Advertisement

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

  • Dragana Bosnić
  • Dragana Nikolić
  • Gordana Timotijević
  • Jelena Pavlović
  • Marek Vaculík
  • Jelena Samardžić
  • Miroslav NikolićEmail author
Regular Article
  • 106 Downloads

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.

Keywords

Cell wall SOD Copper toxicity Cucumber (Cucumis sativus L.) Plastocyanin Silicon 

Notes

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.

Supplementary material

11104_2019_4151_MOESM1_ESM.pdf (812 kb)
ESM 1 (PDF 811 kb)

References

  1. 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 283:15932–15945CrossRefGoogle Scholar
  2. Ainsworth EA, Gillespie KM (2007) Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin–Ciocalteu reagent. Nat Protoc 2:875–877CrossRefGoogle Scholar
  3. 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 38:262CrossRefGoogle Scholar
  4. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396CrossRefGoogle Scholar
  5. Bokor B, Vaculík M, Slováková L, Masarovič D, Lux A (2014) Silicon does not always mitigate zinc toxicity in maize. Acta Physiol Plant 36:733–743CrossRefGoogle Scholar
  6. 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 72:248–254CrossRefGoogle Scholar
  7. Burkhead JL, Reynolds KAG, Abdel-Ghany SE, Cohu CM, Pilon M (2009) Copper homeostasis. New Phytol 182:799–816CrossRefGoogle Scholar
  8. 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 36:745–754CrossRefGoogle Scholar
  9. 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 8:13–17Google Scholar
  10. 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 2:1336–1350CrossRefGoogle Scholar
  11. 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 187:22–30CrossRefGoogle Scholar
  12. 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 52:1101–1109CrossRefGoogle Scholar
  13. 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 63:2411–2420CrossRefGoogle Scholar
  14. 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 136:329–338CrossRefGoogle Scholar
  15. 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 158:266–273CrossRefGoogle Scholar
  16. Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. occurrence in higher plants. Plant Physiol 59:309–314CrossRefGoogle Scholar
  17. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930CrossRefGoogle Scholar
  18. Halliwell B, Gutteridge JM (1984) Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J 219:1–14CrossRefGoogle Scholar
  19. 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 56:244–253CrossRefGoogle Scholar
  20. 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 31:1046–1058CrossRefGoogle Scholar
  21. Haydon MJ, Cobbett CS (2007) Transporters of ligands for essential metal ions in plants. New Phytol 174:499–506CrossRefGoogle Scholar
  22. 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 207:604–611CrossRefGoogle Scholar
  23. Iwasaki K, Sakurai K, Takahashi E (1990) Copper binding by the root cell walls of Italian ryegrass and red clover. Soil Sci Plant Nutr 36:431–439CrossRefGoogle Scholar
  24. 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 241:847–860CrossRefGoogle Scholar
  25. Khandekar S, Leisner S (2011) Soluble silicon modulates expression of Arabidopsis thaliana genes involved in copper stress. J Plant Physiol 168:699–705CrossRefGoogle Scholar
  26. 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 14:13CrossRefGoogle Scholar
  27. Kliebenstein DJ, Monde R-A, Last RL (1998) Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiol 118:637–650CrossRefGoogle Scholar
  28. Kováčik J, Klejdus B (2008) Dynamics of phenolic acids and lignin accumulation in metal-treated Matricaria chamomilla roots. Plant Cell Rep 27:605–615CrossRefGoogle Scholar
  29. 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 151:702–714CrossRefGoogle Scholar
  30. 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 133:670–677CrossRefGoogle Scholar
  31. Liang Y, Nikolic M, Bélanger R, Gong H, Song A (2015) Silicon in agriculture. From theory to practice. Springer, DordrechtCrossRefGoogle Scholar
  32. 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 147:422–428CrossRefGoogle Scholar
  33. 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 4:531–539CrossRefGoogle Scholar
  34. 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 1–27Google Scholar
  35. 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 387:323–336CrossRefGoogle Scholar
  36. 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 167–178Google Scholar
  37. Marschner H (1995) Mineral nutrition of higher plants. Academic Press, LondonGoogle Scholar
  38. 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 178:74–83CrossRefGoogle Scholar
  39. Mitani N, Ma JF (2005) Uptake system of silicon in different plant species. J Exp Bot 414:1255–1261CrossRefGoogle Scholar
  40. 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: 360–376Google Scholar
  41. Nikolic N, Nikolic M (2012) Gradient analysis reveals a copper paradox on floodplain soils under long-term pollution by mining waste. Sci Total Environ 425:146–154CrossRefGoogle Scholar
  42. 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 143:495–503CrossRefGoogle Scholar
  43. Nowakowski W, Nowakowska J (1997) Silicon and copper interaction in the growth of spring wheat seedlings. Biol Plant 39:463–466CrossRefGoogle Scholar
  44. 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 13:591–596CrossRefGoogle Scholar
  45. 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 198:1096–1107CrossRefGoogle Scholar
  46. Peng H-Y, Yang X-E, Tian S-K (2005) Accumulation and ultrastructural distribution of copper in Elsholtzia splendens. J Zhejiang Univ Sci B 6:311–318CrossRefGoogle Scholar
  47. Pilon M, Ravet K, Tapken W (2011) The biogenesis and physiological function of chloroplast superoxide dismutases. Biochim Biophys Acta Bioenerg 1807:989–998CrossRefGoogle Scholar
  48. 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: 144–155Google Scholar
  49. Sharma SS, Dietz K-J (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14:43–50CrossRefGoogle Scholar
  50. 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 15:1333–1346CrossRefGoogle Scholar
  51. 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 344:319–333CrossRefGoogle Scholar
  52. 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 109:435–442CrossRefGoogle Scholar
  53. 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 122:641–648CrossRefGoogle Scholar
  54. 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 159:201–214CrossRefGoogle Scholar
  55. 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 110:433–443CrossRefGoogle Scholar
  56. 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 197:418–429CrossRefGoogle Scholar
  57. 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 23:815–825CrossRefGoogle Scholar
  58. Yruela I (2009) Copper in plants: acquisition, transport and interactions. Funct Plant Biol 36:409–430CrossRefGoogle Scholar
  59. 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 10:1188–1196CrossRefGoogle Scholar
  60. 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 22:3477–3488CrossRefGoogle Scholar
  61. 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 268:1–10CrossRefGoogle Scholar
  62. 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 167:527–533CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Laboratory for Plant Molecular Biology, Institute of Molecular Genetics and Genetic EngineeringUniversity of BelgradeBelgradeSerbia
  2. 2.Department of Plant Nutrition, Institute for Multidisciplinary ResearchUniversity of BelgradeBelgradeSerbia
  3. 3.Department of Plant Physiology, Faculty of Natural SciencesComenius University in BratislavaBratislavaSlovakia
  4. 4.Institute of Botany, Plant Science and Biodiversity CentreSlovak Academy of SciencesBratislavaSlovakia

Personalised recommendations