Abstract
Hydrogen peroxide (H2O2) plays versatile roles in various biological processes and in responses to stress in plants. To investigate effects of exogenous H2O2 on the transcript levels of some genes encoding antioxidative enzymes, such as superoxide dismutase Cu/Zn (Cu/ZnSOD), catalase (CAT) and ascorbate peroxidase (APX), and also on the ultrastructural alterations caused by lead, 7-day-old seedlings of water caltrop (Trapa bicornis) were treated with lead salt (0.05 mmol/L) separately, or combined with H2O2 (2.5 mmol/L). Ultrastructural observation on the mesophyll cells demonstrated that the lead toxicity, which resulted in the membrane instability and abnormal organization within organelles, was eliminated under the condition of the co-treatment with H2O2 and lead. In this relation the combined treatment with H2O2 and lead prevented the increased amount of malondialdehyde to some extent during the whole experimental period (24, 48, and 72 h). Furthermore, quantitative measurements by reverse transcriptase-polymerase chain reaction (RT-PCR) showed that the co-treatment with both compounds, in contrast to the lead treatment alone, significantly up-regulated transcripts of CAT, APX, and a lignin biosynthesis related gene encoding ferulate-5-hydroxylase (F5H). The H2O2-induced F5H expression is thought to modify cell wall and thus lower Pb entry into water caltrop seedlings, thereby enhancing tolerance to Pb stress. Morphological and molecular evidences in the present study perhaps reflect the fact that some antioxidative enzymes, especially CAT and APX, combined with the action of F5H on cell wall modification, contribute to the enhanced antioxidative defense in the examined plants treated with lead.
Acknowledgements
This work was supported by the grants from the Key Subject Construction of Biology in Anhui Province, China (No. 2014SKQJ021 and No. 2014TSTD005), the Provincial Quality Engineer Fund of Anhui Education Department (No. 2014JXTD008 and No. 2015GXK015), the Scientific Research Foundation for the Returned Overseas Chinese Scholars, State Education Ministry, China (No. 2015-1098), and Anhui Agricultural University for the Subject-Talents Program (No. 2014XKPY-43) and the Key Discipline of Plant Biology (No. 2013ZDXK-01).
References
Asada K. 2006. Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol. 141: 391–396.10.1104/pp.106.082040Search in Google Scholar PubMed PubMed Central
Burr S.J. & Fry S.C. 2009. Feruloylated arabinoxylans are oxidatively cross-linked by extracellular maize peroxidase but not by horseradish peroxidase. Mol. Plant 2: 883–892.10.1093/mp/ssp044Search in Google Scholar PubMed
Cobbett C.S. 2000. Phytochelatins and their roles in heavy metal detoxification. Plant Physiol. 123: 825–832.10.1104/pp.123.3.825Search in Google Scholar PubMed PubMed Central
Dushenkov V., Kumar P.B.A.N., Motto H. & Raskin I. 1995.Rhizofiltration: the use of plants to remove heavy metals form aqueous streams. Environ. Sci. Technol. 29: 1239-1245.10.1021/es00005a015Search in Google Scholar PubMed
Fett J.P., Cambraia J., Oliva M.A. & Jord˜ao C.P. 1994. Absorption and distribution of cadmium in water hyacinth plants. J. Plant Nutr. 17: 1219–1230.10.1080/01904169409364800Search in Google Scholar
Foyer C., Lorez-Delgao H., Dat J. & Scott I. 1997. Hydrogen peroxide- and glutathione-associated mechanisms of acclima-tory stress tolerance and signaling. Physiol. Plant. 100: 241– 254.10.1111/j.1399-3054.1997.tb04780.xSearch in Google Scholar
Foyer C. & Noctor G. 2000. Oxygen processing in photosynthesis: regulation and signaling. New Phytol. 146: 359–388.10.1046/j.1469-8137.2000.00667.xSearch in Google Scholar
Gechev T., Gadjev I., van Breusegem F., Inze D., Dukiandjiev S., Toneva V. & Minkov I. 2002. Hydrogen peroxide protects tobacco from oxidative stress by inducing a set of antioxidant enzymes. Cel. Mol. Life Sci. 59: 708–714.10.1007/s00018-002-8459-xSearch in Google Scholar PubMed
Giraud E., van Aken O., Uggalla V. & Whelan J. 2012. Redox regulation of mitochondrial function in plants. Plant Cell Environ. 35: 271–280.10.1111/j.1365-3040.2011.02293.xSearch in Google Scholar PubMed
Gratao P.L., Polle A., Lea P.J. & Azevedo R.A. 2005. Making the life of heavy metal stressed plants a little easier. Funct. Plant Biol. 32: 481–494.10.1071/FP05016Search in Google Scholar PubMed
Heath R.L. & Packer L. 1968. Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch. Biochem. Biophy. 125: 189–198.10.1016/0003-9861(68)90654-1Search in Google Scholar
Katsuhara M., Otsuka T. & Ezaki B. 2005. Salt stress-induced lipid peroxidation is reduced by glutathione S-transferase, but this reduction of lipid peroxides is not enough for a recovery of root growth in Arabidopsis. Plant Sci. 169: 369–373.10.1016/j.plantsci.2005.03.030Search in Google Scholar
Li D.H. 2009. Effects of lead polluted water on activities of su-peroxide dismutase, peroxidase and ultrastructure in leaves of Trapa bicornis seedlings. China Environ. Sci. 29: 136–141.Search in Google Scholar
Li D.H., Shi G.X., Ding X.Y., Zhou C.F., Xie K.B., & Chang F.C. 1999. Effects of Cd2+ and Hg2+ on growth and activity of superoxide dismutase and peroxidase in Trapa biscornis seedlings. J. Wuhan Bot. Res. 17: 206–210.Search in Google Scholar
Lopez-Delgado H., Dat J., Foyer C. & Scott I. 1998. Induction of termotolerance in potato microplants by acetylsalicyclic acid and H2O2. J. Exp. Bot. 49: 713–720.10.1093/jxb/49.321.713Search in Google Scholar
Maksymiec W. 2007. Signaling responses in plants to heavy metal stress. Acta Physiol. Plant 29: 177–187.10.1007/s11738-007-0036-3Search in Google Scholar
Marita J.M., Ralph J., Hatfield R.D. & Chapple C. 1999. NMR characterization of lignins in Arabidopsis altered in the activity of ferulate 5-hydroxylase. Proc. Natl. Acad. Sci. USA 96: 12328–12332.10.1073/pnas.96.22.12328Search in Google Scholar
Mishra S., Srivastava S., Tripathi R.D., Kumar R., Seth C.S. &upta D.K. 2006. Lead detoxification by coontail (Ceratophyllum demersum L.) involves induction of phytochelatins and antioxidant system in response to its accumulation. Chemosphere 65: 1027–1039.10.1016/j.chemosphere.2006.03.033Search in Google Scholar
Muhittin D., Demirors S.S. & Ugur C. 2009. Effect of lead toxicity on aquatic macrophyte Elodea canadensis Michx. Bul. Environ. Contam. Toxicol. 83: 249–254.10.1007/s00128-009-9733-5Search in Google Scholar
Nagajyoti P.C., Lee K.D. & Sreekanth T.V.M. 2010. Heavy metals, occurrence and toxicity for plants: a review. Environ. Chem. Lett. 8: 199–216.10.1007/s10311-010-0297-8Search in Google Scholar
Neill S.J., Desikan R., Clarke A., Hurst R.D. & Hancock J.T.2002a. Hydrogen peroxide and nitric oxide as signalling molecules in plants. J. Exp. Bot. 53: 1237–1247.10.1093/jexbot/53.372.1237Search in Google Scholar
Neill S.J., Desikan R. & Hancock J.T. 2002b. Hydrogen peroxide signalling. Curr. Opin. Plant Biol. 5: 388–395.10.1016/S1369-5266(02)00282-0Search in Google Scholar
Parys E., Romanowska E., Siedlecka M. & Poskuta J.W. 1998.The effect of lead on photosynthesis and respiration in detached leaves and in mesophyll protoplasts of Pisum sativum. Acta Physiol. Plant. 20: 313–322.10.1007/s11738-998-0064-7Search in Google Scholar
Patra M., Bhowmik N., Bandopadhyay B. & Sharma A. 2004.Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance. Environ. Exp. Bot. 52: 199–223.10.1016/j.envexpbot.2004.02.009Search in Google Scholar
Pinto E., Sigaud-Kutner T.C.S., Leit˜ao M.A.S., Okamoto A.K.,Morse D. & Colepicolo P. 2003. Heavy metal-induced oxidative stress in algae. J. Phycol. 39: 1008–1018.10.1111/j.0022-3646.2003.02-193.xSearch in Google Scholar
Quan L.J., Zhang B., Shi W.W. & Li H.Y. 2008. Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network. J. Integr. Plant Biol. 50: 2–18.10.1111/j.1744-7909.2007.00599.xSearch in Google Scholar
Rao K.S. & Kristen U. 1990. The influence of the detergent Triton X-100 on the growth and ultrastructure of tobacco pollen tubes. Can. J. Bot. 68: 1131–1138.10.1139/b90-143Search in Google Scholar
Ray P.D., Huang B.W. & Tsuji Y. 2012. Reactive oxygen species(ROS) homeostasis and redox regulation in cellular signaling. Cell. Signal. 24: 981–990.10.1016/j.cellsig.2012.01.008Search in Google Scholar
Rashid A., Camm E.L. & Ekramoddoullah K.M. 1994. Molecular mechanism of action of Pb2+ and Zn2+ on water oxidizing complex of photosystem II. FEBS Let. 350: 296–298.10.1016/0014-5793(94)00789-6Search in Google Scholar
Reddy A.M., Kumar S.G., Jyothsnakumari G., Thimmanaik S. & Sudhakar C. 2005. Lead induced changes in antioxidant metabolism of horsegram (Macrotyloma uniflorum Verdc.) and bengalgram (Cicer arietinum L.). Chemosphere 60: 97– 104.10.1016/j.chemosphere.2004.11.092Search in Google Scholar PubMed
Reiss H.D. & Herth W. 1979. Calcium ionophore A-23187 affects localized wall secretion in the tip region of pollen tubes of Lilium longiflorum. Planta 145: 225–232.10.1007/BF00454445Search in Google Scholar PubMed
Sandalio L.M., Dalurzo H.C., Gómez M., Romero-Puertas M.C. & del Río L.A. 2001. Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J. Exp. Bot. 52: 2115–2126.10.1093/jexbot/52.364.2115Search in Google Scholar PubMed
Seth C.S., Remans T., Keunen E., Jozefczak M., Gielen H., Opdenakker K., Weyens N., van Gronsveld J. & Cuypers A. 2012. Phytoextraction of toxic metals: a central role for glutathione. Plant Cell Environ. 35: 334–346.10.1111/j.1365-3040.2011.02338.xSearch in Google Scholar
Sharma P. & Dubey R.S. 2004. Ascorbate peroxidase from rice seedlings: properties of enzyme isoforms, effects of stresses and protective roles of osmolytes. Plant Sci. 167: 541–550.10.1016/j.plantsci.2004.04.028Search in Google Scholar
Sharma P. & Dubey R.S. 2005. Lead toxicity in plants. Braz. J.Plant Physiol. 17: 35–52.10.1590/S1677-04202005000100004Search in Google Scholar
Suzuki N., Koussevitzky S., Mittler R. & Miller G. 2012. ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ. 35: 259–270.10.1111/j.1365-3040.2011.02336.xSearch in Google Scholar
Verma S. & Dubey R.S. 2003. Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci. 164: 645–655.10.1016/S0168-9452(03)00022-0Search in Google Scholar
Yasemin E., Deniz T. & Beycan A. 2009. A crop tolerating oxidative stress induced by excess lead: maize. Acta Physiol. Plant. 31: 319–330.10.1007/s11738-008-0238-3Search in Google Scholar
Yu C.W., Murphy T., Sung W.W. & Lin C.H. 2002. H2O2 treatment induces glutathione accumulation and chilling tolerance in mung bean. Funct. Plant Biol. 29: 1081–1087.10.1071/PP01264Search in Google Scholar
Yu C.W., Murphy T. & Lin C.H. 2003. Hydrogen peroxide induced chilling tolerance in mung bean mediated through ABA-independent glutathione accumulation. Funct. Plant Biol. 30: 955–963.10.1071/FP03091Search in Google Scholar
Zacchini M., Rea E., Tullio M. & Agazio M. 2003. Increased antioxidative capacity in maize calli during and after oxidative stress induced by a long lead treatment. Plant Physiol. Biochem. 41: 49–54.10.1016/S0981-9428(02)00008-6Search in Google Scholar
Zhu X.F., Zheng C., Hu Y.T., Jiang T., Liu Y., Dong N.Y., Yang J.L. & Zheng S.J. 2011. Cadmium-induced oxalate secretion from root apex is associated with cadmium exclusion and resistance in Lycopersicon esulentum. Plant Cell Environ. 34: 1055–1064.10.1111/j.1365-3040.2011.02304.xSearch in Google Scholar PubMed
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