ameliorative effect of fullerenol was accompanied by a significant increase in leaf fluorescence parameters: maximum efficiency (\(F_{{{\text{v}}^{{\prime }} }} /F_{{{\text{m}}^{{\prime }} }}\)) and electron transport rate (ETR), indicating that fullerenol addition activated reaction centres of PSII in the Fe-deprived plants. The results suggest for the first time that fullerenol can protect cucumber plants against Fe deficiency through increased utilisation of root apoplastic Fe.

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References

  • Abadía J, Monge E, Montañés L, Heras L (1984) Extraction of iron from plant leaves by Fe(II) chelators. J Plant Nutr 7(1–5):777–784

    Google Scholar 

  • Adamski JM, Danieloski R, Deuner S, Braga EJB, Castro LAS, José AP (2012) Responses to excess iron in sweet potato: impacts on growth, enzyme activities, mineral concentrations, and anatomy. Acta Physiol Plant 34:1827–1836

    CAS  Google Scholar 

  • Alloway BJ (2008) Micronutrients and crop production: an introduction. In: Alloway BJ (ed) Micronutrient deficiency in global crop production. Springer, Dordrecht, pp 1–39

    Google Scholar 

  • Arruda SCC, Silva ALD, Galazzi RM, Azevedo RA, Arruda MAZ (2015) Nanoparticles applied to plant science: a review. Talanta 131:693–705

    PubMed  Google Scholar 

  • Aschberger K, Johnston HJ, Stone V, Aitken RJ, Lang Tran C, Hankin SM, Peters SAK, Christensen FM (2010) Review of fullerene toxicity and exposure—appraisal of a human health risk assessment, based on open literature. Regul Toxicol Pharmacol 58:455–473

    CAS  PubMed  Google Scholar 

  • Balk J, Schaedler TA (2014) Iron cofactor assembly in plants. Ann Rev Plant Biol 65:125–153

    CAS  Google Scholar 

  • Bienfait HF, van den Briel W, Mesland-Mul NT (1985) Free space iron pools in roots. Generation and mobilization Plant Physiol 78:596–600

    CAS  PubMed  Google Scholar 

  • Bityutskii N, Pavlovic J, Yakkonen K, Maksimovic V, Nikolic M (2014) Contrasting effect of silicon on iron, zinc and manganese status and accumulation of metal-mobilizing compounds in micronutrient-deficient cucumber. Plant Physiol Biochem 74:205–211

    CAS  PubMed  Google Scholar 

  • Bityutskii NP, Yakkonen KL, Petrova AI, Shavarda AL (2017) Interactions between aluminium, iron and silicon in Cucumber sativus L. grown under acidic conditions. J Plant Physiol 218:100–108

    CAS  PubMed  Google Scholar 

  • Borišev M, Borišev I, Župunski M, Arsenov D, Pajević S, Živko C, Vasin J, Djordjevic A (2016) Drought impact is alleviated in sugar beets (Beta vulgaris L.) by foliar application of fullerenol nanoparticles. PLoS ONE 10:1–20

    Google Scholar 

  • Chaney RL, Brown JC, Tiffin LO (1972) Obligatory reduction of ferric chelates in iron uptake by soybeans. Plant Physiol 50:208–2013

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen R, Ratnikova TA, Stone MB, Lin S, Lard M, Huang G, Hudson JS, Ke PC (2010) Differential uptake of carbon nanoparticles by plant and mammalian cells. Small 6(5):612–617

    CAS  PubMed  Google Scholar 

  • Donnini S, De Nisi P, Gabotti D, Tato L, Zocchi G (2012) Adaptive strategies of Parietaria diffusa (M.&K.) to calcareous habitat with limited iron availability. Plant Cell Environ 35:1171–1184

    CAS  PubMed  Google Scholar 

  • Donnini S, Guidi L, Degl’Innocenti ZG (2013) Image changes in chlorophyll fluorescence in cucumber leaves in response to iron deficiency and resupply. J Plant Nutr Soil Sci 176:734–742

    CAS  Google Scholar 

  • Gao J, Wang Y, Folta KM, Krishna V, Bai W, Ingeglia P, Georgieva A, Nakamura H, Koopman B, Moudgil B (2011) Polyhydroxy fullerenes (PHFs or fullerenols): beneficial effects on growth and lifespan in diverse biological models. PLoS ONE 6(5):e19976

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guerinot ML (2001) Improving rice yields—ironing out the details. Nat Biotechnol 19:417–418

    CAS  PubMed  Google Scholar 

  • Guerinot ML (2010) Iron. In: Hell RI, Mendel RR (eds) Cell biology of metals and nutrients. Springer, Heidelberg, pp 75–94

    Google Scholar 

  • Hell R, Stephan UW (2003) Iron uptake, trafficking and homeostasis in plants. Planta 216:541–551

    CAS  PubMed  Google Scholar 

  • Husen A, Siddiqi KS (2014) Carbon and fullerne nanomaterials in plant system. J Nanobiotechnol 12:6

    Google Scholar 

  • Jeong J, Connoly EL (2009) Iron uptake mechanisms in plants: functions of the FRO family of ferric reductases. Plant Sci 176:709–714

    CAS  Google Scholar 

  • Jin CW, You GY, He YF, Tang C, Wu P, Zheng SJ (2007) Iron deficiency-induced secretion of phenolics facilitates the reutilization of root apoplastic iron in red clover. Plant Physiol 144:278–285

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kakhlon O, Cabantchik ZI (2002) The labile iron pool: characterization, measurement, and participation in cellular processes. Free Radic Biol Med 33(8):1037–1046

    CAS  PubMed  Google Scholar 

  • Khan MN, Mobin M, Abbas ZH, AlMutairi KA, Siddiqui ZH (2017) Role of nanomaterials in plants under challenging environments. Plant Physiol Biochem 110:194–209

    CAS  PubMed  Google Scholar 

  • Khodakovskaya M, Dervishi E, Mahmood M, Xu Y, Li Z, Watanabe F, Biris AS (2009) Carbon nanotubes are able to penetrate plant seed coat and dramatically affect seed germination and plant growth. ACS Nano 3(10):3221–3227

    CAS  PubMed  Google Scholar 

  • Khodakovskaya MV, de Silva K, Nedosekin DA, Dervishi E, Biris AS, Shashkov EV, Galanzha EI, Zharov VP (2011) Complex genetic, photothermal, and photoacoustic analysis of nanoparticle–plant interactions. Proc Natl Acad Sci USA 108(3):1028–1033

    CAS  PubMed  Google Scholar 

  • Khot LR, Sankaran S, Maja JM, Ehasni R, Schuster EW (2012) Applications of nanomaterials in agricultural production and crop protection: a review. Crop Prot 35:64–70

    CAS  Google Scholar 

  • Kole C, Kole P, Randunu KM, Choudhary P, Podila R, Ke PC, Ra AM, Marcus RK (2013) Nanobiotechnology can boost crop production and quality: first evidence from increased plant biomass, fruit yield and phytomedicine content in bitter melon (Momordica charantia). BMC Biotechnol 13:3

    Google Scholar 

  • Kroto HW, Heath JR, O’Brien SC, Curl RF, Smalley RE (1985) C60: buckminsterfullerene. Nature 318:162–163

    CAS  Google Scholar 

  • Li J, Takeuchi A, Ozawa M, Li X, Saigo K, Kitazawa K (1993) C60 fullerol formation catalysed by quaternary ammonium hydroxides. J Chem Soc Chem Commun 23:1784–1785

    Google Scholar 

  • Liang C, Xiao H, Hu Z, Zhang X, Hu J (2018) Uptake, transport, and accumulation of C60 fullerene and heavy metal ions (Cd, Cu, and Pb) in rice plants grown in an agricultural soil. Environ Pollu 235:330–338

    CAS  Google Scholar 

  • Lin S, Reppert J, Hu Q, Hudson JS, Reid ML, Ratnikova TA, Rao AM, Luo H, Ke PC (2009) Uptake, translocation, and transmission of carbon nanomaterials in rice plants. Small 5(10):1128–1132

    CAS  PubMed  Google Scholar 

  • López-Millán AF, Morales F, Gogorcena Y, Abadia A, Abadia J (2009) Metabolic responses in iron deficient tomato plants. J Plant Physiol 166:375–384

    PubMed  Google Scholar 

  • Lucena C, Romera FJ, Rojas CL, García MJ, Alcántara E, Pérez-Vicente R (2007) Bicarbonate blocks the expression of several genes involved in the physiological responses to Fe deficiency of strategy I plants. Funct Plant Biol 34:1002–1009

    CAS  PubMed  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, London

    Google Scholar 

  • Mchedlov-Petrossyan NO (2013) Fullerenes in liquid media: an unsettling intrusion into the solution chemistry. Chem Rev 113:5149–5193

    CAS  PubMed  Google Scholar 

  • Mengel K (1994) Iron availability in plant tissues—iron chlorosis on calcareous soils. Plant Soil 165:275–283

    CAS  Google Scholar 

  • Miralles P, Johnson E, Church TL, Harris AT (2014) Multiwalled carbon nanotubes in alfalfa and wheat: toxicology and uptake. J R Soc Interface 9:3514–3527

    Google Scholar 

  • Morales F, Belkhodja R, Abadia A, Abadia J (2000) Photosystem II efficiency and mechanisms of energy dissipation in iron-deficient, field grown pear trees (Pyrus communis L.). Phothosynth Res 63:9–21

    CAS  Google Scholar 

  • Panova GG, Ktitorova IN, Skobeleva OV, Sinjavina NG, Charykov NA, Semenov KN (2016) Impact of polyhydroxy fellerene (fullerol or fullerenol on growth and biophysical characteristics of barley seedlings in favourable and stressful conditions. Plant Growth Regul 79(3):309–317

    CAS  Google Scholar 

  • Partha R, Conyers JL (2009) Biomedical applications of functionalized fullerene-based nanomaterials. Int J Nanomed 4:261–275

    CAS  Google Scholar 

  • Pavlovic J, Samardzic J, Kostic L, Laursen KH, Natic M, Timotijevic G, Schjoerring JK, Nikolic M (2016) Silicon enhances leaf remobilization of iron in cucumber under limited iron conditions. Ann Bot 118:271–280

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pavlovic J, Samardzic J, Masimovic V, Timotijevic G, Stevic N, Laursen KH, Hansen TH, Husted S, Schjoerring JK, Liang Y, Nikolic M (2013) Silicon alleviates iron deficiency in cucumber by promoting mobilization of iron in the root apoplast. New Phytol 198:1096–1107

    CAS  PubMed  Google Scholar 

  • Podolsky NE, Marcos MA, Cabaleiro D, Semenov KN, Lugo L, Petrov AV, Charykov NA, Sharoyko VV, Vlasov TD, Murin IV (2019) Physico-chemical properties of C60(OH)22–24 water solutions: density, viscosity, refraction index, isobaric heat capacity and antioxidant activity. J Mol Liq 278:342–355

    CAS  Google Scholar 

  • Prylutska S, Bilyy R, Overchuk M, Bychko A, Andreichenko K, Stoika R, Rybalchenko V, Prylutskyy Yu, Tsierkezos NG, Ritter U (2012) Water-soluble pristine fullerenes C60 increase the specific conductivity and capacity of lipid model membrane and form the channels in cellular plasma membrane. J Biomed Nanotechnol 8:522–527

    CAS  PubMed  Google Scholar 

  • Robin A, Vansuyt G, Hinsinger P, Meyer JM, Briat JF, Lemanceau P (2008) Iron dynamics in the rhizosphere: consequences for plant health and nutrition. Adv Agron 99:183–225

    CAS  Google Scholar 

  • Römheld V, Marschner H (1986) Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiol 80:175–180

    PubMed  PubMed Central  Google Scholar 

  • Roosta HR, Estaji A, Niknam F (2018) Effect of iron, zinc and manganese shortage-induced change on photosynthetic pigments, some osmoregulators and chlorophyll fluorescence parameters in lettuce. Photosynthetica 56(2):606–615

    CAS  Google Scholar 

  • Santi S, Schmidt W (2009) Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. New Phytol 183:1072–1084

    CAS  PubMed  Google Scholar 

  • Schmidt W (2006) Iron stress responses in roots of strategy I plants. In: Barton LL, Abadia J (eds) Iron nutrition in plants and rhizospheric microorganisms. Springer, Dordrecht, pp 229–250

    Google Scholar 

  • Semenov KN, Andrusenko EV, Charykov NA, Litasova EV, Panova GG, Penkova AV, Murin IV, Piotrovskiy LB (2017) Carboxylated fullerenes: physico-chemical properties and potential applications. Progr Solid State Chem 47–48:19–36

    Google Scholar 

  • Semenov KN, Charykov NA, Keskinov VN (2011) Fullerenol synthesis and identification. Properties of the fullerenol water solutions. J Chem Eng Data 56:230–239

    CAS  Google Scholar 

  • Semenov KN, Charykov NA, Postnov VN, Sharoyko VV, Murin IV (2016) Phase equilibria in fullerene-containing systems as a basis for development of manufacture and application processes for nanocarbon materials. Russ Chem Rev 85:38–59

    CAS  Google Scholar 

  • Shen CX, Zhang QF, Li J, Bi FC, Yao N (2010) Induction of programmed cell death in Arabidopsis and rice by single-wall carbon nanotubes. Am J Bot 97(10):1602–1609

    CAS  PubMed  Google Scholar 

  • Singh S, Vishwakarma K, Singh S, Sharma S, Dubey NK, Singh VK, Liu S, Kumar D, Tripathi DK, Chauhan DK (2017) Understanding the plant and nanoparticle interface at transcriptomic and proteomic level: a concentric overview. Plant Gene 11:265–272

    CAS  Google Scholar 

  • Tiwari DK, Dasgupta-Schubert N, Villaseňor Cendejas N, Villegas J, Carreto Montoya L, Borjas García SE (2014) Interfacing carbon nanotubes (CNT) with plants: enhancement of growth, water and ionic nutrient uptake in maize (Zea mays) and implications for nanoagriculture. Appl Nanosci 5:577–591

    Google Scholar 

  • Vose PB (1982) Iron nutrition in plants: a world overview. J Plant Nutr 5:233–249

    CAS  Google Scholar 

  • Wang P, Lombi E, Zhao F-J, Kopittke P (2016) Nanotechnology: a new opportunity in plant sciences. Trends Plant Sci 21(8):699–712

    CAS  PubMed  Google Scholar 

  • Zaytseva O, Neumann G (2016) Carbon nanomaterials: production, impact on plant development, agricultural and environmental applications. Chem Biol Technol Agric 3:17

    Google Scholar 

  • Zhou P, Huo X, Zhang J, Liu Y, Cheng F, Cheng X, Wang Y, Zhang Y (2020) Visible light induced acceleration of Fe(III)/Fe(II) cycles for enhancing phthalate degradation in C60 fullerenol modified Fe(III)/peroxymonosulfate process. Chem Eng J 387:124126

    CAS  Google Scholar 

  • Zuverza-Mena N, Martínez-Fernández D, Du W, Hernandez-Viezcas JA, Bonilla-Bird N, López-Moreno ML, Komárek M, Peralta-Videa JR, Gardea-Torresd JL (2017) Exposure of engineered nanomaterials to plants: insights into the physiological and biochemical responses—a review. Plant Physiol Biochem 110:236–264

    CAS  PubMed  Google Scholar 

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Acknowledgements

We thank the Chemistry Educational Centre, and the Centre for Chemical Analysis and Materials Research of Saint Petersburg State University, for technical assistance.

Funding

This work was funded by the Russian Foundation for Basic Research [grant number 19–016-00003a].

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Authors and Affiliations

  1. Department of Agricultural Chemistry, Saint Petersburg State University, 7/9 Universitetskaya nab., Saint Petersburg, Russia, 199034

    Nikolai P. Bityutskii, Kirill L. Yakkonen & Kseniia A. Lukina

  2. First Pavlov State Medical University, 6-8 L’va Tolstogo ulitsa, Saint Petersburg, Russia, 197022

    Konstantin N. Semenov

  3. Agrophysical Research Institute, Grazhdansky pr. 14, Saint Petersburg, Russia, 195220

    Gayane G. Panova

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  1. Nikolai P. Bityutskii
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  2. Kirill L. Yakkonen
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Bityutskii, N.P., Yakkonen, K.L., Lukina, K.A. et al. Fullerenol can Ameliorate Iron Deficiency in Cucumber Grown Hydroponically. J Plant Growth Regul 40, 1017–1031 (2021). https://doi.org/10.1007/s00344-020-10160-x

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