Skip to main content

Advertisement

Log in

Protection of Artemisia annua roots and leaves against oxidative stress induced by arsenic

  • Original Paper
  • Published:
Biologia Plantarum

Abstract

The present study was conducted to examine differential responses of roots and leaves of Artemisia annua to different arsenic concentrations (50, 100, and 150 μΜ) and treatment durations (1, 3, 5, or 7 d). The values of bioconcentration factor and translocation factor calculated on the basis of total As-accumulation in roots and shoots suggested that A. annua is a good As-accumulator. Above and below ground plant biomass was enhanced at 100 μΜ As but at 150 μΜ As was significantly reduced. As-treatment caused membrane damage more in the roots than in the leaves as reflected by higher degree of lipid peroxidation in the roots than in the leaves. In response to As stress, plants activated antioxidative defense for detoxification of induced reactive oxygen species (ROS), As sequestration via phytochelatins (PCS) as well as production of a wide range of secondary metabolites. All of them were activated differently in roots and leaves. Among enzymatic antioxidants, leaves significantly elevated superoxide dismutase (SOD), ascorbate peroxidase, and glutathione reductase, whereas in roots SOD, catalase, and peroxidase played significant role in ROS detoxification. Plants activated As-sequestration pathway through thiols, glutathione, and PCS and their respective genes were more induced in leaves than in roots. Further gas chromatography in tandem with mass spectroscopy analysis revealed differential modulation of secondary metabolites in leaves and roots to sustain As-stress. For example, roots synthesized linoleic acid (4.85 %) under As-treatment that probably stimulated stress-signalling pathways and in turn activated differential defense mechanisms in roots to cope up with the adverse effects of As.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

APX:

ascorbate peroxidase

BF:

bioconcentration factor

CAT:

catalase

GC-MS:

gas chromatography in tandem with mass spectroscopy

GR:

glutathione reductase

GSH:

glutathione

PCS:

phytochelatin

POX:

peroxidase

ROS:

reactive oxygen species

SOD:

superoxide dismutase

TBARS:

2-thiobarbituric acid reactive substance

TF:

translocation factor

References

  • Aebi, H.: Catalase in vitro. — Methods Enzymol. 105: 121–126, 1984.

    Article  CAS  PubMed  Google Scholar 

  • Ahmad, S.: Oxidative Stress and Antioxidant Defenses in Biology. — Springer, Heidelberg - Berlin 2012.

    Google Scholar 

  • Ali, M.B., Singh, N., Shohael, A.M., Hahn, E.J., Paek, K.Y.: Phenolics metabolism and lignin synthesis in root suspension cultures of Panax ginseng in response to copper stress. — Plant Sci. 171: 147–154, 2006.

    Article  CAS  Google Scholar 

  • Ali, M.B., Vajpayee, P., Tripathi, R.D., Rai, U.N., Singh, S.N., Singh, P.S.: Phytoremediation of lead, nickel, and copper by Salix acmophylla Boiss: role of antioxidant enzymes and antioxidant substances. — Environ. Contam. Toxicol. 70: 462–469, 2003.

    Article  CAS  Google Scholar 

  • Anderson, M.E.: Determination of glutathione and glutathione disulphide in biological samples. — Methods Enzymol. 113: 548–555, 1985.

    Article  CAS  PubMed  Google Scholar 

  • Baker, A.J.M.: Accumulators and excluders strategies in the response of plants to heavy metals. — J. Plant Nutr. 3: 643–654, 1981.

    Article  CAS  Google Scholar 

  • Bates, L.S., Waldren, R.P., Teare, I.D.: Rapid determination of free proline for water-stress studies. — Plant Soil 39: 205–207, 1973.

    Article  CAS  Google Scholar 

  • Beauchamp, C., Fridovich, I.: Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. — Anal. Biochem. 44: 276–287, 1971.

    Article  CAS  PubMed  Google Scholar 

  • Bradford, M.M.: A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. — Anal. Biochem. 72: 248–254, 1976.

    Article  CAS  PubMed  Google Scholar 

  • Bu-Olayan, A.H., Thomas, B.V.: Translocation and bioaccumulation of trace metals in desert plants of Kuwait Governorates. — Res. J. environ. Sci. 3: 581–587, 2009.

    Article  CAS  Google Scholar 

  • Carbonell, A.A., Aarabi, M.A., DeLaune, R.D., Gambrell, R.P., Patrick, W.H., Jr,: Arsenic in wetland vegetation: availability, phytotoxicity, uptake and effects on plant growth and nutrition. — Sci. total Environ. 217: 189–199, 1998.

    Article  CAS  Google Scholar 

  • Chen, G.X., Asada, K.: Ascorbate peroxidase in tea leaves: occurrence of two isoenzymes and the differences in their enzymatic and molecular properties. — Plant Cell Physiol. 30: 987–998, 1989.

    Article  CAS  Google Scholar 

  • Cui, S., Zhou, Q., Chao, L.: Potential hyperaccumulation of Pb, Zn, Cu and Cd in endurant plants distributed in an old smeltery, northeast China. — Environ. Geol. 51: 1043–1048, 2007.

    Article  CAS  Google Scholar 

  • Dubbs, W.E., Grimes, H.D.: The mid-pericarp cell layer in soybean pod walls is a multicellular compartment enriched in specific lipoxygenase isoforms. — Plant Physiol. 123: 1281–1288, 2000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dubey, R.S.: Metal toxicity, oxidative stress and antioxidative defense system in plants. - In Gupta, S.D. (ed): Reactive Oxygen Species and Antioxidants in Higher Plants. Pp. 177–203. CRC Press, Boca Raton 2011.

    Google Scholar 

  • Elobeid, M., Göbel, C., Feussner, I., Polle, A.: Cadmium interferes with auxin physiology and lignification in poplar. — J. exp. Bot. 63: 1413–1421, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Greger, M.: Metal availability and bioconcentration in plants. - In: Prasad, M.N.V., Hagemeyer, J. (ed.): Heavy Metal Stress in Plants. Pp. 1–27. Springer, Berlin - Heidelberg 1999.

    Chapter  Google Scholar 

  • Gupta, M., Sharma, P., Sarin, N.B., Sinha, A.K.: Differential response of arsenic stress in two varieties of Brassica juncea L. — Chemosphere 74: 1201–1208, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Hartley-Whitaker, J., Ainsworth, G., Meharg, A.A.: Copper and arsenate-induced oxidative stress in Holcus lanatus L. - Plant Cell Environ. 24: 713–22, 2001.

    Article  CAS  Google Scholar 

  • Heath, R.L., Packer, L.: Photoperoxidation in isolated chloroplasts: I. kinetics and stoichiometry of fatty acid peroxidation. — Arch. Biochem. Biophys. 125: 189–198, 1968.

    Article  CAS  PubMed  Google Scholar 

  • Imeh, U., Khokhar, S.: Distribution of conjugated and free phenols in fruits: antioxidant activity and cultivar variations. — J. Agr. Food. Chem. 50: 6301–6306, 2002.

    Article  CAS  Google Scholar 

  • Jimi, S., Uchiyama, M., Takaki, A.Y.A., Suzumiya, J., Hara, S.: Mechanisms of cell death induced by cadmium and arsenic. — Ann. N.Y. Acad. Sci. 1011: 325–331, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Khanuja, S.P.S., Shasany, A.K., Darokar, M.P., Kumar, S.: Rapid Isolation of DNA from dry and fresh samples of plants producing large amounts of secondary metabolites and essential oils. — Plant mol. Biol. Rep. 17: 1–7, 1999.

    Article  Google Scholar 

  • Kováčik, J., Klejdus, B.: Dynamics of phenolic acids and lignin accumulation in metal-treated Matricaria chamomilla roots. — Plant Cell Rep. 27: 605–615, 2008.

    Article  PubMed  Google Scholar 

  • Li, C.X., Feng, S.L., Yun, S., Jiang, L.N., Lu, X.Y., Hou, X.L.: Effects of arsenic on seed germination and physiological activities of wheat seedlings. — J. environ. Sci. 19: 725–732, 2007.

    Article  CAS  Google Scholar 

  • Loreto, F., Ciccioli, P., Brancaleoni, E., Valentini, R., De Lillis, M., Csiky, O., Seufert, G.: A hypothesis on the evolution of isoprenoid emission by oaks based on the correlation between emission type and Quercus taxonomy.–Oecologia 115: 302–305, 1998.

    Article  PubMed  Google Scholar 

  • Ma, B., Wan, J., Shen, Z.: H2O2 production and antioxidant responses in seeds and early seedlings of two different rice varieties exposed to aluminum. — Plant Growth Regul. 52: 91–100, 2007.

    Article  CAS  Google Scholar 

  • Mascher, R., Lippmann, B., Holzinger, S., Bergmann, H.: Arsenate toxicity: effects on oxidative stress response molecules and enzymes in red clover plants. — Plant Sci. 163: 961–969, 2002.

    Article  CAS  Google Scholar 

  • Mihucz, V.G., Tatar, E., Virag, I., Cseh, E., Fodor, F., Zaray, G.: Arsenic speciation in xylem sap of cucumber (Cucumis sativus L.). — Anal. Bioanal. Chem. 383: 461–466, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Murzaeva, S.V.: Effect of heavy metals on wheat seedlings:activation of antioxidant enzymes. — Appl. Biochem. Microbiol. 40: 98–103, 2004.

    Article  CAS  Google Scholar 

  • Nagalakshmi, N., Prasad, M.N.V.: Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. — Plant Sci. 160: 291–299, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Pandey, N., Pandey-Rai, S.: Modulations of physiological responses and possible involvement of defense-related secondary metabolites in acclimation of Artemisia annua L. against short-term UV-B radiation. — Planta 240: 611–627, 2014a.

    Article  CAS  PubMed  Google Scholar 

  • Pandey, N., Pandey-Rai, S.: Short term UV-B radiation-mediated transcriptional responses and altered secondary metabolism of in vitro propagated plantlets of Artemisia annua L. — Plant Cell Tissue Organ Cult. 116: 371–385, 2014b.

    Article  CAS  Google Scholar 

  • Pandey, N., Pandey-Rai, S.: Updates on artemisinin: an insight to mode of actions and strategies for enhanced global production. — Protoplasma 253: 15–30, 2016.

    Article  CAS  PubMed  Google Scholar 

  • Patra, J., Panda, B.B.: A comparison of biochemical responses to oxidative and metal stress in seedlings of barley, Hordeum vulgare L. — Environ. Pollut. 101: 99–105, 1998.

    Article  CAS  PubMed  Google Scholar 

  • Paul, S., Shaky, K.: Arsenic, chromium and NaCl induced artemisinin biosynthesis in Artemisia annua L.: a valuable antimalarial plant. — Ecotoxicol. Environ. Safety 98: 59–65, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Pickering, I.J., Prince, R.C., George, M.J., Smith, R.D., George, G.N., Salt, D.E.: Reduction and coordination of arsenic in Indian mustard. — Plant Physiol. 122: 1171–1177, 2000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Possell, M., Loreto, F.: The role of volatile organic compounds in plant resistance to abiotic stresses: responses and mechanisms. - In: Niinemets, Ü., Monson, R.K. (ed.): Biology, Controls and Models of Tree Volatile Organic Compound Emissions. (Tree Physiology. Vol. 5.) Pp. 209–235. Springer, Berlin 2013.

    Chapter  Google Scholar 

  • Rai, R., Meena, R.P., Smita, S.S., Shukla, A., Rai, S.K., Pandey-Rai, S.: UV-B and UV-C pre-treatments induce physiological changes and artemisinin biosynthesis in Artemisia annua L.–an antimalarial plant. — J. Photochem. Photobiol. B: Biol. 105: 216–225, 2011a.

    Article  CAS  Google Scholar 

  • Rai, R., Pandey, S., Pandey-Rai, S.: Arsenic-induced changes in morphological, physiological, and biochemical attributes and artemisinin biosynthesis in Artemisia annua, an antimalarial plant. — Ecotoxicology 20: 1900–1913, 2011b.

    Article  CAS  PubMed  Google Scholar 

  • Ramakrishna, A., Ravishankar, G.A.: Influence of abiotic stress signals on secondary metabolites in plants. — Plant Signal. Behav. 6: 1720–1731, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rauser, W.E.: Phytochelatins and related peptides. Structure, biosynthesis, and function. — Plant Physiol. 109: 1141, 1995.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roessner, U., Wagner, C., Kopka, J., Trethewey, R. N., Willmitzer, L.: Simultaneous analysis of metabolites in potato tuber by gas chromatography-mass spectrometry. — Plant J. 23: 131–142, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Romero-Puertas, M.C., Rodríguez-Serrano, M., Corpas, F.J., Gomez, M.D., Del Rio, L.A., Sandalio, L.M.: Cadmiuminduced subcellular accumulation of O2 - ·and H2O2 in pea leaves. — Plant Cell Environ. 27: 1122–1134, 2004.

    Article  CAS  Google Scholar 

  • Rui, H., Chen, C., Zhang, X., Shen, Z., Zhang, F.: Cd-induced oxidative stress and lignification in the roots of two Vicia sativa L. varieties with different Cd tolerances. — J. Hazard. Materials 301: 304–313, 2016.

    Article  CAS  Google Scholar 

  • Schaedle, M., Bassham, J.A.: Chloroplast glutathione reductase. — Plant Physiol. 59: 1011–1012, 1977.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmoger, M.E.V., Oven, M., Grill, E.: Detoxification of arsenic by phytochelatins in plants. — Plant Physiol. 122: 793–802, 2000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharkey, T.D., Wiberley, A.E., Donohue, A.R.: Isoprene emission from plants: why and how. — Ann.. Bot. 101: 5–18, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Sharma, I.: Arsenic induced oxidative stress in plants. — Biologia 67: 447–453, 2012.

    Article  CAS  Google Scholar 

  • Shi, Y.Z., Ruan, J.Y., Ma, L.F., Han, W.Y., Wang, F.: Accumulation and distribution of arsenic and cadmium by tea plants. — J. Zhejiang Univ. Sci. B. 9: 265–270, 2008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shri, M., Kumar, S., Chakrabarty, D., Trivedi, P.K., Mallick, S., Misra, P., Shukla, D., Mishra, S., Srivastava, S., Tripathi, R.D., Tuli, R.: Effect of arsenic on growth, oxidative stress, and antioxidant system in rice seedlings. — Ecotoxicol. Environ. Safety 72: 1102–1110, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Singh, A.P., Dixit, G., Mishra, S., Dwivedi, S., Tiwari, M., Mallick, S., Pandey, V., Trivedi, P.K., Chakrabarty, D., Tripathi, R.D.: Salicylic acid modulates arsenic toxicity by reducing its root to shoot translocation in rice (Oryza sativa L.). — Front. Plant Sci. 6: 340, 2015.

    PubMed  PubMed Central  Google Scholar 

  • Su, Y.H., McGrath, S.P., Zhu, Y.G., Zhao, F.J.: Highly efficient xylem transport of arsenite in the arsenic hyperaccumulator Pteris vittata. — New Phytol. 180: 434–441, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Tlustos, P., Szakova, J., Pavlikova, D., Balik, J., Hanc, A.: The accumulation of arsenic and cadmium by different species of vegetables. — In: Workshop Towards and Ecologically Sound Fertilisation in Field Vegetable Production 571: 217–224, 2000.

    Google Scholar 

  • Vickers, C.E., Possell, M., Cojocariu, C.I., Velikova, V.B., Laothawornkitkul, J., Ryan, A., Mullineaux, P.M., Hewitt, N.C.: Isoprene synthesis protects transgenic tobacco plants from oxidative stress. — Plant Cell Environ. 32: 520–531, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Waisberg, M., Joseph, P., Hale, B., Beyersmann, D.: Molecular and cellular mechanisms of cadmium carcinogenesis. — Toxicology 192: 95–117, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Xu, X.Y., McGrath, S.P., Zhao, F.J.: Rapid reduction of arsenate in the medium mediated by plant roots. — New Phytol. 176: 590–599, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Yang, Y.J., Cheng, L.M., Liu, Z.H.: Rapid effect of cadmium on lignin biosynthesis in soybean roots. — Plant Sci. 172: 632–639, 2007.

    Article  CAS  Google Scholar 

  • Zenk, M.H.: Heavy metal detoxification in higher plants. — Gene 179: 21–30, 1996.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, J., Cui, S., Li, J., Kirkham, M.B.: Protoplasmic factors, antioxidant responses and chilling resistance in maize. — Plant Physiol. Biochem. 33: 567–575, 1995.

    CAS  Google Scholar 

  • Zhao, F.J., Ma, J.F., Meharg, A.A., McGarth, S.P.: Arsenic uptake and metabolism in plants. — New Phytol. 181: 777–794, 2009.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. Pandey-Rai.

Additional information

Acknowledgements: The authors are thankful to the Council of Scientific and Industrial Research (CSIR-P-25/329) for financial support to carry this work. Authors acknowledge the Advanced Instrumentation Research Facility (AIRF), Jawaharlal Nehru University, New Delhi, for providing a GC-MS facility.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kumari, A., Pandey, N. & Pandey-Rai, S. Protection of Artemisia annua roots and leaves against oxidative stress induced by arsenic. Biol Plant 61, 367–377 (2017). https://doi.org/10.1007/s10535-016-0686-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10535-016-0686-3

Additional key words

Navigation