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Concentration-dependent alterations in gene expression induced by cadmium in Solanum lycopersicum

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Abstract

Cadmium (Cd) toxicity in agricultural soil has received significant attention because of its higher transformation in the food chain and toxicity to humans. The aim of the present study was to develop sensitive and specific biomarkers for Cd stress. Therefore, transcriptional analyses were performed to investigate concentration-response characteristics of Cd responsive genes identified from a Solanum lycopersicum microarray. The results showed that the lowest observable adverse effect concentrations (LOAECs) of Cd to S. lycopersicum were 1 mg/kg for seed germination, 8 mg/kg for root dry weight, 8 mg/kg for root elongation, and 8 mg/kg for root morphology. Furthermore, the genes were differentially expressed even at the lowest Cd concentrations (0.5 mg/kg), indicating that the detection of Cd in soil at the molecular level is a highly sensitive method. Cd in soil was positively correlated with the expression of the F-box protein PP2-B15 (r = 0.809, p < 0.01) and zinc transporter 4 (r = 0.643, p < 0.01), indicating that these two genes could be selected as indicators of soil Cd contamination.

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References

  • Alhelal AA (1995) Effect of cadmium and mercury on seed-germination and early seedling growth of rice and alfalfa. Journal of the University of Kuwait-Science 22:76–83

    CAS  Google Scholar 

  • Aslam R, Ansari MYK, Choudhary S, Bhat TM, Jahan N (2014) Genotoxic effects of heavy metal cadmium on growth, biochemical, cyto-physiological parameters and detection of DNA polymorphism by RAPD in Capsicum annuum L.—an important spice crop of India. Saudi J Biol Sci 21:465–472

    Article  CAS  Google Scholar 

  • Bai R, Chao G, Sun H, Fan M, Sun Z (2009) Toxicity of cadmium on the seed germination and growth of Althaea rosea and Orychophragmus violace. Acta Agriculturae Boreali-Sinica 24:134–138

    Google Scholar 

  • Bala R, Thukral AK (2011) Phytoremediation of Cr (VI) by Spirodela polyrrhiza (L.) Schleiden employing reducing and chelating agents. Int J Phytoremediat 13:465–491

    Article  CAS  Google Scholar 

  • Baster P, Robert S, Kleine-Vehn J, Vanneste S, Kania U, Grunewald W, De Rybel B, Beeckman T, Friml J (2013) SCFTIR1/AFB-auxin signalling regulates PIN vacuolar trafficking and auxin fluxes during root gravitropism. EMBO J 32:260–274

    Article  CAS  Google Scholar 

  • Carvalho BA, Gabriel CM, Carvalho R, Ribeiro BA, Puggina FM, Dos SAA (2012) Lycopersicon esculentum submitted to Cd-stressful conditions in nutrition solution: nutrient contents and translocation. Ecotoxicol Environ Saf 86:176–181

    Article  Google Scholar 

  • Chen YX, He YF, Luo YM, Yu YL, Lin Q, Wong MH (2003) Physiological mechanism of plant roots exposed to cadmium. Chemosphere 50:789–793

    Article  CAS  Google Scholar 

  • Chen Z, Sheng X, He L, Huang Z, Zhang W (2013) Effects of root inoculation with bacteria on the growth, Cd uptake and bacterial communities associated with rape grown in Cd-contaminated soil. J Hazard Mater 244:709–717

    Article  Google Scholar 

  • Chen T, Zhou Z, Han R, Meng R, Wang H, Lu W (2015) Adsorption of cadmium by biochar derived from municipal sewage sludge: impact factors and adsorption mechanism. Chemosphere 134:286–293

    Article  CAS  Google Scholar 

  • Colangelo EP, Guerinot ML (2006) Put the metal to the petal: metal uptake and transport throughout plants. Curr Opin Plant Biol 9:322–330

    Article  CAS  Google Scholar 

  • Cui W, Li L, Gao Z, Wu H, Xie Y, Shen W (2012) Haem oxygenase-1 is involved in salicylic acid-induced alleviation of oxidative stress due to cadmium stress in Medicago sativa. J Exp Bot 63:5521–5534

    Article  CAS  Google Scholar 

  • Cui H, Zhang Z, Lv W, Xu J, Wang X (2015) Genome-wide characterization and analysis of F-box protein-encoding genes in the Malus domestica genome. Mol Gen Genomics 290:1435–1446

    Article  CAS  Google Scholar 

  • Da Rosa Corrêa AX, Rörig LR, Verdinelli MA, Cotelle S, Férard J, Radetski CM (2006) Cadmium phytotoxicity: quantitative sensitivity relationships between classical endpoints and antioxidative enzyme biomarkers. Sci Total Environ 357:120–127

    Article  Google Scholar 

  • Delperee C, Lutts S (2008) Growth inhibition occurs independently of cell mortality in tomato (Solanum lycopersicum) exposed to high cadmium concentrations. J Integr Plant Biol 50:300–310

    Article  CAS  Google Scholar 

  • Dill A, Thomas SG, Hu JH, Steber CM, Sun TP (2004) The Arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellin-induced degradation. Plant Cell 16:1392–1405

    Article  CAS  Google Scholar 

  • Djebali W, Zarrouk M, Brouquisse R, El KS, Limam F, Ghorbel MH, Chaibi W (2005) Ultrastructure and lipid alterations induced by cadmium in tomato (Lycopersicon esculentum) chloroplast membranes. Plant Biol (Stuttg) 7:358–368

    Article  CAS  Google Scholar 

  • Dong J, Wu F, Zhang G (2006) Influence of cadmium on antioxidant capacity and four microelement concentrations in tomato seedlings (Lycopersicon esculentum). Chemosphere 64:1659–1666

    Article  CAS  Google Scholar 

  • Filippone C, Marianneau P, Murri S, Mollard N, Avsic-Zupanc T, Chinikar S, Despres P, Caro V, Gessain A, Berthet N, Tordo N (2013) Molecular diagnostic and genetic characterization of highly pathogenic viruses: application during Crimean-Congo haemorrhagic fever virus outbreaks in Eastern Europe and the Middle East. Clin Microbiol Infec 19:E118–E128

    Article  CAS  Google Scholar 

  • Forde B, Lorenzo H (2001) The nutritional control of root development. Plant Soil 232:51–68

    Article  CAS  Google Scholar 

  • Grotz N, Guerinot ML (2006) Molecular aspects of Cu, Fe and Zn homeostasis in plants. BBA-MOL Cell Res 1763:595–608

  • Guerinot ML (2000) The ZIP family of metal transporters. Bba-Biomembranes 1465:190–198

    Article  CAS  Google Scholar 

  • Hediji H, Djebali W, Cabasson C, Maucourt M, Baldet P, Bertrand A, Boulila ZL, Deborde C, Moing A, Brouquisse R, Chaibi W, Gallusci P (2010a) Effects of long-term cadmium exposure on growth and metabolomic profile of tomato plants. Ecotoxicol Environ Saf 73:1965–1974

    Article  CAS  Google Scholar 

  • Hediji H, Djebali W, Cabasson C, Maucourt M, Baldet P, Bertrand A, Zoghlami LB, Deborde C, Moing A, Brouquisse R, Chaibi W, Gallusci P (2010b) Effects of long-term cadmium exposure on growth and metabolomic profile of tomato plants. Ecotox Environ Safe 73:1965–1974

    Article  CAS  Google Scholar 

  • Hou J, Liu X, Wang J, Zhao S, Cui B (2015) Microarray-based analysis of gene expression in Lycopersicon esculentum seedling roots in response to cadmium, chromium, mercury, and lead. Environ Sci Technol 49:1834–1841

    Article  CAS  Google Scholar 

  • Huang H, Yu N, Wang L, Gupta DK, He Z, Wang K, Zhu Z, Yan X, Li T, Yang X (2011) The phytoremediation potential of bioenergy crop Ricinus communis for DDTs and cadmium co-contaminated soil. Bioresour Technol 102:11034–11038

    Article  CAS  Google Scholar 

  • Husnjak K, Dikic I (2012) Ubiquitin-binding proteins: decoders of ubiquitin-mediated cellular functions. Annu Rev Biochem 81:291–322

    Article  CAS  Google Scholar 

  • Janicka-Russak M, Kabala K, Burzynski M (2012) Different effect of cadmium and copper on H+-ATPase activity in plasma membrane vesicles from Cucumis sativus roots. J Exp Bot 63:4133–4142

    Article  CAS  Google Scholar 

  • Jezequel K, Lebeau T (2008) Soil bioaugmentation by free and immobilized bacteria to reduce potentially phytoavailable cadmium. Bioresour Technol 99:690–698

    Article  CAS  Google Scholar 

  • Ju Y, Chen W, Liao C (2012) Assessing human exposure risk to cadmium through inhalation and seafood consumption. J Hazard Mater 227:353–361

    Article  Google Scholar 

  • Krasnodębska-Ostręga B, Sadowska M, Ostrowska S (2012) Thallium speciation in plant tissues-Tl(III) found in Sinapis alba L. grown in soil polluted with tailing sediment containing thallium minerals. Talanta 93:326–329

    Article  Google Scholar 

  • Kumar G, Singh RP (1993) Nitrate assimilation and biomass production in Sesamum indicuml. Seedlings in a lead enriched environment. Water Air Soil Pollut 66:163–171

    Article  CAS  Google Scholar 

  • Li Z, Chen L, Wu R, Wang X (2011) Effect of cadmium on seed germination, seedling growth and development of wheat. Journal of Triticeae Crops 31:1153–1157

    CAS  Google Scholar 

  • Li S, Zhou X, Huang Y, Zhu L, Zhang S, Zhao Y, Guo J, Chen J, Chen R (2013) Identification and characterization of the zinc-regulated transporters, iron-regulated transporter-like protein (ZIP) gene family in maize. BMC Plant Biol 13:114–127

    Article  Google Scholar 

  • Li L, Li Y, Song S, Deng H, Li N, Fu X, Chen G, Yuan L (2015) An anther development F-box (ADF) protein regulated by tapetum degeneration retardation (TDR) controls rice anther development. Planta 241:157–166

    Article  CAS  Google Scholar 

  • Lin Y, Aarts MGM (2012) The molecular mechanism of zinc and cadmium stress response in plants. Cell Mol Life Sci 69:3187–3206

    Article  CAS  Google Scholar 

  • Llamas A, Ullrich CI, Sanz A (2000) Cd2+ effects on transmembrane electrical potential difference, respiration and membrane permeability of rice (Oryza sativa L) roots. Plant Soil 219:21–28

    Article  CAS  Google Scholar 

  • Lopez-Millan A, Sagardoy R, Solanas M, Abadia A, Abadia J (2009) Cadmium toxicity in tomato (Lycopersicon esculentum) plants grown in hydroponics. Environ Exp Bot 65:376–385

    Article  CAS  Google Scholar 

  • Lozano P, Trombini C, Crespo E, Blasco J, Moreno-Garrido I (2014) ROI-scavenging enzyme activities as toxicity biomarkers in three species of marine microalgae exposed to model contaminants (copper, Irgarol and atrazine). Ecotox Environ Safe 104:294–301

    Article  CAS  Google Scholar 

  • Nelson DC, Scaffidi A, Dun EA, Waters MT, Flematti GR, Dixon KW, Beveridge CA, Ghisalberti EL, Smith SM (2011) F-box protein MAX2 has dual roles in karrikin and strigolactone signaling in Arabidopsis thaliana. P Natl Acad Sci Usa 108:8897–8902

    Article  CAS  Google Scholar 

  • Nie J, Liu Y, Zeng G, Zheng B, Tan X, Liu H, Xie J, Gan C, Liu W (2016) Cadmium accumulation and tolerance of Macleaya cordata: a newly potential plant for sustainable phytoremediation in Cd-contaminated soil. Environ Sci Pollut R 23:10189–10199

    Article  CAS  Google Scholar 

  • Orecchio S, Amorello D (2010) Platinum and rhodium associated with the leaves of Nerium oleander L.; analytical method using voltammetry; assessment of air quality in the Palermo (Italy) area. J Hazard Mater 174:720–727

    Article  CAS  Google Scholar 

  • Ortega-Villasante C, Rellán-Álvarez R, Del Campo FF, Carpena-Ruiz RO, Hernández LE (2005) Cellular damage induced by cadmium and mercury in Medicago sativa. J Exp Bot 56:2239–2251

    Article  CAS  Google Scholar 

  • Pitzschke A, Forzani C, Hirt H (2006) Reactive oxygen species signaling in plants. Antioxid Redox Sign 8:1757–1764

    Article  CAS  Google Scholar 

  • Rashed MN (2010) Monitoring of contaminated toxic and heavy metals, from mine tailings through age accumulation, in soil and some wild plants at Southeast Egypt. J Hazard Mater 178:739–746

    Article  CAS  Google Scholar 

  • Remans T, Thijs S, Truyens S, Weyens N, Schellingen K, Keunen E, Gielen H, Cuypers A, Vangronsveld J (2012) Understanding the development of roots exposed to contaminants and the potential of plant-associated bacteria for optimization of growth. Ann Bot-London 110:239–252

    Article  CAS  Google Scholar 

  • Schiefelbein JW (2000) Constructing a plant cell. The genetic control of root hair development. Plant Physiol 124:1525–1531

    Article  CAS  Google Scholar 

  • Shahabivand S, Maivan HZ, Goltapeh EM, Sharifi M, Aliloo AA (2012) The effects of root endophyte and arbuscular mycorrhizal fungi on growth and cadmium accumulation in wheat under cadmium toxicity. Plant Physiol Biochem 60:53–58

    Article  CAS  Google Scholar 

  • Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17:35–52

    Article  CAS  Google Scholar 

  • Smeets K, Cuypers A, Lambrechts A, Semane B, Hoet P, Van Laere A, Vangronsveld J (2005) Induction of oxidative stress and antioxidative mechanisms in Phaseolus vulgaris after Cd application. Plant Physiol Biochem 43:437–444

    Article  CAS  Google Scholar 

  • Song JB, Wang YX, Li HB, Li BW, Zhou ZS, Gao S, Yang ZM (2015) The F-box family genes as key elements in response to salt, heavy mental, and drought stresses in Medicago truncatula. Funct Integr Genomic 15:495–507

    Article  CAS  Google Scholar 

  • Stephens BW, Cook DR, Grusak MA (2011) Characterization of zinc transport by divalent metal transporters of the ZIP family from the model legume Medicago truncatula. Biometals 24:51–58

    Article  CAS  Google Scholar 

  • Sun X, Guo L (2013) Relationship between cadmium-induced root subapical hair development and ethylene biosynthesis in oilseed rape seedlings. Acta Biol Cracov Ser Bot 55:68–75

    CAS  Google Scholar 

  • Swartjes FA, Versluijs KW, Otte PF (2013) A tiered approach for the human health risk assessment for consumption of vegetables from with cadmium-contaminated land in urban areas. Environ Res 126:223–231

    Article  CAS  Google Scholar 

  • Teng Y, Luo Y, Ma W, Zhu L, Ren W, Luo Y, Christie P, Li Z (2015) Trichoderma Reesei FS10-C enhances phytoremediation of Cd-contaminated soil by Sedum plumbizincicola and associated soil microbial activities. Front Plant Sci 6:1–10

    Article  Google Scholar 

  • Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCFCO11 complex during jasmonate signalling. Nature 448:661–662

    Article  CAS  Google Scholar 

  • U.S. Environmental Protection Agency (1996) Ecological effects test guidelines, EPA712-C-96-154, Prevention, Pesticides and Toxic Substances

  • Wang Q, Zhang J, Zhao B, Xin X, Zhang C, Zhang H (2014) The influence of long-term fertilization on cadmium (Cd) accumulation in soil and its uptake by crops. Environ Sci Pollut R 21:10377–10385

    Article  CAS  Google Scholar 

  • Wargent JJ, Pickup DA, Paul ND, Roberts MR (2013) Reduction of photosynthetic sensitivity in response to abiotic stress in tomato is mediated by a new generation plant activator. BMC Plant Biol 13:108–122

    Article  CAS  Google Scholar 

  • Waters MT, Scaffidi A, Flematti GR, Smith SM (2013) The origins and mechanisms of karrikin signalling. Curr Opin Plant Biol 16:667–673

    Article  CAS  Google Scholar 

  • Weber M, Trampczynska A, Clemens S (2006) Comparative transcriptome analysis of toxic metal responses in Arabidopsis thaliana and the Cd2+-hypertolerant facultative metallophyte Arabidopsis halleri. Plant Cell Environ 29:950–963

    Article  CAS  Google Scholar 

  • Williams TD, Davies IM, Wu H, Diab AM, Webster L, Viant MR, Chipman JK, Leaver MJ, George SG, Moffat CF, Robinson CD (2014) Molecular responses of European flounder (Platichthys flesus) chronically exposed to contaminated estuarine sediments. Chemosphere 108:152–158

    Article  CAS  Google Scholar 

  • Xu J, Sun J, Du L, Liu X (2012) Comparative transcriptome analysis of cadmium responses in Solanum nigrum and Solanum torvum. New Phytol 196:110–124

    Article  CAS  Google Scholar 

  • Yan Y, Chen X, Yang K, Sun Z, Fu Y, Zhang Y, Fang R (2011) Overexpression of an F-box protein gene reduces abiotic stress tolerance and promotes root growth in rice. Mol Plant 4:190–197

    Article  CAS  Google Scholar 

  • Zheng H, Li S, Wu Z, Zhang Y, Hu S, Yan Y, Li Y (2011) Differential response of multiple zebrafish hepatic F-box protein genes to 17 alpha-ethinylestradiol treatment. J Environ Sci-China 23:664–670

    Article  CAS  Google Scholar 

  • Zhou S, Kong X, Kang H, Sun X, Wang W (2015) The involvement of wheat F-box protein gene TaFBA1 in the oxidative stress tolerance of plants. PLoS One 10:1–16

    Google Scholar 

  • Zhou Q, Guo J, He C, Shen C, Huang Y, Chen J, Guo J, Yuan J, Yang Z (2016) Comparative transcriptome analysis between low- and high-cadmium-accumulating genotypes of pakchoi (Brassica chinensis L.) in response to cadmium stress. Environ Sci Technol 50:6485–6494

    Article  CAS  Google Scholar 

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Acknowledgments

National Basic Research Program of China (2013CB430400); the National Natural Science Foundation of China (21377013, 21607043); the Fundamental Research Funds for the Central Universities (2016ZZD06); and the Open Project of Key Laboratory of Environmental Biotechnology, CAS (Grant No. kf2016009), provided the financial support.

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Correspondence to Xinhui Liu or Xiangke Wang.

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Responsible editor: Yi-ping Chen

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Hou, J., Liu, X., Cui, B. et al. Concentration-dependent alterations in gene expression induced by cadmium in Solanum lycopersicum . Environ Sci Pollut Res 24, 10528–10536 (2017). https://doi.org/10.1007/s11356-017-8748-4

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