Plant Soil Environ., 2022, 68(5):213-222 | DOI: 10.17221/65/2022-PSE

Arsenic-induced response in roots of arsenic-hyperaccumulator fern and soil enzymatic activity changesOriginal Paper

Veronika Zemanová1,2, Daniela Pavlíková1, Milan Novák1, Petre I. Dobrev3, Tomáš Matoušek4, Václav Motyka3, Milan Pavlík ORCID...*,1,2
1 Department of Agro-Environmental Chemistry and Plant Nutrition, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Prague, Czech Republic
2 Isotope Laboratory, Institute of Experimental Botany of the Czech Academy of Sciences, Prague, Czech Republic
3 Laboratory of Hormonal Regulations in Plants, Institute of Experimental Botany of the Czech Academy of Sciences, Prague, Czech Republic
4 Department of Trace Element Analysis, Institute of Analytical Chemistry of the Czech Academy of Sciences, Brno, Czech Republic

In a pot experiment, arsenic-hyperaccumulating Pteris cretica cv. Albo-lineata plant ferns were cultivated and exposed to low and high doses of arsenate (20 and 100 mg As/kg, respectively) for six months. Physiological and morphological changes of roots, as well as changes in soil quality of the root zone and bulk soil (water-soluble fraction of elements and activity of soil enzymes), were determined. The results showed that the accumulation of inorganic As, mainly in the form of As3+, did not significantly affect the yield of roots, but caused changes in root morphology (deformation of root cell walls due to lignification) and metabolism (decrease of auxin indole-3-acetic acid and 2-oxoindole-3-acetic acid contents). Although the soil quality results varied according to the As dose, there was a clear difference between the root zone and the bulk soil. The activities of enzymes in the root zone were greater that those in the bulk soil. The results showed a significant influence of the high dose of As (100 mg As/kg), which decreased the activity of arylsulfatase, nitrate reductase, and urease in the root zone, while a decrease in acid phosphatase and nitrate reductase was observed in the bulk soil. The water-soluble fractions of As, organic nitrogen, nitrate nitrogen and organic carbon were significantly affected by the high dose of As.

Keywords: phytohormone; contamination; manganese; metalloid; risk, toxic element

Published: May 15, 2022  Show citation

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Zemanová V, Pavlíková D, Novák M, Dobrev PI, Matoušek T, Motyka V, Pavlík M. Arsenic-induced response in roots of arsenic-hyperaccumulator fern and soil enzymatic activity changes. Plant Soil Environ.. 2022;68(5):213-222. doi: 10.17221/65/2022-PSE.
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References

  1. Abbas G., Murtaza B., Bibi I., Shahid M., Niazi N.K., Khan M.I., Amjad M., Hussain M., Natasha (2018): Arsenic uptake, toxicity, detoxification, and speciation in plants: physiological, biochemical, and molecular aspects. International Journal of Environmental Research and Public Health, 15: 59. Go to original source... Go to PubMed...
  2. Abou-Shanab R.A.I., Mathai P.P., Santelli C., Sadowsky M.J. (2020): Indigenous soil bacteria and the hyperaccumulator Pteris vittata mediate phytoremediation of soil contaminated with arsenic species. Ecotoxicology and Environmental Safety, 195: 110458. Go to original source... Go to PubMed...
  3. Ali S., Tyagi A., Mushtaq M., Al-Mahmoudi H., Bae H.H. (2022): Harnessing plant microbiome for mitigating arsenic toxicity in sustainable agriculture. Environmental Pollution, 300: 118940. Go to original source... Go to PubMed...
  4. Aponte H., Meli P., Butler B., Paolini J., Matus F., Merino C., Cornejo P., Kuzyakov Y. (2020): Meta-analysis of heavy metal effects on soil enzyme activities. Science of The Total Environment, 737: 139744. Go to original source... Go to PubMed...
  5. Balík J., Pavlíková D., Vaněk V., Kulhánek M., Kotková B. (2007): The influence of long-term sewage sludge application on the activity of phosphatases in the rhizosphere of plants. Plant, Soil and Environment, 53: 375-381. Go to original source...
  6. Bertin C., Yang X.H., Weston L.A. (2003): The role of root exudates and allelochemicals in the rhizosphere. Plant and Soil, 256: 67-83. Go to original source...
  7. Bhattacharyya P., Tripathy S., Kim K.J., Kim S.-H. (2008): Arsenic fractions and enzyme activities in arsenic-contaminated soils by groundwater irrigation in West Bengal. Ecotoxicology and Environmental Safety, 71: 149-156. Go to original source... Go to PubMed...
  8. Broadley M., Brown P., Cakmak I., Rengel Z., Zhao F. (2012): Function of nutrients: micronutrients. In: Marschner P. (ed.): Marschner's Mineral Nutrition of Higher Plants. 3rd Edition. Cambridge, Academic Press, 191-248. ISBN: 978-0-12-384905-2 Go to original source...
  9. Chen Y.S., Fu J.W., Han Y.H., Rathinasabapathi B., Ma L.Q. (2016): High As exposure induced substantial arsenite efflux in As-hyperaccumulator Pteris vittata. Chemosphere, 144: 2189-2194. Go to original source... Go to PubMed...
  10. Cosio C., Dunand C. (2009): Specific functions of individual class III peroxidase genes. Journal of Experimental Botany, 60: 391-408. Go to original source... Go to PubMed...
  11. Das S., Chou M.L., Jean J.S., Yang H.J., Kim P.J. (2017): Arsenicenrichment enhanced root exudates and altered rhizosphere microbial communities and activities in hyperaccumulator Pteris vittata. Journal of Hazardous Materials, 325: 279-287. Go to original source... Go to PubMed...
  12. Duan G.L., Zhu Y.G., Tong Y.P., Cai C., Kneer R. (2005): Characterization of arsenate reductase in the extract of roots and fronds of Chinese brake fern, an arsenic hyperaccumulator. Plant Physiology, 138: 461-469. Go to original source... Go to PubMed...
  13. Kandeler E., Poll C., Frankenberger W.T., Tabatabai M.A. (2011): Nitrogen cycle enzymes. In: Dick R.P. (ed.): Methods of Soil Enzymology. Soil Science Society of America Book Series, 9. Madison, Soil Science Society of America, 211-245. ISBN: 9780-891-18854-4 Go to original source...
  14. Kidwai M., Dhar Y.V., Gautam N., Tiwari M., Ahmad I.Z., Asif M.H., Chakrabarty D. (2019): Oryza sativa class III peroxidase (OsPRX38) overexpression in Arabidopsis thaliana reduces arsenic accumulation due to apoplastic lignification. Journal of Hazardous Materials, 362: 383-393. Go to original source... Go to PubMed...
  15. Kiselev K.V., Tyunin A.P., Karetin Y.A. (2015): Salicylic acid induces alterations in the methylation pattern of the VaSTS1, VaSTS2, and VaSTS10 genes in Vitis amurensis Rupr. cell cultures. Plant Cell Reports, 34: 311-320. Go to original source... Go to PubMed...
  16. Kotková B., Balík J., Černý J., Kulhánek M., Bazalová M. (2008): Crop influence on mobile sulphur content and arylsulphatase activity in the plant rhizosphere. Plant, Soil and Environment, 54: 100-107. Go to original source...
  17. Krishnamurthy A., Rathinasabapathi B. (2013): Auxin and its transport play a role in plant tolerance to arsenite-induced oxidative stress in Arabidopsis thaliana. Plant, Cell and Environment, 36: 1838-1849. Go to original source... Go to PubMed...
  18. Lyubun Y.V., Pleshakova E.V., Mkandawire M., Turkovskaya O.V. (2013): Diverse effects of arsenic on selected enzyme activities in soil-plant-microbe interactions. Journal of Hazardous Materials, 262: 685-690. Go to original source... Go to PubMed...
  19. Ma L.Q., Komar K.M., Tu C., Zhang W.H., Cai Y., Kennelley E.D. (2001): A fern that hyperaccumulates arsenic. Nature, 409: 579. Go to original source... Go to PubMed...
  20. MacLachlan G.A., Waygood E.R. (1956): Catalysis of indoleacetic acid oxidation by manganic ions. Physiologia Plantarum, 9: 321-330. Go to original source...
  21. Magidin M., Pittman J.K., Hirschi K.D., Bartel B. (2003): ILR2, a novel gene regulating IAA conjugate sensitivity and metal transport in Arabidopsis thaliana. Plant Journal, 35: 523-534. Go to original source... Go to PubMed...
  22. Mondal S., Pramanik K., Ghosh S.K., Pal P., Ghosh P.K., Ghosh A., Maiti T.K. (2022): Molecular insight into arsenic uptake, transport, phytotoxicity, and defense responses in plants: a critical review. Planta, 255: 87. Go to original source... Go to PubMed...
  23. Pavlíková D., Zemanová V., Pavlík M., Dobrev P.I., Hnilička F., Motyka V. (2020): Response of cytokinins and nitrogen metabolism in the fronds of Pteris sp. under arsenic stress. PLoS One, 15: e0233055. Go to original source... Go to PubMed...
  24. Piacentini D., Rovere F.D., Sofo A., Fattorini L., Falasca G., Altamura M.M. (2020): Nitric oxide cooperates with auxin to mitigate the alterations in the root system caused by cadmium and arsenic. Frontiers in Plant Science, 11: 1182. Go to original source... Go to PubMed...
  25. Popov M., Zemanová V., Sácký J., Pavlík M., Leonhardt T., Matoušek T., Kaňa A., Pavlíková D., Kotrba P. (2021): Arsenic accumulation and speciation in two cultivars of Pteris cretica L. and characterization of arsenate reductase PcACR2 and arsenite transporter PcACR3 genes in the hyperaccumulating cv. Albo-lineata. Ecotoxicology and Environmental Safety, 216: 112196. Go to original source... Go to PubMed...
  26. Savitsky P.A., Gazaryan I.G., Tishkov V.I., Lagrimini L.M., Ruzgas T., Gorton L. (1999): Oxidation of indole-3-acetic acid by dioxygen catalysed by plant peroxidases: specificity for the enzyme structure. Biochemical Journal, 340: 579-583. Go to original source...
  27. Singh N., Ma L.Q., Vu J.C., Raj A. (2009): Effects of arsenic on nitrate metabolism in arsenic hyperaccumulating and non-hyperaccumulating ferns. Environmental Pollution, 157: 2300-2305. Go to original source... Go to PubMed...
  28. Smalla K., Wieland G., Buchner A., Zock A., Parzy J., Kaiser S., Roskot N., Heuer H., Berg G. (2001): Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Applied and Environmental Microbiology, 67: 4742- 4751. Go to original source... Go to PubMed...
  29. Sutherland G.R.J., Aust S.D. (1996): The effects of calcium on the thermal stability and activity of manganese peroxidase. Archives of Biochemistry and Biophysics, 332: 128-134. Go to original source... Go to PubMed...
  30. Tripathi D.K., Rai P., Guerriero G., Sharma S., Corpas F.J., Singh V.P. (2021): Silicon induces adventitious root formation in rice under arsenate stress with involvement of nitric oxide and indole3-acetic acid. Journal of Experimental Botany, 72: 4457-4471. Go to original source... Go to PubMed...
  31. Wang Z.Q., Tian H.X., Lei M., Megharaj M., Tan X.P., Wang F., Jia H.Z., He W.X. (2020): Soil enzyme kinetics indicate ecotoxicity of long-term arsenic pollution in the soil at field scale. Ecotoxicology and Environmental Safety, 191: 110215. Go to original source... Go to PubMed...
  32. Wasternack C., Hause B. (2013): Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. Annals of Botany, 111: 1021-1058. Go to original source... Go to PubMed...
  33. Xian Y., Wang M., Chen W.P. (2015): Quantitative assessment on soil enzyme activities of heavy metal contaminated soils with various soil properties. Chemosphere, 139: 604-608. Go to original source... Go to PubMed...
  34. Xiong Q.Q., Hu J.L., Wei H.Y., Zhang H.C., Zhu J.Y. (2021): Relationship between plant roots, rhizosphere microorganisms, and nitrogen and its special focus on rice. Agriculture, 11: 234. Go to original source...
  35. Zemanová V., Pavlíková D., Dobrev P.I., Motyka V., Pavlík M. (2019): Endogenous phytohormone profiles in Pteris fern species differing in arsenic accumulating ability. Environmental and Experimental Botany, 166: 103822. Go to original source...
  36. Zemanová V., Popov M., Pavlíková D., Kotrba P., Hnilička F., Česká J., Pavlík M. (2020): Effect of arsenic stress on 5-methylcytosine, photosynthetic parameters and nutrient content in arsenic hyperaccumulator Pteris cretica (L.) var. Albo-lineata. BMC Plant Biology, 20: 130. Go to original source... Go to PubMed...
  37. Zemanová V., Pavlíková D., Hnilička F., Pavlík M. (2021a): Arsenic toxicity-induced physiological and metabolic changes in the shoots of Pteris cretica and Spinacia oleracea. Plants, 10: 2009. Go to original source... Go to PubMed...
  38. Zemanová V., Pavlíková D., Hnilička F., Pavlík M., Zámečníková H., Hlavsa T. (2021b): A comparison of the photosynthesis response to arsenic stress in two Pteris cretica ferns. Photosynthetica, 59: 228-236. Go to original source...

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