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Silicon alleviates copper (Cu) toxicity in cucumber by increased Cu-binding capacity

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Abstract

Aims

Although silicon (Si) is known to increase plant resistance to metal toxicity stress, the mechanisms responsible for alleviation of copper (Cu) toxicity are still insufficiently clear. We investigated the role of Si on Cu-binding processes involved in buffering excessive Cu in cucumber (Cucumis sativus L.) tissues.

Methods

Cucumber plants were subjected to moderate Cu toxicity stress (10 μM Cu) without (−Si) or with (+Si) supply of 1.5 mM Si. We analyzed total and cell wall concentrations of Cu and Cu-binding compounds (organic acids and Cu-proteins) along with parameters of oxidative stress (e.g. lipid peroxidation and lignification).

Results

Supply of Si decreased total Cu concentration in both root and leaf tissues, but increased the root cell wall Cu fraction. Also, Si increased superoxide dismutase (SOD) activity in 10 μM Cu-treated plants. Concomitantly, protein levels of Cu/Zn SOD isoforms (CSD1 and CSD2) in root tissues also increased in +Si plants. The leaf Cu-binding compounds, such as aconitate and plastocyanin (including the expression of CsPC gene) were higher in the +Si plants. Consequently, Si supply effectively lowered lipid peroxidation in both roots and leaves of Cu-stressed plants.

Conclusions

Supply of Si enhanced both the accumulation of Cu-binding molecules (Zn/Cu SOD in roots; aconitate and plastocyanin in leaves), and the Cu-binding capacity of the root cell wall.

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References

  • Abdel-Ghany SE, Pilon M (2008) MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. J Biol Chem 283:15932–15945

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ainsworth EA, Gillespie KM (2007) Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin–Ciocalteu reagent. Nat Protoc 2:875–877

    Article  CAS  PubMed  Google Scholar 

  • Ali S, Rizwan M, Ullah N, Bharwana SA, Waseem M, Farooq MA, Abbasi GH, Farid M (2016) Physiological and biochemical mechanisms of silicon-induced copper stress tolerance in cotton (Gossypium hirsutum L.). Acta Physiol Plant 38:262

    Article  CAS  Google Scholar 

  • Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bokor B, Vaculík M, Slováková L, Masarovič D, Lux A (2014) Silicon does not always mitigate zinc toxicity in maize. Acta Physiol Plant 36:733–743

    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 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Burkhead JL, Reynolds KAG, Abdel-Ghany SE, Cohu CM, Pilon M (2009) Copper homeostasis. New Phytol 182:799–816

    Article  CAS  PubMed  Google Scholar 

  • Chai M, Shi F, Li R, Qiu G, Liu F, Liu L (2014) Growth and physiological responses to copper stress in a halophyte Spartina alterniflora (Poaceae). Acta Physiol Plant 36:745–754

    Article  CAS  Google Scholar 

  • Choi SM, Suh KH, Kim J-S, Park Y-I (2001) Inactivation of photosystem I in cucumber leaves exposed to paraquat-induced oxidative stress. J Photosci 8:13–17

    CAS  Google Scholar 

  • Cohu CM, Abdel-Ghany SE, Gogolin Reynolds KA, Onofrio AM, Bodecker JR, Kimbrel JA, Niyogi KK, Pilon M (2009) Copper delivery by the copper chaperone for chloroplast and cytosolic copper/zinc-superoxide dismutases: regulation and unexpected phenotypes in an Arabidopsis mutant. Mol Plant 2:1336–1350

    Article  CAS  PubMed  Google Scholar 

  • Collin B, Doelsch E, Keller C, Cazevieille P, Tella M, Chaurand P, Panfili F, Hazemann J-L, Meunier J-D (2014) Evidence of sulfur-bound reduced copper in bamboo exposed to high silicon and copper concentrations. Environ Pollut 187:22–30

    Article  CAS  PubMed  Google Scholar 

  • Dixit V, Pandey V, Shyam R (2001) Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv. Azad). J Exp Bot 52:1101–1109

    Article  CAS  PubMed  Google Scholar 

  • Dragišić Maksimović J, Mojović M, Maksimović V, Römheld V, Nikolic M (2012) Silicon ameliorates manganese toxicity in cucumber by decreasing hydroxyl radical accumulation in the leaf apoplast. J Exp Bot 63:2411–2420

    Article  CAS  PubMed  Google Scholar 

  • Frantz JM, Khandekar S, Leisner S (2011) Silicon differentially influences copper toxicity response in silicon-accumulator and non-accumulator species. J Am Soc Hortic Sci 136:329–338

    Article  CAS  Google Scholar 

  • Geng A, Wang X, Wu L, Wang F, Wu Z, Yang H, Chen Y, Wen D, Liu X (2018) Silicon improves growth and alleviates oxidative stress in rice seedlings (Oryza sativa L.) by strengthening antioxidant defense and enhancing protein metabolism under arsanilic acid exposure. Ecotoxicol Environ Saf 158:266–273

    Article  CAS  PubMed  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. occurrence in higher plants. Plant Physiol 59:309–314

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • Halliwell B, Gutteridge JM (1984) Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J 219:1–14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hashemi A, Abdolzadeh A, Sadeghipour HR (2010) Beneficial effects of silicon nutrition in alleviating salinity stress in hydroponically grown canola, Brassica napus L., plants. Soil Sci Plant Nutr 56:244–253

    Article  CAS  Google Scholar 

  • Hattori T, Sonobe K, Inanaga S, An P, Morita S (2008) Effects of silicon on photosynthesis of young cucumber seedlings under osmotic stress. J Plant Nutr 31:1046–1058

    Article  CAS  Google Scholar 

  • Haydon MJ, Cobbett CS (2007) Transporters of ligands for essential metal ions in plants. New Phytol 174:499–506

    Article  CAS  PubMed  Google Scholar 

  • Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611

    Article  CAS  Google Scholar 

  • Iwasaki K, Sakurai K, Takahashi E (1990) Copper binding by the root cell walls of Italian ryegrass and red clover. Soil Sci Plant Nutr 36:431–439

    Article  Google Scholar 

  • Keller C, Rizwan M, Davidian J-C, Pokrovsky OS, Bovet N, Chaurand P, Meunier J-D (2015) Effect of silicon on wheat seedlings (Triticum turgidum L.) grown in hydroponics and exposed to 0 to 30 μM cu. Planta 241:847–860

    Article  CAS  PubMed  Google Scholar 

  • Khandekar S, Leisner S (2011) Soluble silicon modulates expression of Arabidopsis thaliana genes involved in copper stress. J Plant Physiol 168:699–705

    Article  CAS  PubMed  Google Scholar 

  • Kim Y-H, Khan AL, Kim D-H, Lee S-Y, Kim K-M, Waqas M, Jung H-Y, Shin J-H, Kim J-G, Lee I-J (2014) Silicon mitigates heavy metal stress by regulating P-type heavy metal ATPases, Oryza sativa low silicon genes, and endogenous phytohormones. BMC Plant Biol 14:13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kliebenstein DJ, Monde R-A, Last RL (1998) Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiol 118:637–650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kováčik J, Klejdus B (2008) Dynamics of phenolic acids and lignin accumulation in metal-treated Matricaria chamomilla roots. Plant Cell Rep 27:605–615

    Article  CAS  PubMed  Google Scholar 

  • Küpper H, Götz B, Mijovilovich A, Küpper FC, Meyer-Klaucke W (2009) Complexation and toxicity of copper in higher plants. I. Characterization of copper accumulation, speciation, and toxicity in Crassula helmsii as a new copper accumulator. Plant Physiol 151:702–714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Leisner SM, Frantz J (2008) Alleviation of copper toxicity in Arabidopsis thaliana by silicon addition to hydroponic solutions. J Am Soc Hortic Sci 133:670–677

    Article  Google Scholar 

  • Liang Y, Nikolic M, Bélanger R, Gong H, Song A (2015) Silicon in agriculture. From theory to practice. Springer, Dordrecht

    Google Scholar 

  • Liang Y, Sun W, Zhu Y-G, Christie P (2007) Mechanisms of silicon-mediated alleviation of abiotic stresses in higher plants: a review. Environ Pollut 147:422–428

    Article  CAS  PubMed  Google Scholar 

  • Lin J-T, Liu S-C, Shen Y-C, Yang D-J (2011) Comparison of various preparation methods for determination of organic acids in fruit vinegars with a simple ion-exclusion liquid chromatography. Food Anal Methods 4:531–539

    Article  Google Scholar 

  • Líška D, Soukup M, Lukačová Z, Bokor B, Vaculík M (2017) Mechanisms of silicon-mediated alleviation of abiotic stress in plants: recent advances and future perspective. In: Tripathi D, Singh V, Ahmad P, Chauhan D, Prasad S (eds) Silicon in plants: advances and future prospects. CRC Press, Taylor & Francis, Boca Raton, pp 1–27

    Google Scholar 

  • Liu Q, Zheng L, He F, Zhao F-J, Shen Z, Zheng L (2015) Transcriptional and physiological analyses identify a regulatory role for hydrogen peroxide in the lignin biosynthesis of copper-stressed rice roots. Plant Soil 387:323–336

    Article  CAS  Google Scholar 

  • Lux A, Vaculík M, Kováč J (2015) Improved methods for clearing and staining of plant samples. In: Yeung E, Stasolla C, Sumner M, Huang B (eds) Plant microtechniques and protocols. Springer, pp 167–178

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

    Google Scholar 

  • Mateos-Naranjo E, Gallé A, Florez-Sarasa I, Perdomo JA, Galmés J, Ribas-Carbó M, Flexas J (2015) Assessment of the role of silicon in the cu-tolerance of the C4 grass Spartina densiflora. J Plant Physiol 178:74–83

    Article  CAS  PubMed  Google Scholar 

  • Mitani N, Ma JF (2005) Uptake system of silicon in different plant species. J Exp Bot 414:1255–1261

    Article  CAS  Google Scholar 

  • Moura JCMS, Bonine CAV, de Oliveira Fernandes Viana J, Dornelas MC, Mazzafera P (2010) Abiotic and biotic stresses and changes in the lignin content and composition in plants. J Integr Plant Biol 52: 360–376

  • Nikolic N, Nikolic M (2012) Gradient analysis reveals a copper paradox on floodplain soils under long-term pollution by mining waste. Sci Total Environ 425:146–154

    Article  CAS  PubMed  Google Scholar 

  • Nikolic M, Nikolic N, Liang Y, Kirkby EA, Römheld V (2007) Germanium-68 as an adequate tracer for silicon transport in plants. Characterization of silicon uptake in different crop species. Plant Physiol 143:495–503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nowakowski W, Nowakowska J (1997) Silicon and copper interaction in the growth of spring wheat seedlings. Biol Plant 39:463–466

    Article  CAS  Google Scholar 

  • Oliva SR, Mingorance MD, Leidi EO (2011) Effects of silicon on copper toxicity in Erica andevalensis Cabezudo and Rivera: a potential species to remediate contaminated soils. J Environ Monit 13:591–596

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Peng H-Y, Yang X-E, Tian S-K (2005) Accumulation and ultrastructural distribution of copper in Elsholtzia splendens. J Zhejiang Univ Sci B 6:311–318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pilon M, Ravet K, Tapken W (2011) The biogenesis and physiological function of chloroplast superoxide dismutases. Biochim Biophys Acta Bioenerg 1807:989–998

    Article  CAS  Google Scholar 

  • Sagasti S, Bernal M, Sancho D, B. del Castillo M, Picorel R (2014) Regulation of the chloroplastic copper chaperone (CCS) and cuprozinc superoxide dismutase (CSD2) by alternative splicing and copper excess in Glycine max. Funct Plant Biol 41: 144–155

  • Sharma SS, Dietz K-J (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14:43–50

    Article  CAS  PubMed  Google Scholar 

  • Shikanai T, Müller-Moulé P, Munekage Y, Niyogi KK, Pilon M (2003) PAA1, a P-type ATPase of Arabidopsis, functions in copper transport in chloroplasts. Plant Cell 15:1333–1346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song A, Li P, Li Z, Fan F, Nikolic M, Liang Y (2011) The alleviation of zinc toxicity by silicon is related to zinc transport and antioxidative reactions in rice. Plant Soil 344:319–333

    Article  CAS  Google Scholar 

  • Sreenivasulu N, Grimm B, Wobus U, Weschke W (2001) Differential response of antioxidant compounds to salinity stress in salt-tolerant and salt-sensitive seedlings of foxtail millet (Setaria italica). Physiol Plant 109:435–442

    Article  Google Scholar 

  • Sun H, Duan Y, Qi X, Zhang L, Huo H, Gong H (2018) Isolation and functional characterization of CsLsi2, a cucumber silicon efflux transporter gene. Ann Bot 122:641–648

    Article  PubMed  PubMed Central  Google Scholar 

  • Sun H, Guo J, Duan Y, Zhang T, Huo H, Gong H (2017) Isolation and functional characterization of CsLsi1, a silicon transporter gene in Cucumis sativus. Physiol Plant 159:201–214

    Article  CAS  PubMed  Google Scholar 

  • Vaculík M, Landberg T, Greger M, Luxová M, Stoláriková M, Lux A (2012) Silicon modifies root anatomy, and uptake and subcellular distribution of cadmium in young maize plants. Ann Bot 110:433–443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S-H, Zhang H, Zhang Q, Jin G-M, Jiang S-J, Jiang D, He Q-Y, Li Z-P (2011) Copper-induced oxidative stress and responses of the antioxidant system in roots of Medicago sativa. J Agron Crop Sci 197:418–429

    Article  CAS  Google Scholar 

  • Wu J-W, Shi Y, Zhu Y-X, Wang Y-C, Gong H-J (2013) Mechanisms of enhanced heavy metal tolerance in plants by silicon: a review. Pedosphere 23:815–825

    Article  CAS  Google Scholar 

  • Yruela I (2009) Copper in plants: acquisition, transport and interactions. Funct Plant Biol 36:409–430

    Article  CAS  PubMed  Google Scholar 

  • Zeng F, Zhao F, Qiu B, Ouyang Y, Wu F, Zhang G (2011) Alleviation of chromium toxicity by silicon addition in rice pants. Agric Sci China 10:1188–1196

    Article  CAS  Google Scholar 

  • Zhang Y, Du N, Wang L, Zhang H, Zhao J, Sun G, Wang P (2015) Physical and chemical indices of cucumber seedling leaves under dibutyl phthalate stress. Environ Sci Pollut Res 22:3477–3488

    Article  CAS  Google Scholar 

  • Zhou X-T, Wang F, Ma Y-P, Jia L-J, Liu N, Wang H-Y, Zhao P, Xia G-X, Zhong N-Q (2018) Ectopic expression of SsPETE2, a plastocyanin from Suaeda salsa, improves plant tolerance to oxidative stress. Plant Sci 268:1–10

    Article  CAS  PubMed  Google Scholar 

  • Zhu Z, Wei G, Li J, Qian Q, Yu J (2004) Silicon alleviates salt stress and increases antioxidant enzymes activity in leaves of salt-stressed cucumber (Cucumis sativus L.). Plant Sci 167:527–533

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by the Serbian Ministry of Education, Science and Technological Development (ON-173005 and ON-173028) and in part by the grant of bilateral scientific cooperation between Serbia and Slovakia SK-SRB-2013-0021 (451-03-545/2015-09/02). We thank Dr. Nina Nikolic (University of Belgrade, Serbia) for critical reading of the manuscript.

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Authors and Affiliations

  1. Laboratory for Plant Molecular Biology, Institute of Molecular Genetics and Genetic Engineering, University of Belgrade, Belgrade, Serbia

    Dragana Bosnić, Dragana Nikolić, Gordana Timotijević & Jelena Samardžić

  2. Department of Plant Nutrition, Institute for Multidisciplinary Research, University of Belgrade, Belgrade, Serbia

    Jelena Pavlović & Miroslav Nikolić

  3. Department of Plant Physiology, Faculty of Natural Sciences, Comenius University in Bratislava, Bratislava, Slovakia

    Marek Vaculík

  4. Institute of Botany, Plant Science and Biodiversity Centre, Slovak Academy of Sciences, Bratislava, Slovakia

    Marek Vaculík

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  1. Dragana Bosnić
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  2. Dragana Nikolić
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  3. Gordana Timotijević
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  4. Jelena Pavlović
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  5. Marek Vaculík
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  6. Jelena Samardžić
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  7. Miroslav Nikolić
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Correspondence to Miroslav Nikolić.

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Bosnić, D., Nikolić, D., Timotijević, G. et al. Silicon alleviates copper (Cu) toxicity in cucumber by increased Cu-binding capacity. Plant Soil 441, 629–641 (2019). https://doi.org/10.1007/s11104-019-04151-5

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