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Mutation of mpk6 enhances cadmium tolerance in Arabidopsis plants by alleviating oxidative stress

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Abstract

Background and aims

Cadmium (Cd) could activate activity of mitogen-activated protein kinase MPK6 in plants. In this study, we investigated the role of MPK6 in mediating Cd toxicity in plants.

Methods

The wild type Arabidopsis plants (WT) and the mpk6-2 mutants were subjected either 0 (Control) or 10 μM Cd treatment. Kinase activity of MPK6, nitric oxide (NO) level, Cd concentration, and oxidative stress were measured.

Results

In WT plants, Cd exposure rapidly stimulated kinase activity of MPK6. However, upon Cd exposure, mpk6-2 showed better growth than the WT. Although Cd-induced production of NO in roots was greater in WT than in mpk6-2, there was no difference in Cd concentration between the two plants. Nevertheless, the Cd-induced hydroperoxide burst, lipid peroxidation and loss of membrane integrity, were all more severe in the WT than in mpk6-2. Foliar applications of antioxidant ascorbic acid, vigorously improved the growth of both the WT and mpk6-2 under Cd exposure. Thereby the growth difference between these two plants was minimized.

Conclusions

Mutation of mpk6 enhances Cd tolerance in plants by alleviating oxidative stress, but did not affect cadmium accumulation in plants.

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References

  • Alloway BJ (1990) Heavy metals in soils. Blackie Son, New Jersey

    Google Scholar 

  • Bai TH, Li CY, Ma FW, Feng FJ, Shu HR (2010) Responses of growth and antioxidant system to root-zone hypoxia stress in two Malus species. Plant Soil 327(1–2):95–105

    Article  CAS  Google Scholar 

  • Baker CJ, Mock NM (1994) An improved method for monitoring cell death in a cell suspension and leaf disk assays using Evans blue. Plant Cell Tiss Org Cult 39(1):7–12

    Article  Google Scholar 

  • Besson-Bard A, Gravot A, Richaud P (2009) Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake. Plant Physiol 149:1302–1315

    Article  PubMed  CAS  Google Scholar 

  • Cavalcanti FR, Lima JPMS, Ferreira-Silva SL, Viégas RA, Silveira JAG (2007) Roots and leaves display contrasting oxidative response during salt stress and recovery in cowpea. J Plant Physiol 164(5):591–600

    Article  PubMed  CAS  Google Scholar 

  • Chen F, Wang F, Wu F, Mao W, Zhang G, Zhou M (2010) Modulation of exogenous glutathione in antioxidant defense system against Cd stress in the two barley genotypes differing in Cd tolerance. Plant Physiol Biochem 48:663–672

    Article  PubMed  CAS  Google Scholar 

  • Colcombet J, Hirt H (2008) Arabidopsis MAPKs: A complex signalling network involved in multiple biological processes. Biochem J 413:217–226

    Article  PubMed  CAS  Google Scholar 

  • Das P, Samantaray S, Rout GR (1997) Studies on cadmium toxicity in plants: A review. Environ Pollut 98:29–36

    Article  PubMed  CAS  Google Scholar 

  • Guo FQ, Crawford NM (2005) Arabidopsis nitric oxide synthase1 is targeted to mitochondria and protects against oxidative damage and dark-induced senescence. Plant Cell 17:3436–3450

    Article  PubMed  CAS  Google Scholar 

  • Jin CW, Du ST, Chen WW, Li GX, Zhang YS, Zheng SJ (2009a) Elevated carbon dioxide improves plant Fe nutrition through enhancing the Fe-deficiency-induced responses under Fe-limited conditions in tomato. Plant Physiol 150:272–280

    Article  PubMed  CAS  Google Scholar 

  • Jin CW, Du ST, Zhang YS, Lin XY, Tang CX (2009b) Differential regulatory role of nitric oxide in mediating nitrate reductase activity in roots of tomato (Solanum lycocarpum). Ann Bot 104:9–17

    Article  PubMed  CAS  Google Scholar 

  • Laspina NV, Groppa MD, Tomaro ML, Benavides MP (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169:323–330

    Article  CAS  Google Scholar 

  • Liu XM, Kim KE, Kim KC, Nguyen XC, Han HJ, Jung MS, Kim HS, Kim SH, Park HC, Yun DJ, Chung WK (2010) Cadmium activates Arabidopsis MPK3 and MPK6 via accumulation of reactive oxygen species. Phytochem 71:614–618

    Article  CAS  Google Scholar 

  • Luo BF, Du ST, Lu KX, Liu WJ, Lin XY, Jin CW (2012) Iron uptake system mediates nitrate-facilitated cadmium accumulation in tomato (Solanum lycopersicum) plants. J Exp Bot 63:3127–3136

    Article  PubMed  CAS  Google Scholar 

  • Lux A, Martinka M, Vaculík M, White PJ (2011) Root responses to cadmium in the rhizosphere: A review. J Exp Bot 62:21–37

    Article  PubMed  CAS  Google Scholar 

  • Ma WW, Xu WZ, Xu H, Chen YS, He ZY, Ma M (2010) Nitric oxide modulates cadmium influx during cadmium-induced programmed cell death in tobacco BY-2 cells. Planta 232:325–335

    Article  PubMed  CAS  Google Scholar 

  • Menke FLH, Van Pelt JA, Pieterse CMJ, Klessig DF (2004) Silencing of the mitogen-activated protein kinase MPK6 compromises disease resistance in Arabidopsis. Plant Cell 16:897–907

    Article  PubMed  CAS  Google Scholar 

  • Mullineaux PM, Baker NR (2010) Oxidative stress: Antagonistic signaling for acclimation or cell death? Plant Physiol 154(2):521–525

    Article  PubMed  CAS  Google Scholar 

  • Pan K, Wang WX (2012) Trace metal contamination in estuarine and coastal environments in China. Sci Total Environ 421–422:3–16

    Article  PubMed  Google Scholar 

  • Pitzschke A, Schikora A, Hirt H (2009) MAPK cascade signalling networks in plant defence. Curr Opin Plant Biol 12:421–426

    Article  PubMed  CAS  Google Scholar 

  • Poschenrieder C, Gunsé B, Barceló J (1989) Influence of cadmium on water relations, stomatal resistance, and abscisic acid content in expanding bean leaves. Plant Physiol 90:1365–1371

    Article  PubMed  CAS  Google Scholar 

  • Qin YH, da Silva JAT, Bi JH, Zhang SL, Hu GB (2011) Response of in vitro strawberry to antibiotics. Plant Growth Regul 65:183–193

    Article  CAS  Google Scholar 

  • Romero-Puertas MC, Palma JM, Gómez M, del Río LA, Sandalio LM (2002) Cadmium causes the oxidative modification of proteins in pea plants. Plant Cell Environ 25:677–686

    Article  CAS  Google Scholar 

  • Ronald E (2000) Handbook of chemical risk assessment: health hazards to humans, plants, and animals. Lewis Publishers, Boca Raton, pp 1–43

    Google Scholar 

  • Sandalio LM, Dalurzo HC, Gómez M, Romero-Puertas MC, del Río LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126

    PubMed  CAS  Google Scholar 

  • Sarwar N, Malhi SS, Zia MH, Naeem A, Bibi S, Farid G (2010) Role of mineral nutrition in minimizing cadmium accumulation by plants. J Sci Food Agric 90:925–937

    PubMed  CAS  Google Scholar 

  • Shapiro AD (2005) Nitric oxide signaling in plants. Vita Hor 72:339–398

    Article  CAS  Google Scholar 

  • Sharma SS, Dietz KJ (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14(1):43–50

    Article  PubMed  CAS  Google Scholar 

  • Shukla N, Awasthi RP, Rawat L, Kumar J (2012) Biochemical and physiological responses of rice (Oryza sativa L.) as influenced by Trichoderma harzianum under drought stress. Plant Physiol Biochem 54:78–88

    Article  PubMed  CAS  Google Scholar 

  • Singh HP, Batish DR, Kaur G, Arora K, Kohli RK (2008) Nitric oxide (as sodium nitroprusside) supplementation ameliorates Cd toxicity in hydroponically grown wheat roots. Environ Exp Bot 63:158–167

    Article  CAS  Google Scholar 

  • Singh PK, Tewari RK (2003) Cadmium toxicity induced changes in plant water relations and oxidative metabolism of Brassica juncea L. plants. J Environ Biol 24:107–112

    PubMed  CAS  Google Scholar 

  • Stanisavljević N, Savić J, Jovanović Ž, Miljuš-Djukić J, Radović S, Vinterhalter D, Vinterhalter B (2012) Antioxidative-related enzyme activity in Alyssum markgrafii shoot cultures as affected by nickel level. Acta Physiol Plant 34(5):1997–2006

    Article  Google Scholar 

  • Villiers F, Ducruix C, Hugouvieux V, Jarno N, Ezan E, Garin J, Junot C, Bourguignon J (2011) Investigating the plant response to cadmium exposure by proteomic and metabolomic approaches. Proteomics 11:1650–1663

    Article  PubMed  CAS  Google Scholar 

  • Wang P, Du Y, Li Y, Ren D, Song CP (2010) Hydrogen peroxide-mediated activation of MAP kinase 6 modulates nitric oxide biosynthesis and signal transduction in Arabidopsis. Plant Cell 22:2981–2998

    Article  PubMed  CAS  Google Scholar 

  • Wong SC, Li XD, Zhang G, Qi SH, Min YS (2002) Heavy metals in agricultural soils of the Pearl River Delta, South China. Environ Pollut 119:33–44

    Article  PubMed  CAS  Google Scholar 

  • Xing Y, Jia W, Zhang J (2008) AtMKK1 mediates ABA-induced CAT1 expression and H2O2 production via AtMPK6-coupled signaling in Arabidopsis. Plant J 54:440–451

    Article  PubMed  CAS  Google Scholar 

  • Xiong J, An L, Lu H, Zhu C (2009) Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicellulose contents in root cell wall. Planta 230:755–765

    Article  PubMed  CAS  Google Scholar 

  • Xu J, Wang W, Yin H, Liu X, Sun H, Mi Q (2010) Exogenous nitric oxide improves antioxidative capacity and reduces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil 326:321–330

    Article  CAS  Google Scholar 

  • Xu FJ, Li G, Jin CW, Liu WJ, Zhang SS, Zhang YS, Lin XY (2012) Aluminum-induced changes in reactive oxygen species accumulation, lipid peroxidation and antioxidant capacity in wheat root tips. Biol Plant 56:89–96

    Article  CAS  Google Scholar 

  • Ye Y, Li Z, Xing D (2013) Nitric oxide promotes MPK6-mediated caspase-3-like activation in cadmium-induced Arabidopsis thaliana programmed cell death. Plant Cell Environ 36(1):1–15

    Article  PubMed  CAS  Google Scholar 

  • Yu L, Nie J, Cao C, Jin Y, Yan M, Wang F, Liu J, Xiao Y, Liang Y, Zhang W (2010) Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana. New Phytol 188:762–773

    Article  PubMed  CAS  Google Scholar 

  • Zhang T, Liu Y, Yang T, Zhang L, Xu S, An L (2006) Diverse signals converge at MAPK cascades in plant. Plant Physiol Biochem 44:274–283

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the Natural Science foundation of China (Grant Nos 31270041, 30900170), the Zhejiang Province Natural Science Foundation (No.Y5090106). We thank Professor Jianhua Zhang (Chinese University of Hong Kong, Hong Kong) for kindly providing mpk6-3 mutant seeds.

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Authors and Affiliations

  1. MOE Key Laboratory of Environment Remediation and Ecosystem Health, College of Environmental and Resource Science, Zhejiang University, Hangzhou, 310058, China

    Chong-Wei Jin, Qian-Qian Mao, Bing-Fang Luo & Xian-Yong Lin

  2. College of Environmental Science and Engineering, Zhejiang Gongshang University, Hangzhou, 310035, China

    Shao-Ting Du

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  1. Chong-Wei Jin
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  2. Qian-Qian Mao
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  3. Bing-Fang Luo
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  4. Xian-Yong Lin
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  5. Shao-Ting Du
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Correspondence to Shao-Ting Du.

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Responsible Editor: Henk Schat.

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Jin, CW., Mao, QQ., Luo, BF. et al. Mutation of mpk6 enhances cadmium tolerance in Arabidopsis plants by alleviating oxidative stress. Plant Soil 371, 387–396 (2013). https://doi.org/10.1007/s11104-013-1699-8

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  • DOI: https://doi.org/10.1007/s11104-013-1699-8

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