Biologia Plantarum 63: 43-53, 2019 | DOI: 10.32615/bp.2019.006

Effects of short-term arsenic exposure in Arabidopsis thaliana: tolerance versus toxicity responses

A. Pita-Barbosa1,*, T.C.R. Williams2, M.E. Loureiro1,3
1 Plant Biology Department, Federal University of Viçosa – Peter Henry Rolfs, 36570-000, Viçosa, Minas Gerais, Brazil
2 Botany Department, University of Brasília – Asa Norte, 70910-900, Brasilia, Federal District, Brazil
3 Institute of Humanities, Arts and Sciences Paulo Freire – Joana Angélica, 45988-058, Teixeira de Freitas, Bahia, Brazil

The metalloid arsenic (As) is highly phytotoxic, in part due to the similarity of the arsenates to phosphates, but also due to its ability to induce reactive oxygen species (ROS) formation, and in the form of arsenite directly interact with certain enzymes. Here we aimed to determine the effects of a short period of As exposure on Arabidopsis thaliana. Particular focus was given to shoot responses, which have received less attention in previous studies. A. thaliana (ecotype Col-0) plants (28-d-old) were cultivated hydroponically in the presence of 0, 27, 108, and 216 µM arsenic in the form of sodium arsenate for five days. Translocation of As from root to shoot increased with increasing As concentration in the medium and caused a reduction in growth. Photosynthesis was severely affected due to stomatal closure, increased ROS accumulation, and alterations in expression of genes involved in oxidative stress responses and As detoxification. Primary metabolism was also perturbed, suggesting both the direct inhibition of certain enzymes as well as active defensive responses. Overall the effects of As toxicity depended greatly on the degree of translocation from root to shoot and involved both direct effects on biological processes and secondary effects caused by the accumulation of ROS.

Keywords: arsenate, gene expression, leaf anatomy, metabolic profile, oxidative stress, photosynthesis

Accepted: November 13, 2018; Prepublished online: November 14, 2018; Published online: January 19, 2019Show citation

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Pita-Barbosa, A., Williams, T.C.R., & Loureiro, M.E. (2019). Effects of short-term arsenic exposure in Arabidopsis thaliana: tolerance versus toxicity responses. Biologia plantarum, 63, 43-53. doi: 10.32615/bp.2019.006.
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    References

    1. Araújo, W.L., Ishizaki, K., Nunes-Nesi, A., Larson, T.R., Tohge, T., Kranert I., Witt, S., Obata, T., Schauer, N., Graham I.A., Leaver, C.J., Fernie, A.R.: Identification of the 2-hydroxyglutarate and isovaleryl-CoA dehydrogenases as alternative electron donors linking lysine catabolism to the electron transport chain of Arabidopsis mitochondria. - Plant Cell 22: 1549-1563, 2010. Go to original source...
    2. Bienert, G.P., Moller, A.L.B., Kristiansen, K.A., Schulz, A., Moller, I.M., Schjoerring, J.K., Jahn, T.P.: Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. - J. biol. Chem. 282: 1183-1192, 2006.
    3. Bleeker, P.M., Hakvoort, H.W.J., Bliek, M., Souer, E., Schat, H.: Enhanced arsenate reduction by CDC25-like tyrosine phosphatase explains increased phytochelation accumulation in arsenate-tolerant Holcus lanatus. - Plant J. 45: 917-929, 2006. Go to original source...
    4. Borba, R.P., Figueiredo, B.R., Rawlins, B., Matschullat, J.: Geochemical distribution of arsenic in waters, sediments and weathered gold mineralized rocks from Iron Quadrangle, Brazil. - Environ. Geol. 44: 39-52, 2003. Go to original source...
    5. Campos, N.V., Loureiro, M.E., Azevedo, A.A.: Differences in phosphorus translocation contributes to differential arsenic tolerance between plants of Borreria verticillata (Rubiaceae) from mine and non-mine sites. - Environ. Sci. Pollut. Res. Int. 21: 5586-5596, 2014. Go to original source...
    6. Cao, X., Ma, L.Q., Tu, C.: Antioxidative responses to arsenic in the arsenic-hyperaccumulator Chinese brake fern (Pteris vittata L.). - Environ. Pollut. 128: 317-325, 2004. Go to original source...
    7. Castrillo, G., Sánchez-Bermejo, E., De Lorenzo, L., Crevillén, P., Fraile-Escanciano, A., Mohan, T.C., Mouriz, A., Catarecha, P., Sobrino-Plata, J., Olsson, S., Del Puerto, Y.L., Mateos, I., Rojo, E., Hernández, L.E., Jarillo, J.A., Piñero, M., Paz-Ares, J., Leyva, A.: WRKY6 transcription factor restricts arsenate uptake and transposon activation in Arabidopsis. - Plant Cell 25: 2944-2957, 2013. Go to original source...
    8. Catarecha, P., Segura, M.D., Franco-Zorrilla, J.M., García-Ponde, B., Lanza, M., Solano, R., Paz-Ares, J., Leyva, A.: A mutant of the Arabidopsis phosphate transporter PHT1;1 displays enhanced arsenic accumulation. - Plant Cell 19: 1123-1133, 2007. Go to original source...
    9. Chao, D.Y., Chen, Y., Chen, J., Shi, S., Chen, Z., Wang, C., Danku, J., Zhao, F.J., Salt, D.: Genome-wide association mapping identifies a new arsenate reductase critical for limiting arsenic accumulation in plants. - PLoS Biol. 12: e1002009, 2014. Go to original source...
    10. Chen, W., Taylor, N.L., Chi, Y., Millar, A.H., Lambers, H., Finnegan, P.M.: The metabolic acclimation of Arabidopsis thaliana to arsenate is sensitized by the loss of mitochondrial lipoamide dehydrogenase2, a key enzyme in oxidative metabolism. - Plant Cell Environ. 37: 684-695, 2014. Go to original source...
    11. Clarck, G.T., Dunlop, J., Phung, H.T.: Phosphate absorption by Arabidopsis thaliana. - Aust. J. Plant Physiol. 27: 959-965, 2000.
    12. Clark, R.B.: Nutrient solution growth of sorghum and corn in mineral nutrition studies. - J. Plant Nutr. 5: 1039-1057, 1982. Go to original source...
    13. Costa, J.M., Grant, O.M., Chaves, M.M.: Thermography to explore plant-environment interactions. - J. exp. Bot. 64: 3937-3949, 2013. Go to original source...
    14. Del Pozo, O., Lam, E.: Caspases and programmed cell death in the hypersensitive response of plants to pathogens. - Curr. Biol. 3: 1129-1132, 1998. Go to original source...
    15. Downey, L.A., Miller, J.W.: Rapid measurements of relative turgidity in maize (Zea mays L.). - New Phytol. 70: 555-560, 1971. Go to original source...
    16. Fenton, H.J.H.: Oxidation of tartaric acid in presence of iron. - J. chem. Soc. 65: 899-910, 1984.
    17. Figueiredo, B.R., Borba, R.P., Angélica, R.S.: Arsenic occurrence in Brazil and human exposure. - Environ. Geochem. Health 29: 109-118, 2007. Go to original source...
    18. Finnegan, P.M., Chen, W.: Arsenic toxicity: the effects on plant metabolism. - Front. Physiol. 3:1-18, 2012. Go to original source...
    19. Garraway, M.O., Akhtar, M., Wokoma, E.C.W.: Effect of high temperature stress on peroxidase activity and electrolyte leakage in maize in relation to sporulation of Bipolaris maydis race T. - Phytopathology 79: 800-805, 1989. Go to original source...
    20. Gunes, A., Pilbeam, D.J., Inal, A.: Effect of arsenic-phosphorus interaction on arsenic-induced oxidative stress in chickpea plants. - Plant Soil 314: 211-220, 2009. Go to original source...
    21. Hodges, D.M., DeLong, J.M., Forney, C.F., Prange, R.K.: Improving the thiobabituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. - Planta 207: 604-611, 1999. Go to original source...
    22. Hughes, M.F.: Arsenic toxicity and potential mechanisms of action. - Toxicol. Lett. 133: 1-16, 2002. Go to original source...
    23. Irtelli, B., Navari-Izzo, F.: Uptake kinetics of different arsenic species by Brassica carinata. - Plant Soil 303: 105-113, 2008. Go to original source...
    24. Karnovsky, M.J.: A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. - J. cell. Biol. 27: 1A-149A, 1965.
    25. Kumar, S., Asif, M.H., Chakrabarty, D., Tripathi, R.D., Dubey, R.S., Trivedi, P.K.: Expression of a rice Lambda class of glutathione S-transferase, OsGSTL2, in Arabidopsis provides tolerance to heavy metal and other abiotic stresses. - J. Hazard Mater. 248-249: 228-237, 2013. Go to original source...
    26. Lazova, G.N., Naidenova, T., Velinova, K.: Carbonic anhydrase activity and photosynthetic rate in the tree species Paulownia tomentosa Steud. Effect of dimethylsulfoxide treatment and zinc accumulation in leaves. - J. Plant Physiol. 161: 295-301, 2004. Go to original source...
    27. Li, W.X., Chen, T.B., Huang, Z.C., Lei, M., Liao, X.Y.: Effect of arsenic on chloroplast ultrastructure and cadmium distribution in arsenic hyperaccumulator Pteris vittata L. - Chemosphere 62: 803-809, 2006. Go to original source...
    28. Lisec, J., Schauner, N., Kopka, J., Willmitzer, L., Fernie, A.R.: Gas chromatography mass spectrometry-based metabolite profiling in plants. - Nat. Protoc. 1: 387-396, 2006. Go to original source...
    29. Livak, K.J., Schmittgen, T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2-CT method. - Methods 25: 402-408, 2001. Go to original source...
    30. Lommen, A.: MetAlign: interface-driven, versatile metabolomics tool for hyphenated full-scan mass spectrometry data preprocessing. - Anal. Chem. 15: 3079-3086, 2009. Go to original source...
    31. Ma, Z., Bielenberg D.G., Brown K.M., Lynch J.P.: 2001. Regulation of root hair density by phosphorus availability in Arabidopsis thaliana. - Plant Cell Environ. 24: 459-467, 2001. Go to original source...
    32. Martinez, V.D., Vucic, E.A., Lam, S., Lam, W.L.: Emerging arsenic threat in Canada. - Science 342: 559, 2013. Go to original source...
    33. Murata, N., Takahashi, S., Nishiyama, Y., Allakhverdiev, S.I.: Photoinhibition of photosystem II under environmental stress. - BBA Bioenergetics 1767: 414-421, 2007. Go to original source...
    34. Murray, J.R., Hackett, W.P.: Dihydroflavonol reductase activity in relation to differential anthocyanin accumulation in juvenile and mature phase Hedera helix L. - Plant Physiol. 97: 343-351, 1991. Go to original source...
    35. Nicholson, D.W., Ali, A., Thornberry, N.A., Vaillancourt, J.P., Ding, C.K., Gallant, M., Gareau, Y., Griffin, P.R., Labelle, M., Lazebnik, Y.A.: Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. - Nature 376: 37-43, 1995. Go to original source...
    36. Norén, H., Svensson, P., Andersson, B.: A convenient and versatile hydroponic cultivation system for Arabidopsis thaliana. - Physiol. Plant. 121: 343-348, 2004. Go to original source...
    37. O'Toole, J.C., Cruz, R.T.: Response of leaf water potential, stomatal resistance, and leaf rolling to water stress. - Plant Physiol. 65: 428-432, 1980. Go to original source...
    38. Pita-Barbosa, A., Gonçalves, E.C., Azevedo, A.A.: Morpho-anatomical and growth alterations induced by arsenic in Cajanus cajan (L.) DC (Fabaceae). - Environ. Sci. Pollut. Res. Int. 22: 11265-11274, 2015. Go to original source...
    39. Plas, D.R., Thompson, C.B.: Cell metabolism in the regulation of programmed cell death. - Trends Endocrinol. Metabol. 13: 75-78, 2002. Go to original source...
    40. Ramel, F., Sulmon, C., Bogard, M., Couée, I., Gouesbet, G.: Differential patterns of reactive oxygen species and antioxidative mechanisms during atrazine injury and sucrose-induced tolerance in Arabidopsis thaliana plantlets. - BMC Plant Biol. 9: 28-46, 2009. Go to original source...
    41. Rejeb, K.B., Abdelly, C., Savouré, A.: How reactive oxygen species and proline face stress together. - Plant Physiol. Biochem. 80: 278-284, 2014. Go to original source...
    42. Rodríguez-Lado, L., Sun, G., Berg, M., Zhang, Q., Xue, H., Zheng, Q., Johnson, C.A.: Groundwater arsenic contamination throughout China. - Science 341: 866-868, 2013. Go to original source...
    43. Sánchez-Bermejo, E., Castrillo, G., del Llano, B., Navarro, C., Zarco-Fernández, S., Martinez-Herrera, D.J., Puerto, Y.L., Muñoz, R., Cámara, C., Paz-Ares, J., Alonso-Blanco, C., Leyva, A.: Natural variation in arsenate tolerance identifies an arsenate reductase in Arabidopsis thaliana. - Nat. Commun. 5: 4617-4625, 2014. Go to original source...
    44. Sánchez-Viveiros, G., Ferrera-Cerrato, R., Alarcón, A.: Short-term effects of arsenate-induced toxicity on growth, chlorophyll and carotenoid contents, and total content of phenolic compounds of Azolla filiculoides. - Water Air Soil Pollut. 217: 455-462, 2011. Go to original source...
    45. Sasaki, H., Hirose, T., Watanabe, Y., Ohsugi, R.: Carbonic anhydrase activity and CO2-transfer resistance in Zn-deficient rice leaves. - Plant Physiol. 118: 929-934, 1998. Go to original source...
    46. Schulz, H., Härtling, S., Tanneberg, H.: The identification of arsenic-induced phytochelatins - comparison between plants with varying As sensitivities. - Plant Soil 303: 275-287, 2008. Go to original source...
    47. Shaibur, M.R., Kitajima, N., Sugawara, R., Kondo, T., Alam, S., Huq, S.M.I., Kawai, S.: Critical toxicity level of arsenic and elemental composition of arsenic-induced chlorosis in hydroponic sorghum. - Water Air Soil Pollut. 191: 279-292, 2008. Go to original source...
    48. Shi, Y., Ruan, J., Ma, I., Han, W., Wang, F.: Accumulation and distribution of arsenic and cadmium by tea plants. - J. Zhejiang Univ. Sci. B 9: 265-270, 2008. Go to original source...
    49. Singh, H.P., Batish, D.R., Kohli, R.K., Arora, K.: Arsenic-induced root growth inhibition in mung bean (Phaseolus aureus Roxb.) is due to oxidative stress resulting from enhanced lipid peroxidation. - Plant Growth Regul. 53: 65-73, 2007. Go to original source...
    50. Slesak, I., Libik, M., Karpinska, B., Karpinski, S., Miszalski.: The role of hydrogen peroxide in regulation of plant metabolism and cellular signalling in response to environmental stresses. - Acta Biochim. Polon. 54: 39-50, 2007.
    51. Stoeva, N., Berova, M., Zlatez, Z.: Physiological response of maize to arsenic contamination. - Biol. Plant. 47: 449-452, 2004. Go to original source...
    52. Tedesco, M.J., Gianello, C., Bissani, C.A., Bohnen, H., Volkweiss, S.J. (ed): Análise de solo, plantas e outros materiais. [title in English], - UFRGS: Porto Alegre, 1995. [in Span.]
    53. Trethewey, R.N., Geigenberger, P., Riedel, K., Riesmeier, J.W., Willmitzer, L.: Combined expression of glucokinase and invertase in potato tubers leads to a dramatic reduction in starch accumulation and a stimulation of glycolysis. - Plant J. 15: 109-118, 1998. Go to original source...
    54. Tripathi, R.D., Srivastava, S., Mishra, S., Singh, N., Tuli, R., Gupta, D.K., Maathuis, F.J.M.: Arsenic hazards: strategies for tolerance and remediation by plants. - Trends Biotechnol. 25: 158-165, 2007. Go to original source...
    55. Verbruggen, N., Hermans, C., Schat, H.: Mechanisms to cope with arsenic or cadmium excess in plants. - Curr. Opin. Plant Biol. 12: 364-372, 2009. Go to original source...
    56. Vishwakarma, A., Tetali, SD., Selinski, J., Scheibe, R., Padmasree, K.: Importance of the alternative oxidase (AOX) pathway in regulating cellular redox and ROS homeostasis to optimize photosynthesis during restriction of the cytochrome oxidase pathway in Arabidopsis thaliana. - Ann. Bot. 116: 555-569, 2015. Go to original source...
    57. Wang, X., Tian, W., Li, W.: Development of an efficient protocol of RNA isolation from recalcitrant tree tissues. - Mol. Biotechnol. 38: 57-64, 2008. Go to original source...
    58. Wang, C., Na, G., Bermejo, E.S., Chen, Y., Banks, J.A., Salt, D.E., Zhao, F.J.: Dissecting the components controlling root-to-shoot arsenic translocation in Arabidopsis thaliana. - New Phytol. 217: 206-218, 2018. Go to original source...
    59. Zabludowska, E., Kowalska, J., Jedynak, L., Wojas, S., Sklodowska, A., Antosiewicz, D.M.: Search for a plant phytoremediation - what can we learn from field and hydroponic studies? - Chemosphere 77: 301-107, 2009. Go to original source...
    60. Zhao, S., Fernald, R.D. Comprehensive algorithm for quantitative real-time polymerase chain reaction. - J. comput. Biol. 12: 1047-1064, 2005. Go to original source...

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