Antioxidant defense gene analysis in Brassica oleracea and Trifolium repens exposed to Cd and/or Pb

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• 作者：F. Bernard ; S. Dumez ; F. Brulle ; S. Lemière…
• 关键词：Brassica oleracea ; Trifolium repens ; Antioxidant response ; Gene expression ; Metal trace elements ; Metal accumulation
• 刊名：Environmental Science and Pollution Research
• 出版年：2016
• 出版时间：February 2016
• 年：2016
• 卷：23
• 期：4
• 页码：3136-3151
• 全文大小：1,370 KB
• 参考文献：Abercrombie JM, Halfhill MD, Ranjan P, Murali RR, Saxton AM, Yuan JS, Stewart CN Jr (2008) Transcriptional responses of Arabidopsis thaliana plants to As (V) stress. BMC Plant Biol 8:87–101CrossRef
  Akashi K, Nishimura N, Ishida Y, Yokota A (2004) Potent hydroxyl radical scavenging activity of drought-induced type-2 metallothionein in wild watermelon. Biochem Biophys Res Commun 323:72–78CrossRef
  Andersen CL, Jensen JL, Ørntoft TF (2004) Normalization of real time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 64:5245–5250CrossRef
  Arduini I, Godbold DL, Onnis A (1996) Cadmium and copper uptake and distribution in Mediterranean tree seedlings. Physiol Plant 97:111–117CrossRef
  Ayele M, Haas BJ, Kumar N, Wu H, Xiao Y, Van Aken S, Utterback TR, Wortman JR, White OR, Town CD (2005) Whole genome shotgun sequencing of Brassica oleracea and its application to gene discovery and annotation in Arabidopsis. Genome Res 15:487–495CrossRef
  Baccouch S, Chaoui A, El Ferjani E (2001) Nickel toxicity induces oxidative damage in Zea mays roots. J Plant Nutr 24:1085–1097CrossRef
  Bargagli R (1998) Chemical elements and plant life. In: Bargagli R (ed) Trace elements in terrestrial plants: an ecophysiological approach to biomonitoring and biorecovery. Springer, New York, 324 pp
  Baycu G, Tolunay D, Özden H, Günebakan S (2006) Ecophysiological and seasonal variations in Cd, Pb, Zn and Ni concentrations in the leaves of urban deciduous trees in Istanbul. Environ Pollut 143:545–554CrossRef
  Bernard F, Brulle F, Douay F, Lemière S, Demunyck S, Vandenbulcke F (2010) Metallic trace element body burdens and gene expression analysis of biomarker candidates in Eisenia fetida, using an “exposure/depuration” experimental scheme with field soils. Ecotoxicol Environ Saf 73:1034–1045CrossRef
  Bernard F, Brulle F, Dumez S, Lemiere S, Platel A, Nesslany F, Cuny D, Deram A, Vandenbulcke F (2015) Antioxidant responses of Annelids, Brassicaceae and Fabaceae to pollutants: a review. Ecotoxicol Environ Saf 114:273–303CrossRef
  Bidar G, Garçon G, Pruvot C, Dewaele D, Cazier F, Douay F, Shirali P (2007) Behavior of Trifolium repens and Lolium perenne growing in a heavy metal contaminated field: plant metal concentration and phytotoxicity. Environ Pollut 147:546–553CrossRef
  Bidar G, Pruvot C, Garçon G, Verdin A, Shirali P, Douay F (2009) Seasonal and annual variations of metal uptake, bioaccumulation, and toxicity in Trifolium repens and Lolium perenne growing in a heavy metal-contaminated field. Environ Sci Pollut Res 16:42–53CrossRef
  Brooks RR (1998) Phytochemistry of hyperaccumulators. In: Brooks RR (ed) Plants that hyperaccumulate heavy metals: their role in archaeology, microbiology, mineral exploration, phytomining and phytoremediation. CAB International, Wallingford, 380 pp
  Brulle F, Mitta G, Cocquerelle C, Vieau D, Lemière S, Leprêtre A, Vandenbulcke F (2006) Cloning and real-time PCR testing of 14 potential biomarkers in Eisenia fetida following cadmium exposure. Environ Sci Technol 40:2844–2850CrossRef
  Brulle F, Bernard F, Vandenbulcke F, Cuny D, Dumez S (2014) Identification of suitable qPCR reference genes in leaves of Brassica oleracea under abiotic stresses. Ecotoxicology 23(3):459–471CrossRef
  Chaoui A, Jarrar B, El Ferjani E (2004) Effect of cadmium and copper on peroxidase NADH oxidase and IAA oxidase activities in cell wall soluble and microsomal membrane fraction of pea roots. J Plant Physiol 161:1225–1234CrossRef
  Cobbett C (1999) A family of phytochelatin synthase genes from plant, fungal and animal species. Trends Plant Sci 4:335–337CrossRef
  Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182CrossRef
  Coyle P, Philcox JC, Carey LC, Rofe AM (2002) Metallothionein: the multi-purpose protein. Cell Mol Life Sci 59:627–647CrossRef
  Cui Y, McBride SJ, Boyd WA, Alper S, Freedman JH (2007) Toxicogenomic analysis of Caenorhabditis elegans reveals novel genes and pathways involved in the resistance to cadmium toxicity. Genome Biol 8:R122, art. nCrossRef
  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 168:309–316CrossRef
  De Nicola F, Maistro G, Alfani A (2003) Assessment of nutritional status and trace element contamination of holm oak woodlands through analyses of leaves and surrounding soils. Sci Total Environ 311:191–203CrossRef
  Dembitsky V (2003) Natural occurrence of arseno compounds in plants, lichens, fungi, algal species, and microorganisms. Plant Sci 165:1177–1192CrossRef
  Demuynck S, Grumiaux F, Mottier V, Schikorski D, Lemiere S, Leprêtre A (2007) Cd/Zn exposure interactions on metallothionein response in Eisenia fetida (Annelida, Oligochaeta). Comp Biochem Physiol C 145:658–668
  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 52:1101–1109CrossRef
  Edwards R, Dixon DP, Walbot V (2000) Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends Plant Sci 5:193–198CrossRef
  Fabisiak JP, Borisenko GG, Liu SX, Tyurin VA, Pitt BR, Kagan VE (2002) Redox sensor function of metallothioneins. Methods Enzymol 353:268–281CrossRef
  Fritsch C, Giraudoux P, Cœurdassier M, Douay F, Raoul F, Pruvot C, Waterlot C, de Vaufleury A, Scheifler R (2010) Spatial distribution of metals in smelter-impacted soils of woody habitats: influence of landscape and soil properties, and risk for wildlife. Chemosphere 81:141–155CrossRef
  Fritsch C, Cœurdassier M, Giraudoux P, Raoul F, Douay F, Rieffel D, de Vaufleury A, Scheifler R (2011) Spatially explicit analysis of metal transfer to biota: influence of soil contamination and landscape. PLoS One 6:e20682CrossRef
  Godet JP, Demuynck S, Waterlot C, Lemiere S, Souty-Grosset C, Scheifler R, Douay F, Lepretre A, Pruvot C (2011) Growth and metal accumulation in Porcellio scaber exposed to poplar litter from Cd-, Pb-, and Zn-contaminated sites. Ecotoxicol Environ Saf 74:451–458CrossRef
  Haq F, Mahoney M, Koropatnick J (2003) Signaling events for metallothionein induction. Mutat Res 523:211–226CrossRef
  Hasan SA, Fariduddin Q, Ali B, Hayat S, Ahmad A (2009) Cadmium: toxicity and tolerance in plants. J Environ Biol 30:165–174
  Hasanuzzaman M, Hossain MA, Fujita M (2012) Exogenous selenium pretreatment protects rapeseed seedlings from cadmium-induced oxidative stress by upregulating antioxidant defense and methylglyoxal detoxification systems. Biol Trace Elem Res 149:248–261CrossRef
  Hassan Z, Aarts MGM (2011) Opportunities and feasibilities for biotechnological improvement of Zn, Cd or Ni tolerance and accumulation in plants. Environ Exp Bot 72:53–63CrossRef
  Huala E, Dickerman AW, Garcia-Hernandez M, Weems D, Reiser L, LaFond F, Hanley D, Kiphart D, Zhuang M, Huang W, Mueller LA, Bhattacharyya D, Bhaya D, Sobral BW, Beavis W, Meinke DW, Town CD, Somerville C, Rhee SY (2001) The Arabidopsis Information Resource (TAIR): a comprehensive database and web-based information retrieval, analysis, and visualization system for a model plant. Nucleic Acids Res 29(1):102–105CrossRef
  Karataglis S, Moustakas M, Symeonidis L (1991) Effects of heavy metals on isoperoxidases of wheat. Biol Plant 33:3–9CrossRef
  Kastori R, Petrovic M, Petrovic N (1992) Effect of excess lead, cadmium, copper and zinc on water relations in sunflower. J Plant Nutr 15:2427–2439CrossRef
  Kilili KG, Atanassova N, Vardanyan A, Clatot N, Al-Sabarna K, Kanellopoulos PN, Makris AM, Kampranis SC (2004) Differential roles of tau class glutathione S-transferases in oxidative stress. J Biol Chem 279:24540–24551CrossRef
  Kratovalieva S, Cvetanowska L (2001) Influence of different lead concentrations to some morphophysiological parameters at tomato (Lycopersicon esculentum Mill.) in experimental conditions. Maced Agric Rev 48(1/2):35–41
  Kusznierewicz B, Baczek-Kwinta R, Bartoszek A, Piekarska A, Huk A, Manikowska A, Antonkiewicz J, Namieśnik J, Konieczka P (2012) The dose-dependent influence of zinc and cadmium contamination of soil on their uptake and glucosinolate content in white cabbage (Brassica oleracea var. capitata f. alba). Environ Toxicol Chem 31:2482–2489CrossRef
  Lamb DT, Ming H, Megharaj M, Naidu R (2010) Phytotoxicity and accumulation of lead in Australian native vegetation. Arch Environ Contam Toxicol 58(3):613–621CrossRef
  Malecka A, Piechalak A, Tomaszewska B (2009) Reactive oxygen species production and antioxidative defense system in pea root tissues treated with lead ions: the whole roots level. Acta Physiol Plant 31:1053–1063CrossRef
  Manier N, Deram A, Broos K, Denayer FO, Wan Haluwyn C (2009) White clover modulation index in heavy metal contaminated soils–a potential bioindicator. J Environ Qual 38:685–692CrossRef
  Manier N, Brulle F, Le Curieux F, Vandenbulcke F, Deram A (2012) Biomarker measurements in Trifolium repens and Eisenia fetida to assess the toxicity of soil contaminated with landfill leachate: a microcosm study. Ecotoxicol Environ Saf 80:339–348CrossRef
  Mazhoudi S, Chaoui A, Ghorbal MH, El Ferjani E (1997) Response of antioxidant enzymes to excess copper in tomato (Lycopersicon esculentum, Mill). Plant Sci 127:129–137CrossRef
  Meyers DER, Auchterlonie GJ, Webb RI, Wood B (2008) Uptake and localisation of lead in the root system of Brassica juncea. Environ Pollut 153:323–332CrossRef
  Mohanpuria P, Rana NK, Yadav SK (2007) Cadmium induced oxidative stress influence on glutathione metabolic genes of Camellia sinensis (L.) O Kuntze. Environ Toxicol 22:368–374CrossRef
  Morgan AJ, Kille P, Stürzenbaum SR (2007) Microevolution and ecotoxicology of metals in invertebrates. Environ Sci Technol 41:1085–1096CrossRef
  Palmiter RD (1998) The elusive function of metallothioneins. Proc Natl Acad Sci U S A 95:8428–8430CrossRef
  Passardi F, Longet D, Penel C, Dunand C (2004) The class III peroxidase multigenic family in rice and its evolution in land plants. Phytochemistry 65(13):1879–1893CrossRef
  Peijnenburg WJGM, Posthuma L, Eijsackers HJP, Allen HE (1997) A conceptual framework for implementation of bioavailability of metals for environmental management purposes. Ecotoxicol Environ Saf 37:163–172CrossRef
  Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30(9):e36CrossRef
  Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP (2004) Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper–Excel-based tool using pair-wise correlations. Biotechnol Lett 26:509–515CrossRef
  Qiu Q, Wang Y, Yang Z, Xin J, Yuan J, Wang J, Xin G (2011) Responses of different Chinese flowering cabbage (Brassica parachinensis L.) cultivars to cadmium and lead exposure: screening for Cd + Pb pollution-safe cultivars. Clean (Weinh) 39(11):925–932
  Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana, Totowa, pp 365–386
  Salt DE, Prince RC, Pickering IJ, Raskin I (1995) Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol 109:1427–1433
  Sanità di Toppi L, Gabbrielli R (1999) Response to Cd in higher plants. Environ Exp Bot 41:105–130CrossRef
  Sawbridge T, Ong EK, Binnion C, Emmerling M, Meath K, Nunan K, O'Neill M, O'Toole F, Simmonds J, Wearne K, Winkworth A, Spangenberg G (2003) Generation and analysis of expressed sequence tags in white clover (Trifolium repens L.). Plant Sci 165:1077–1087CrossRef
  Schell LM, Burnitz KK, Lathrop PW (2010) Pollution and human biology. Ann Hum Biol 37:347–366CrossRef
  Semane B, Cuypers A, Smeets K, Van Belleghem F, Horemans N, Schat H, Vangronsveld J (2007) Cadmium responses in Arabidopsis thaliana: glutathione metabolism and antioxidative defence system. Physiol Plant 129:519–528CrossRef
  Seth CS, Kumar Chaturvedi P, Misra V (2008) The role of phytochelatins and antioxidants in tolerance to Cd accumulation in Brassica juncea L. Ecotoxicol Environ Saf 71:76–85CrossRef
  Shahandeh H, Hossner LR (2002) Role of soil properties in phytoaccumulation of uranium. Water Air Soil Pollut 141:165–180CrossRef
  Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17:35–52CrossRef
  Smeets K, Ruytinx J, Semane B, Van Belleghem F, Remans T, Van Sanden S, Vangronsveld J, Cuypers A (2008) Cadmium-induced transcriptional and enzymatic alterations related to oxidative stress. Environ Exp Bot 63:1–8CrossRef
  Smeets K, Opdenakker K, Remans T, Van Sanden S, Van Belleghem 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 166:1982–1992CrossRef
  Stavreva DA, Gichner T (2002) DNA damage induced by hydrogen peroxide in cultured tobacco cells is dependent on the cell growth stage. Mutat Res 514:147–152CrossRef
  Sterckeman T, Douay F, Proix N, Fourrier H (2000) Vertical distribution of Cd, Pb and Zn in soils near smelters in the north of France. Environ Pollut 107:377–389CrossRef
  Sterckeman T, Douay F, Proix F, Fourrier H, Perdrix E (2002) Assessment of the contamination of cultivated soils by eighteen trace elements around smelters in the North of France. Water Air Soil Pollut 135:173–194CrossRef
  Stone D, Jepson P, Kramarz P, Laskowski R (2001) Time to death response in carabid beetles exposed to multiple stressors along a gradient of heavy metal pollution. Environ Pollut 113:239–244CrossRef
  Stürzenbaum SR, Georgiev O, Morgan AJ, Kille P (2004) Cadmium detoxification in earthworms: from genes to cells. Environ Sci Technol 38:6283–6289CrossRef
  The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815CrossRef
  Timmermans MJTN, Ellers J, Roelofs D, van Straalen NM (2005) Metallothionein mRNA expression and cadmium tolerance in metal-stressed and reference populations of the springtail Orchesella cincta. Ecotoxicology 14:727–739CrossRef
  Uraguchi S, Mori S, Kuramata M, Kawasaki A, Arao T, Ishikawa S (2009) Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice. J Exp Bot 60:2677–2688CrossRef
  Valério L, De Meyer M, Penel C, Dunand C (2004) Expression analysis of the Arabidopsis peroxidase multigenic family. Phytochemistry 65:1331–1342CrossRef
  Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:RESEARCH0034CrossRef
  Vanhoudt N, Vandenhove H, Horemans N, Wannijn J, Bujanic A, Vangronsveld J, Cuypers A (2010) Study of oxidative stress related response induced in Arabidopsis thaliana following mixed exposure to uranium and cadmium. Plant Physiol Biochem 48:879–886CrossRef
  Verkleij JAC, Schat H (1990) Mechanisms of metal tolerance in higher plants. In: Shaw AJ (ed) Heavy metal tolerance in plants: evolutionary aspects. CRC, Boca Raton, pp 179–193
  Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655CrossRef
  Wang CQ, Song H (2009) Calcium protects Trifolium repens L. seedlings against cadmium stress. Plant Cell Rep 28:1341–1349CrossRef
  Wojcik M, Tukiendorf A (2004) Phytochelatin synthesis and cadmium localization in wild type of Arabidopsis thaliana. Plant Growth Regul 44:71–80CrossRef
  Wong HL, Sakamoto T, Kawasaki T, Umemura K, Shimamoto K (2004) Down-regulation of metallothionein, a reactive oxygen scavenger, by the small GTPase OsRac1 in rice. Plant Physiol 135:1447–1456CrossRef
  Xin JL, Huang BF, Yang ZY, Yuan JG, Dai HW, Qiu Q (2010) Responses of different water spinach cultivars and their hybrid to Cd, Pb and Cd–Pb exposures. J Hazard Mater 17:468–476CrossRef
  Zhang H, Xu W, Guo J, He Z, Ma M (2005) Coordinated responses of phytochelatins and metallothioneins to heavy metals in garlic seedlings. Plant Sci 169:1059–1065CrossRef
  Zhou GK, Xu YF, Li J, Yang L, Liu JY (2006) Molecular analysis of the metallothionein gene family in rice (Oryza sativa L.). J Biochem Mol Biol 39:595–606CrossRef
  
• 作者单位：F. Bernard (1) (2) (3)
  S. Dumez (1) (3)
  F. Brulle (1) (3)
  S. Lemière (1) (2)
  A. Platel (1) (4)
  F. Nesslany (1) (4)
  D. Cuny (1) (3)
  A. Deram (1) (3) (5)
  F. Vandenbulcke (1) (2)
  
  1. Université de Lille, F-59000, Lille, France
  2. Laboratoire de Génie Civil et géo-Environnement EA4515, Université Lille Nord de France-Lille 1, F-59655, Villeneuve d’Ascq, France
  3. Laboratoire des Sciences Végétales et Fongiques, Faculté des Sciences Pharmaceutiques et Biologiques, Université de Lille, EA4483, 59006, Lille Cedex, France
  4. Laboratoire de Toxicologie Génétique, Institut Pasteur de Lille, EA 4483, 59800, Lille, France
  5. Faculté de Management de la Santé (ILIS), Université de Lille, EA4483, F-59120, Loos, France
  
• 刊物类别：Earth and Environmental Science
• 刊物主题：Environment
  Environment
  Atmospheric Protection, Air Quality Control and Air Pollution
  Waste Water Technology, Water Pollution Control, Water Management and Aquatic Pollution
  Industrial Pollution Prevention
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1614-7499

文摘

This study focused on the expression analysis of antioxidant defense genes in Brassica oleracea and in Trifolium repens. Plants were exposed for 3, 10, and 56 days in microcosms to a field-collected suburban soil spiked by low concentrations of cadmium and/or lead. In both species, metal accumulations and expression levels of genes encoding proteins involved and/or related to antioxidant defense systems (glutathione transferases, peroxidases, catalases, metallothioneins) were quantified in leaves in order to better understand the detoxification processes involved following exposure to metals. It appeared that strongest gene expression variations in T. repens were observed when plants are exposed to Cd (metallothionein and ascorbate peroxidase upregulations) whereas strongest variations in B. oleracea were observed in case of Cd/Pb co-exposures (metallothionein, glutathione transferase, and peroxidase upregulations). Results also suggest that there is a benefit to use complementary species in order to better apprehend the biological effects in ecotoxicology. Keywords Brassica oleracea Trifolium repens Antioxidant response Gene expression Metal trace elements Metal accumulation