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Effects of copper deficiency and copper toxicity on organogenesis and some physiological and biochemical responses of Scots pine (Pinus sylvestris L.) seedlings grown in hydroculture

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Abstract

The morphological, physiological, and biochemical parameters of 6-week-old seedlings of Scots pine (Pinus sylvestris L.) were studied under deficiency (1.2 nM) and chronic exposure to copper (0.32, 1, 2.5, 5, and 10 μM CuSO4) in hydroculture. The deposit of copper in the seed allowed the seedlings to develop under copper deficiency without visible disruption of growth. The high sensitivity of Scots pine to the toxic effects of copper was shown, which manifested as a significant inhibition of growth and development. The loss of dominance of the main root and a strong inhibition of lateral root development pointed to a lack of adaptive reorganization of the root system architecture under copper excess. A preferential accumulation of copper in the root and a minor translocation in aerial organs confirmed that Scots pine belongs to a group of plants that exclude copper. Selective impairment in the absorption of manganese was discovered, under both deficiency and excess of copper in the nutrient solution, which was independent of the degree of development of the root system. Following 10 μM CuSO4 exposure, the absorption of manganese and iron from the nutrient solution was completely suppressed, and the development of seedlings was secured by the stock of these micronutrients in the seed. The absence of signs of oxidative stress in the seedling organs was shown under deficiency and excess of copper, as evidenced by the steady content of malondialdehyde and 4-hydroxyalkenals. Against this background, no changes in total superoxide dismutase activity in the organs of seedlings were revealed, and the increased content of low-molecular-weight antioxidants was observed in the roots under 1 μM and in the needles under 5 μM CuSO4 exposures.

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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. doi:10.1074/jbc.M801406200

    Article  CAS  Google Scholar 

  • Adriaensen K, VrÃ¥lstad T, Noben JP, Vangronsveld J, Colpaert JV (2005) Copper-adapted Suillus luteus, a symbiotic solution for pines colonizing Cu mine spoils. Appl Environ Microb 71:7279–7284. doi:10.1128/AEM.71.11.7279-7284.2005

    Article  CAS  Google Scholar 

  • Arduini I, Godbold DL, Onnis A (1995) Influence of copper on root growth and morphology of Pinus pinea L. and Pinus pinaster Ait. seedlings. Tree Physiol 15:411–415. doi:10.1093/treephys/15.6.411

    Article  CAS  Google Scholar 

  • Chen Y, Nara K, Wen Z, Shi L, Xia Y, Shen Z, Lian C (2015) Growth and photosynthetic responses of ectomycorrhizal pine seedlings exposed to elevated Cu in soils. Mycorrhiza 25:561–571. doi:10.1007/s00572-015-0629-4

    Article  CAS  Google Scholar 

  • Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101. doi:10.1093/jxb/32.1.93

    Article  CAS  Google Scholar 

  • Gérard-Monnier D, Erdelmeier I, Régnard K, Moze-Henry N, Yadan JC, Chaudière J (1998) Reactions of 1-methyl-2-phenylindole with malondialdehyde and 4-hydroxyalkenals. Analytical applications to a colorimetric assay of lipid peroxidation. Chem Res Toxicol 11:1176–1183. doi:10.1021/tx9701790

    Article  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. doi:10.1016/0003-9861(68)90654-1

    Article  CAS  Google Scholar 

  • Irving HM, Williams RJP (1953) The stability of transition-metal complexes. J Chem Soc 637:3192–3210, Resumed

    Article  Google Scholar 

  • Ivanov YV, Savochkin YV, Shumeiko EV, Kuznetsov VV (2013a) Implementation of Scots pine’s early ontogenetic stage against copper toxic effect. Tomsk State Univ. J Biol 21:103–117, In Russian, English Summary

  • Ivanov YV, Savochkin YV, Kuznetsov VV (2013b) Effect of mineral composition and medium pH on Scots pine tolerance to toxic effect of zinc ions. Russ. J Plant Physl 60:260–269. doi:10.1134/S102144371302009X

  • Ivanov VP, Marchenko SI, Nartov DI, Ivanov YV (2015) Growth status of Scots pine artificial stands under the influence of para-aminobenzoic acid. Contemp Probl Ecol 8:133–140. doi:10.1134/S1995425515010059

    Article  Google Scholar 

  • Ivanov YV, Kartashov AV, Ivanova AI, Savochkin YV, Kuznetsov VV (2016) Effects of zinc on Scots pine (Pinus sylvestris L.) seedlings grown in hydroculture. Plant Physiol Bioch 102:1–9. doi:10.1016/j.plaphy.2016.02.014

    Article  CAS  Google Scholar 

  • Johnston JW, Horne S, Harding K, Benson EE (2007) Evaluation of the 1-methyl-2-phenylindole colorimetric assay for aldehydic lipid peroxidation products in plants: malondialdehyde and 4-hydroxynonenal. Plant Physiol Bioch 45:108–112. doi:10.1016/j.plaphy.2007.01.011

    Article  CAS  Google Scholar 

  • Jungqvist G, Oni SK, Teutschbein C, Futter MN (2014) Effect of climate change on soil temperature in Swedish boreal forests. PLoS One 9:e93957. doi:10.1371/journal.pone.0093957

    Article  Google Scholar 

  • Kahle H (1993) Response of roots of trees to heavy metals. Environ Exp Bot 33:99–119. doi:10.1016/0098-8472(93)90059-O

    Article  Google Scholar 

  • Koh YH, Yoon SJ, Park JW (1999) Inactivation of copper, zinc superoxide dismutase by the lipid peroxidation products malondialdehyde and 4-hydroxynonenal. BMB Rep 32:440–444

    CAS  Google Scholar 

  • Kozlov MV, Zvereva EI (2007) Industrial barrens: extreme habitats created by non-ferrous metallurgy. Rev Environ Sci Biotechnol 6:231–259. doi:10.1007/978-1-4020-6285-8_5

    Article  CAS  Google Scholar 

  • Kukkola E, Rautio P, Huttunen S (2000) Stress indications in copper-and nickel-exposed Scots pine seedlings. Environ Exp Bot 43:197–210. doi:10.1016/S0098-8472(99)00057-X

    Article  CAS  Google Scholar 

  • Kupper H, Andresen E (2016) Mechanisms of metal toxicity in plants. Metallomics 8:269–285. doi:10.1039/C5MT00244C

    Article  Google Scholar 

  • Lequeux H, Hermans C, Lutts S, Verbruggen N (2010) Response to copper excess in Arabidopsis thaliana: impact on the root system architecture, hormone distribution, lignin accumulation and mineral profile. Plant Physiol Bioch 48:673–682. doi:10.1016/j.plaphy.2010.05.005

    Article  CAS  Google Scholar 

  • Mineral commodity summaries (2015) Mineral Commodities Summaries/U.S. Geological Survey. Report. p 196, 1 Appendix. DOI: 10.3133/70140094

  • Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216. doi:10.1007/s10311-010-0297-8

    Article  CAS  Google Scholar 

  • Nieminen TM (2004) Effects of soil copper and nickel on survival and growth of Scots pine. J Environ Monitor 6:888–896. doi:10.1039/B405958C

    Article  CAS  Google Scholar 

  • Patsikka E, Kairavuo M, Sersen F, Aro EM, Tyystjarvi E (2002) Excess copper predisposes photosystem II to photoinhibition in vivo by outcompeting iron and causing decrease in leaf chlorophyll. Plant Physiol 129:1359–1367. doi:10.1104/pp.004788

    Article  CAS  Google Scholar 

  • Pietrzykowski M, Socha J, van Doorn NS (2014) Linking heavy metal bioavailability (Cd, Cu, Zn and Pb) in Scots pine needles to soil properties in reclaimed mine areas. Sci Total Environ 470:501–510. doi:10.1016/j.scitotenv.2013.10.008

    Article  Google Scholar 

  • Rautio P, Kukkola E, Huttunen S (2004) Alterations in the nutrient status of Scots pine seedlings grown in copper-and nickel-treated soil. J Appl Bot 78:48–57

    CAS  Google Scholar 

  • Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Bio Med 26:1231–1237. doi:10.1016/S0891-5849(98)00315-3

    Article  CAS  Google Scholar 

  • Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot. doi:10.1155/2012/217037

    Google Scholar 

  • Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Viticult 16:144–158

    CAS  Google Scholar 

  • Sukhareva TA, Lukina NV (2014) Mineral composition of assimilative organs of conifers after reduction of atmospheric pollution in the Kola Peninsula. Russ J Ecol 45:95–102. doi:10.1134/S1067413614020088

    Article  CAS  Google Scholar 

  • Sun B, Ricardo-da-Silva JM, Spranger I (1998) Critical factors of vanillin assay for catechins and proanthocyanidins. J Agr Food Chem 46:4267–4274. doi:10.1021/jf980366j

    Article  CAS  Google Scholar 

  • Sytar O, Kumar A, Latowski D, Kuczynska P, StrzaÅ‚ka K, Prasad MNV (2013) Heavy metal-induced oxidative damage, defense reactions, and detoxification mechanisms in plants. Acta Physiol Plant 35:985–999. doi:10.1007/s11738-012-1169-6

    Article  CAS  Google Scholar 

  • Taulavuori E, Hellstrom E-K, Taulavuori K, Laine K (2001) Comparison of two methods used to analyse lipid peroxidation from Vaccinium myrtillus (L.) during snow removal, reacclimation and cold acclimation. J Exp Bot 52:2375–2380. doi:10.1093/jexbot/52.365.2375

    Article  CAS  Google Scholar 

  • Van Tichelen KK, Vanstraelen T, Colpaert JV (1999) Nutrient uptake by intact mycorrhizal Pinus sylvestris seedlings: a diagnostic tool to detect copper toxicity. Tree Physiol 19:189–196. doi:10.1093/treephys/19.3.189

    Article  Google Scholar 

  • Wingsle G, Gardeström P, Hällgren JE, Karpinski S (1991) Isolation, purification, and subcellular localization of isozymes of superoxide dismutase from Scots pine (Pinus sylvestris L.) needles. Plant Physiol 95:21–28. doi:10.1104/pp.95.1.21

    Article  CAS  Google Scholar 

  • Yruela I (2009) Copper in plants: acquisition, transport and interactions. Funct Plant Biol 36:409–430. doi:10.1071/FP08288

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Tatiana V. Litonova, an engineer of the Laboratory of Physiological and Molecular Mechanisms of Adaptation, Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, for the technical assistance.

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Correspondence to Yury V. Ivanov.

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This work was supported by the Russian Foundation for Basic Research (projects Nos. 12-04-01715-a and 16-34-01269-mol_a) and by the Presidium of the Russian Academy of Sciences (Molecular and Cellular Biology Program).

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Responsible editor: Elena Maestri

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Ivanov, Y.V., Kartashov, A.V., Ivanova, A.I. et al. Effects of copper deficiency and copper toxicity on organogenesis and some physiological and biochemical responses of Scots pine (Pinus sylvestris L.) seedlings grown in hydroculture. Environ Sci Pollut Res 23, 17332–17344 (2016). https://doi.org/10.1007/s11356-016-6929-1

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  • DOI: https://doi.org/10.1007/s11356-016-6929-1

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