Abstract
Hydroponic experiments were conducted with rice seedlings (Oryza sativa L. cv. XZX45) exposed to gallium nitrate (Ga3+) to investigate the accumulation of Ga in plant tissues and phytotoxic responses. Results showed that phyto-transport of Ga was apparent, and roots were the dominant site for Ga accumulation. The total accumulation rates of Ga responded biphasically to Ga treatments by showing increases at low (1.06–8.52 mg Ga/L) and constants at high (8.52–15.63 mg Ga/L) concentrations, suggesting that accumulation kinetics of Ga followed a typical saturation curve. Higher amount of Ga accumulation in plant tissues led to significant inhibition in relative growth rate and water use efficiency in a dose-dependent manner. DNA-protein cross-links (DPCs) analysis revealed that overaccumulation of Ga in plant tissues positively stimulated formation of DPCs in roots. Likewise, the measure of root cell viability evaluated by Evan blue uptake showed a similar trend. These results suggested that Ga can be absorbed, transported, and accumulated in plant materials of rice seedlings. Overaccumulation of Ga in plant tissues provoked the formation of DPCs in roots, which resulted in cell death and growth inhibition of rice seedlings.
Similar content being viewed by others
References
Achery VMM, Jena S, Panda KK, Panda BB (2008) Aluminum induced oxidative stress and DNA damage in root cells of Allium cepa L. Ecotox Environ Safe 70:300–310
Babula P, Adam V, Opatrilova R, Zehnalek J, Havel L, Kizek R (2008) Uncommon heavy metals, metalloids and their toxicity: a review. Environ Chem Lett 6:189–213
Baker CJ, Mock NM (1994) An improved method for monitoring cell death in cell suspension and leaf disc assays using Evans blue. Plant Cell Tissue Org Cult 39:7–12
Banks MK, Schwab AP, Henderson C (2006) Leaching and reduction of chromium in soil as affected by soil organic content and plants. Chemosphere 62:255–264
Barker S, Weinfeld M, Murray D (2005) DNA-protein crosslinks: their induction, repair, and biological consequences. Mutat Res 589:111–135
Cai FY, Wang M, Wang J, Qin LJ, Yang X (2009) Oxidative damage of rat liver cells induced by DPB. J Pub Health Prev Med 20:4–7 (in Chinese)
Chakrabarti SK, Bai C, Subramanian KS (2001) DNA-protein rosslinks induced by nickel compounds in isolated rat lymphocytes: role of reactive oxygen species and specific amino acids. Toxicol Appl Pharmacol 170:153–165
Citterio S, Aina R, Labra M, Ghiani A, Fumagalli P, Sgorbati S, Santagostino A (2002) Soil genotoxicity: a new strategy based on biomolecular tools and plants bioindicators. Environ Sci Technol 36:2748–2753
Cuypers A, Smeets K, Ruytinx J, Opdenakker K, Keunen E, Remans T, Horemans N, Vanhoudt N, Van Sanden S, Van Belleghem F, Guisez Y, Colpaert J, Vangronsveld J (2011) The cellular redox state as a modulator in cadmium and copper responses in Arabidopsis thaliana seedlings. J Plant Physiol 168:309–316
Ebbs SD, Piccinin RC, Goodger JQD, Kolev SD, Woodrow IE, Baker AJM (2008) Transport of ferrocyanide by two eucalypt species and sorghum. Int J Phytorem 10:343–357
Eide D (1997) Molecular biology of iron and zinc uptake in eukaryotes. Curr Opin Cell Biol 9:573–577
Gichner T, Patkova Z, Szakova J, Demnerova K (2004) Cadmium induces DNA damage in tobacco roots, but no DNA damage, somatic mutations or homologous recombination in tobacco leaves. Mutat Res 559:49–57
Gichner T, Patkova Z, Szakova J, Znidar I, Mukherjee A (2008) DNA damage in potato plants induced by cadmium, ethyl methanesulphonate and γ-rays. Environ Exp Bot 62:113–1194
Harada E, Sugase K, Namba K, Iwashita T, Murata Y (2007) Structural element responsible for the Fe(III)–phytosiderophores specific transport by HvYS1 transporter in barley. FEBS Lett 581:4298–4302
Huang WX, Luo ZA, Yang F (2003) Study of Ga recovery from granulation slag. Rare Met Cem Carbides 31:8–11 (in Chinese)
Ide H, Shoulkamy MI, Nakano T, Miyamoto-Matsubara M, Salem AM (2011) Repair and biochemical effects of DNA-protein crosslinks. Mutat Res 711:113–122
Johnson GV, Barton LL (2007) Inhibition of iron deficiency stress response in cucumber by rare earth elements. Plant Physiol Biochem 45:302–308
Kim SA, Guerinot ML (2007) Mining iron: iron uptake and transport in plants. FEBS Lett 581:2273–2280
Kinraide TB, Yermiyahu U (2007) A scale of metal ion binding strengths correlating with ionic charge, Pauling electronegativity, toxicity, and other physiological effects. J Inorg Biochem 101:1201–1213
Koodkaew I, Sunohara Y, Matsuyama S, Matsumoto H (2012) Phytotoxic action mechanism of hapalocyclamide in lettuce seedlings. Plant Physiol Biochem 58:23–28
Kopittke PM, Mekenna BA, Blamey FPC, Wehr JB, Menzies NW (2009) Metal-induced cell rupture in elongating roots is associated with metal ion binding strengths. Plant Soil 322:303–315
Kragten J (1978) Atlas of metal-ligand equilibria in aqueous solution. John Wiley & Sons, New York
Kumar AK, Prasad MNV, Achary VMM, Panda BB (2013) Elucidation of lead-induced oxidative stress in Talinum triangulare roots by analysis of antioxidant responses and DNA damage at cellular level. Environ Sci Pollut Res 20:4551–4561
Kuykendall JR, Miller KL, Mellinger KN, Cain AV, Perry MW, Bradley M, Jarvi EJ, Paustenbach DJ (2009) DNA-protein cross-links in erythrocytes of freshwater fish exposed to hexavalent chromium or divalent nickel. Arch Environ Contam Toxicol 56:260–267
Liu JJ, Liu Y (2012) Determination of trace metal elements in water samples from Gansu-Ningxia-Inner Mongolia section of Yellow River by HR-ICP-MS. Sepctrosc Spectr Anal 32:331–332
Liu JG, Zhu QS, Zhang ZJ, Xu JK, Yang JC, Wong MH (2005) Variations in cadmium accumulation among rice cultivars and types and the selection of cultivars for reducing cadmium in the diet. J Sci Food Agric 85:147–153
Lockshin RA, Zakeri Z (2004) Apoptosis, autophagy, and more. Int J Biochem Cell Biol 36:2405–2419
Maluszynska J, Juchimiuk J (2005) Plant genotoxicity: a molecular cytogenetic approach in plant bioassays. Arh Hig Rada Toksikol 56:177–184
McCabe PF, Levine A, Meijer PJ, Tapon NA, Pennell RI (1997) A programmed cell death pathway activated in carrot cells cultured at low cell density. Plant J 12:267–280
Mino Y, Ishida T, Ota N, Inoue M, Nomoto K, Takemoto T, Tanaka H, Sugiura Y (1983) Mugineic acid-iron (III) complex and its structurally analogous cobalt (III) complex: characterization and implication for absorption and transport of iron in gramineous plants. J Am Chem Soc 105:4611–4676
Monteiro MS, Rodriguez E, Loureiro J, Mann RM, Soares AMVM, Santos C (2010) Flow cytometric assessment of Cd genotoxicity in three plants with different metal accumulation and detoxification capacities. Ecotox Environ Saf 73:1231–1237
Palta JP, Levitt J, Stadelmann EJ (1978) Plant viability assay. Cryobiology 15:249–255
Panda KK, Achary VMM, Krishnaveni R, Padhi BK, Sarangi SN, Sahu SN, Panda BB (2011) In vitro biosynthesis and genotoxicity bioassay of silver nanoparticles using plants. Tocxicol In Vitro 25:1097–1105
Petriccione M, Forte V, Valente D, Ciniglia C (2013) DNA integrity of onion root cells under catechol influence. Environ Sci Pollut Res 20:4859–4871
Reape TJ, McCabe PF (2008) Apoptotic-like programmed cell death in plants. New Phytol 180:13–26
Reid RJ, Rengel Z, Smith FA (1996) Membrane fluxes and comparative toxicities of aluminum, scandium and gallium. J Exp Bot 47:1881–1888
Ren JH, Ma L, Sun H, Cai F, Luo J (2014) Antimony uptake, translocation and speciation in rice plants exposed to antimonite and anal antimonate. Sci Tot Environ 475:83–89
Rodriguez E, Fernandes JP, Silva RA, Santos CL (2011) Cr(VI) induces DNA damage, cell cycle arrest and polyploidization: a flow cytometric and comet assay study in Pisum sativum. Chem Res Toxicol 24:1040–1047
Sachs L (1992) Angewandte statistik. Springer Verlag, Berlin
Shamberger RJ (1981) Selenium in the environment. Sci Tot Envrion 17:59–74
Shoulkamy MI, Nakano T, Ohshima M, Hirayama R, Uzawa A, Furusawa Y, Hiroshi I (2012) Detection of DNA-protein crosslinks (DPCs) by novel direct fluorescence labeling methods: distinct stabilities of aldehyde and radiation-induced DPCs. Nucleic Acids Res 40:e143
Smeets K, Opdenakker K, Remans T, Van Sanden S, Van Bellephem F, Semane B, Horemans N, Guisez Y, Vangronsveld J, Cuypers A (2009) Oxidative stress-related responses at transcriptional and enzymatic levels after exposure to Cd or Cu in a multipollution context. J Plant Physiol 166:1982–1992
Souguir D, Ferjani E, Ledoigt G, Goupil P (2008) Exposure of Vicia faba and Pisum sativum to copper-induced genotoxicity. Protoplasma 233:203–207
Tanaka A (2004) Toxicity of indium arsenide, gallium arsenide, and aluminium gallium arsenide. Toxicol Appl Pharm 198:405–411
Trapp S, McFarlane C, Matthies M (1994) Model for uptake of xenobiotics into plants: validation withbromacil experiments. Environ Toxicol Chem 13:413–422
Trapp S, Zambrano KC, Kusk KO, Karlson U (2000) A phytotoxicity test using transpiration of willows. Arch Environ Contam Toxicol 39:154–160
Türkoglu S (2007) Genotoxicity of five food preservatives tested on root tips of Allium cepa L. Mutat Res 626:4–14
Valverde M, Trejo C, Rojas E (2001) Is the capacity of leadacetate and cadmium chloride to induce genotoxic damagedue to direct DNA-metal interaction? Mutagenesis 16:265–270
Wang Q, An YL, Gy XX, Fu SH, Fy L, Yang HY (2010) Enrichment of the dispersed elements Cd, Ge and Ga in the Daliangzi lead-zinc deposit, Huidong Sichuan. Sediment Geol Techyan Geol 30:78–84 (in Chinese)
Wang CR, Zhang KG, He M, Jiang CJ, Tian LM, Tian Y, Wang XR (2012) Mineral nutrient imbalance, DNA lesion and DNA-protein crosslink involved in growth retardation of Vicia faba L seedlings exposed to lanthanum ions. J Environ Sci-China 24:214–220
Wheeler DM, Power IL (1995) Comparison of plant uptake and plant toxicity of various ions in wheat. Plant Soil 172:167–173
Yin SG, Chen HX, Luo XP (2006) Gallium resources application and the studying situation on separation and abstraction technology. Sichuan Nonferrous Metals 6:24–27 (in Chinese)
Yu XZ, Zhang FZ (2013) Effects of exogenous thiocyanate on mineral nutrients, antioxidative responses and free amino acids in rice seedlings. Ecotoxicology 22:752–760
Yu JB, Dong HF, Wang HB, Chen XB, Xie WJ, Mao PL, Gao YJ, Shan K, Chen JC, Ma XM (2011) Spatial distribution characteristics of metals in new-born coastal wetlands in the Yellow river Delta. Wetl Sci 9:297–304 (in Chinese)
Yu XZ, Zhang XH, Liu W (2014) Responses of free amino acids in rice seedlings during cyanide metabolism. Environ Sci Pollut Res 21:1411–1417
Zeng F, Zhou W, Qiu B, Ali S, Wu F, Zhang G (2011) Subcellular distribution and chemical forms of chromium in rice plants suffering from different levels of chromium toxicity. J Plant Nutr Soil Sci 174:249–256
Zhu YL, Zayed AM, Qian JH, Souza M, Terry N (1999) Phytoaccumulation of trace elements by wetland plants: II. Water hyacinth. J Environ Qual 28:339–344
Acknowledgments
This work was financially supported by the research foundations from Guilin University of Technology (Grant No.: GUTRC2011007) and The Guangxi Key Laboratory of Theory and Technology for Environmental Pollution Control (Grant No.: 1201Z029) and The Guangxi Talent Highland for Hazardous Waste Disposal Industrialization.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Elena Maestri
Rights and permissions
About this article
Cite this article
Yu, XZ., Zhang, XH. DNA-protein cross-links involved in growth inhibition of rice seedlings exposed to Ga. Environ Sci Pollut Res 22, 10830–10838 (2015). https://doi.org/10.1007/s11356-015-4305-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-015-4305-1