Cellular and signaling mechanisms supporting cadmium tolerance in salicylic acid treated seedlings

Authors

  • Aicha Belkadhi University of Tunis El Manar http://orcid.org/0000-0001-5911-0974
  • Wahbi Djebali University of Tunis El Manar
  • Hédia Hédiji University of Tunis El Manar
  • Wided Chaïbi University of Tunis El Manar

DOI:

https://doi.org/10.14719/pst.2016.3.1.180

Keywords:

cadmium tolerance, salicylic acid, intracellular chelation, extracellular chelation, signal transduction

Abstract

This review spotlights on recent indications that recognizes potential cellular mechanisms that may be involved in the tolerance of salicylic acid (SA)-treated seedlings to the presence of cadmium (Cd) in their environment. It appears probable that SA stimulates signaling systems implicated in plant defense-related actions against Cd-induced oxidative stress. These include mechanisms that reduce uptake of metals into the cytosol by extracellular chelation through extruded ligands and binding onto cell-wall constituents. Cellular chelation of metals in the cytosol by a range of ligands (peptides, phytochelatins (PCs)), or increased efflux from the cytosol out of the cell or into sequestering compartments are also key mechanisms improving tolerance. Free-radical scavenging capacities through the activity of antioxidant enzymes or production of peptides and PCs add another line of defense against the toxic effect of Cd. The SA signaling events can be attributed to the extracellular SA perception model in which reactions between SA and apoplastic proteins result in acute oxidative burst under Cd stress.

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Author Biography

Aicha Belkadhi, University of Tunis El Manar

In 2009, I obtained a Master`s degree in Environmental Physiology and Toxicology in the Department of Biology/Faculty of Science (University of Tunis El Manar, Tunisia). Then, in 2010-2011, I moved to Córdoba (Spain) and joined the Department of Agronomy and Plant Breeding (CSIC/Institute of Sustainable Agriculture; Prof Antonio De Haro) in a pre-doctoral training to study the flax and Brassica carinata response to abiotic stresses. The main goal was to understand how the plants adapt to environmental stresses in polluted soils (toxic metals). This knowledge was necessary to select tolerant species and help to develop strategies for improving tolerance of plants in contaminated areas. This work was further extended during another pre-doctoral fellowship at the Department of Plant Genetics in Pontevedra (CSIC/Misión Biológica de Galicia; Dr. María Elena Cartea). Major findings were the revelation of the role played by salicylic acid in membrane lipids during cadmium stress.  We have found that when grown in the presence of up to 100 µM CdCl2, salicylic acid is able to restrict cadmium transport from the roots to the leaves limiting its toxicity in the photosynthetic tissues. Salicylic acid-induced Changes in membrane lipid composition (glycolipids, phospholipids and neutral lipids), photosynthesis and antioxidant capacities have been also reported in contaminated plants.

 

      In 2011-2012, I moved toEdmonton(Canada) and started studying the mechanisms of transcription in plants in the Department of Biological Sciences/Faculty of Science (UniversityofAlberta, Prof Michael Deyholos). I have been trained in extraction, purification, and separation of proteins for proteomics, growth and stress treatment of plant samples, and gene expression studies. Since 2012, we still continue to study the role of the chloroplast 2-Cys peroxiredoxinBAS1 in the protection of flax against oxidative damages.

      In 2014, I obtained my Doctorate Degree in Biological Sciences.

References

Aranega-Bou, P., M. de la O Leyva, I. Finiti, P. García-Agustín, and C. González-Bosch. 2014. Priming of plant resistance by natural compounds. Hexanoic acid as a model. Frontiers in Plant Science 5: 488. doi: 10.3389/fpls.2014.00488. PMID: PMC4181288.

Armendariz, A.L., M.A. Talano, C. Travaglia, H. Reinoso, A.L. Wevar Oller, and E. Agostini. 2016. Arsenic toxicity in soybean seedlings and their attenuation mechanisms. Plant Physiology and Biochemistry 98: 119-127. doi: 10.1016/j.plaphy.2015.11.021. PMID: 26686284.

Atkinson, N.J., and P.E. Urwin. 2012. The interaction of plant biotic and abiotic stresses: from genes to the field. Journal of Experimental Botany 63: 3523–3543. doi: 10.1093/jxb/ers100. PMID: 22467407.

Belkadhi, A., H. Hediji, Z. Abbes, W. Djebali, and W. Chaïbi. 2012. Influence of salicylic acid pretreatment on cadmium tolerance and its relationship with non-protein thiol production in flax root. African Journal of Biotechnology 11 : 9788-9796. doi: 10.5897/AJB11.2051.

Belkadhi, A., A. De Haro, P. Soengas, S. Obregόn, M.E. Cartea, W. Djebali, and W. Chaïbi. 2013. Salicylic acid improves root antioxidant defense system and total antioxidant capacities of flax subjected to cadmium. OMICS : A Journal of Integrative Biology 17(7): 398-406. doi: 10.1089/omi.2013.0030. PMID: 23758477.

Belkadhi, A., A. De Haro, P. Soengas, S. Obregόn, M.E. Cartea, W. Chaϊbi, and W. Djebali. 2014. Salicylic acid increases tolerance to oxidative stress induced by hydrogen peroxide accumulation in leaves of cadmium-exposed flax (Linum usitatissimum L.). Journal of Plant Interactions 9(1): 647–654. doi: 10.1080/17429145.2014.890751.

Belkadhi A., A. De Haro, S. Obregon, W. Chaϊbi, and W. Djebali. 2015. Positive effects of salicylic acid pretreatment on the composition of flax plastidial membrane lipids under cadmium stress. Environmental Science and Pollution Research 22 (2): 1457-1467. doi: 10.1007/s11356-014-3475-6. PMID: 25163565.

Belkadhi A., A. De Haro, S. Obregon, W. Chaϊbi, and W. Djebali. 2015. Exogenous salicylic acid protects phospholipids against cadmium stress in flax (Linum usitatissimum L.). Ecotoxicology and Environmental Safety 120: 102-109. doi: 10.1016/j.ecoenv.2015.05.028. PMID: 26057076.

Belkhadi, A., H. Hediji, Z. Abbes, I. Nouairi, Z. Barhoumi, M. Zarrouk, W. Chaïbi, and W. Djebali. 2010. Effects of exogenous salicylic acid pre-treatment on cadmium toxicity and leaf lipid content in Linum usitatissimum L. Ecotoxicology and Environmental Safety 73: 1004-1011. doi: 10.1016/j.ecoenv.2010.03.009. PMID: 20399499.

Brunetti, P., L. Zanella, A. Proia, A. De Paolis, G. Falasca, M.M. Altamura, L. Sanita‘ di Toppi, P. Costantino, and M. Cardarelli. 2011. Cadmium tolerance and phytochelatin content of Arabidopsis seedlings over-expressing the phytochelatin synthase gene AtPCS1. Journal of Experimental Botany 62: 5509–5519. doi: 10.1093/jxb/err228. PMID: 21841172.

Brunetti, P., L. Zanella, A. De Paolis, D. Di Litta, V. Cecchetti, G. Falasca, M. Barbieri, M.M. Altamura, P. Costantino, M. Cardarelli. 2015. Cadmium-inducible expression of the ABC-type transporter AtABCC3 increases phytochelatin-mediated cadmium tolerance in Arabidopsis. Journal of Experimental Botany 66: 3815–3829. doi: 10.1093/jxb/erv185. PMID: 25900618.

Choudhury, S., and S.K. Panda. 2004. Role of salicylic acid in regulating cadmium induced oxidative stress in Oryza sativa L. roots. Bulgarian Journal of Plant Physiology 30: 95–110.

Clemens, S. 2006. Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88: 1707-1719. doi:10.1016/j.biochi.2006.07.003. PMID: 16914250.

Cosio, C., E. Martinoia, C. Keller. 2004. Hyperaccumulation of cadmium and zinc in Thlaspi caerulescens and Arabidopsis halleri at the leaf cellular level. Plant Physiology 134: 716–725. doi: 10.1104/pp.103.031948. PMID: 14730081.

Djebali, W., W. Chaibi, and M.H. Ghorbel. 2002. Croissance, activité peroxydasique et modifications ultrastructurales induites par le cadmium dans la racine de tomate. Canadian Journal of Botany 80 : 942-953. doi: 10.1055/s-2005-837696.

Djebali , W., M. Zarrouk, R. Brouquisse, S. El Kahoui, F. Liman, M.H. Ghorbel, and W. Chaïbi. 2005. Ultrastructure and lipid alterations induced by cadmium in tomato Lycopersicon esculentum chloroplast membranes. Plant Biology 7: 258–368. doi: 10.1055/s-2005-837696. PMID: 16025408.

Eichhorn, H., M. Klinghammer, P. Becht and R. Tenhaken. 2006. Isolation of a novel ABC-transporter gene from soybean induced by salicylic acid. Journal of Experimental Botany 57: 2193-2201. doi:10.1093/jxb/erj179. PMID: 16720608.

Freeman, J. L., M.W. Persans, K. Nieman, C. Albrecht, W. Peer, I.J. Pickering, and D.E. Salt. 2004. Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Cell 16: 2176–2191. doi: 10.1105/tpc.104.023036. PMID: 15269333.

Freeman, J. L., D. Garcia, D. Kim, A. Hopf, and D.E. Salt. 2005. Constitutively elevated salicylic acid signals glutathione-mediated nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Physiology 137: 1082-1091. doi: 10.1104/pp.104.055293. PMID: 15734913.

Guo, B., Y.C. Liang, Y.G. Zhu, and F.J. Zhao. 2007. Role of salicylic acid in alleviating oxidative damage in rice roots (Oryza sativa) subjected to cadmium stress. Environmental Pollution 147: 743–749. doi:10.1016/j.envpol.2006.09.007. PMID: 17084493.

Hall, J.L. 2002. Cellular mechanisms for heavy metal detoxification and tolerance. Journal of Experimental Botany 53: 1–11. doi: 10.1093/jexbot/53.366.1. PMID: 11741035.

Hall, J.L., and L.E. Williams. 2003. Transition metal transporters in plants. Journal of Experimental Botany 54: 2601–2613. doi: 10.1093/jxb/erg303. PMID:14585824.

Kang, J., J. Park, H. Choi, B. Burla, T. Kretzschmar, Y. Lee, and E. Martinoia. 2011. Plant ABC transporters. Arabidopsis Book 9: e0153 10.1199. doi: 10.1199/tab.0153. PMID: 3268509.

Kawano, T., and F. Bouteau. 2013. Crosstalk between intracellular and extracellular salicylic acid signaling events leading to long-distance spread of signals. Plant Cell Reports 32: 1125–1138. doi: 10.1007/s00299-013-1451-0. PMID: 23689257.

Kim D.Y., L. Bovet, M. Maeshima, E. Martinoia, Y. Lee. 2007. The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. Plant Journal 50: 207–218. doi: 10.1111/j.1365-313X.2007.03044.x. PMID: 17355438.

Knörzer, O. C., B. Lederer, J. Durner, and P. Böger. 1999. Antioxidative defense activation in soybean cells. Physiologia Plantarum 107: 294-302. doi: 10.1034/j.1399-3054.1999.100306.x.

Li, X., L. Ma, N. Bu, Y. Li, and L. Zhang. 2014. Effects of salicylic acid pre-treatment on cadmium and/or UV-B stress in soybean seedlings. Biologia Plantarum 58: 195-199. doi: 10.1007/s10535-013-0375-4.

Ma, J. F., N. Yamaji, N. Mitani, X.Y. Xu, Y.H. Su, S.P. McGrath, and F.J. Zhao. 2008. Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proceedings of the National Academy of Sciences U.S.A. 105: 9931–993510. doi: 10.1073/pnas.0802361105. PMID: 18626020.

Metwally A., I. Finkemeier, M. Georgi, and K.J. Dietz. 2003. Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiology 132: 272-281. doi: 10.​1104/​pp.​102.​018457. PMID: 12746532.

Mishra S., G. Wellenreuther, J. Mattusch, H.J. Stärk, and H. Küpper. 2013. Speciation and distribution of arsenic in the nonhyperaccumulator macrophyte Ceratophyllum demersum. Plant Physiology 163: 1396–1408. doi: 10.1104/pp.113.224303. PMID: 24058164.

Moussa, H.R., and S.M. EL-Gamal. 2010. Effect of salicylic acid pretreatment on cadmium toxicity in wheat. Biologia Plantarum 54: 315-320. doi: 10.1007/s10535-010-0054-7.

Noctor, G., A. Mhamdi, S. Chaouch, Y. Han, J. Neukermans, B. Marquez-Garcia, G. Queval, and C.H. Foyer. 2012. Glutathione in plants: an integrated overview. Plant, Cell and Environment 35: 454–484. doi: 10.1111/j.1365-3040.2011.02400.x. PMID: 21777251.

Oota, Y. 1975. Short-day flowering of Lamma gibba G3 induced by salicylic acid. Plant Cell Physiology 16: 1131-1135. doi: 10.12692/ijb/5.9.237-243.

Ortiz, D.F., T. Ruscitti, K.F. McCue, and D.W. Ow. 1995. Transport of metal-binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein. Journal of Biological Chemistry 270: 4721–4728. doi: 10.1074/jbc.270.9.4721. PMID: 7876244.

Pál, M., G. Szalai, E. Horváth, T. Janda, and E. Páldi. 2002. Effect of salicylic acid during heavy metal stress. Acta Biologica Szegediensis 46: 119-120. Perrin, D. D. 1958. Stability of Metal Complexes with Salicylic Acid and Related Substances. Nature 182 : 741 - 742. doi: 10.1038/182741a0. PMID: 13590098.

Rao, V.M., M.P. Latha, T.S. Rao, and G.N. Rao. 2006. Mixed ligand complexes of toxic metal ions with L-glutamic acid and L-methionine in urea-water mixtures. Chemical Speciation and Bioavailability 18: 143. doi: 10.1080/09542299.2006.11073749.

Szalai, G., A. Krantev, R. Yordanova, L.P. Popova, and T. Janda. 2013. Influence of salicylic acid on phytochelatin synthesis in Zea mays during Cd stress. Turkish Journal of Botany 37: 708–714. doi: 10.3906/bot-1210-6.

Singh, A.P., G. Dixit, S. Mishra, S. Dwivedi, M. Tiwari, S. Mallick, V. Pandey, P.K. Trivedi, D. Chakrabarty, R.D. Tripathi. 2015. Salicylic acid modulates arsenic toxicity by reducing its root to shoot translocation in rice (Oryza sativa L.). Frontiers in Plant Science 6 : 340. doi: 10.3389/fpls.2015.00340. PMID: 26042132.

Srivastava, A. K., S. Srivastava, S. Mishra, S.F. D’Souza, and P. Suprasanna. 2014. Identification of redox-regulated components of arsenate (AsV) tolerance through thiourea supplementation in rice. Metallomics 6: 1718–1730. doi: 10.1039/c4mt00039k. PMID: 25008039.

Williams, L.E., J.K. Pittman, and J.L. Hall. 2000. Emerging mechanisms for heavy metal transport in plants. Biochimica et Biophysica Acta 1465: 104-126. doi: 10.1016/S0005-2736(00)00133-4. PMID: 10748249.

Xu, L. L., Z.Y. Fan, Y.J. Dong, J. Kong, and X.Y. Bai. 2015. Effects of exogenous salicylic acid and nitric oxide on physiological characteristics of two peanut cultivars under cadmium stress. Biologia Plantarum 59: 171-182. doi: 10.​1007/​s10535-014-0475-9.

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Published

18-02-2016

How to Cite

1.
Belkadhi A, Djebali W, Hédiji H, Chaïbi W. Cellular and signaling mechanisms supporting cadmium tolerance in salicylic acid treated seedlings. Plant Sci. Today [Internet]. 2016 Feb. 18 [cited 2024 Nov. 21];3(1):41-7. Available from: https://horizonepublishing.com/journals/index.php/PST/article/view/180

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