Photosynthetica, 2018 (vol. 56), issue 2

Photosynthetica 2018, 56(2):495-504 | DOI: 10.1007/s11099-017-0698-z

Tolerance mechanisms in Cassia alata exposed to cadmium toxicity - potential use for phytoremediation

J. R. R. Silva1, A. R. Fernandes1, M. L. Silva Junior1, C. R. C. Santos1, A. K. S. Lobato2,*
1 Instituto de Ciências Agrárias, Universidade Federal Rural da Amazônia, Belém, Pará, Brazil
2 Núcleo de Pesquisa Vegetal Básica e Aplicada, Universidade Federal Rural da Amazônia, Paragominas, Pará, Brazil

Cadmium is often detected in areas contaminated by heavy metals and the incidence of this element in dangerous concentrations has been increasing due to anthropogenic activities. The aim of this research was to determine Cd concentrations in tissues, quantify compounds, pigments and enzymes, and to evaluate the gas exchange. Our aim was also to identify components that can modify and contribute to tolerance of Cassia alata against Cd toxicity. We used five Cd concentrations (0, 22, 44, 88, and 132 μM) to validate our hypothesis. The Cd concentrations in tissues of C. alata plants increased significantly, compared with the control treatment, in the following graduated sequence: root > leaf > stem. Progressive enhancement in glutathione (GSH) was verified in plants treated with all Cd concentrations used, when compared with treatment without Cd. Antioxidant enzyme activities presented similar patterns with progressive enhancements, being a desirable characteristic for plants with a potential to hyperaccumulate Cd. Our results suggest that C. alata plants can be used for phytoremediation programs. Their defense mechanism is based on Cd accumulation in roots, coupled with increase in GSH and the efficient activity of antioxidant enzymes that contribute to minimize the oxidative stress and consequently improve the protection of the metabolic machinery.

Keywords: detoxification; gas exchange; heavy metal; reactive oxygen species; remediation

Received: March 16, 2016; Accepted: December 20, 2016; Published: June 1, 2018Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Silva, J.R.R., Fernandes, A.R., Junior, M.L., Santos, C.R.C., & Lobato, A.K.S. (2018). Tolerance mechanisms in Cassia alata exposed to cadmium toxicity - potential use for phytoremediation. Photosynthetica, 56(2), 495-504. doi: 10.1007/s11099-017-0698-z.
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Akhter M.F., McGarvey B., Macfie S.M.: Reduced translocation of cadmium from roots is associated with increased production of phytochelatins and their precursors. - J. Plant Physio. 169:1821-1829, 2012.
    2. Badawi G.H., Yamauchi Y., Shimada E. et al.: Enhanced tolerance to salt and water deficit by overexpressing superoxide dismutase in tobacco (Nicotiana tabacum) chloroplasts. - Plant Sci. 166: 919-928, 2004. Go to original source...
    3. Bauddh K., Singh R.P.: Growth, tolerance efficiency and phytoremediation potential of Ricinus communis (L.) and Brassica juncea (L.) in salinity and drought affected cadmium contaminated soil. - Ecotox. Environ. Safe. 85: 13-22, 2012. Go to original source...
    4. Bech J., Duran P., Roca N. et al.: Accumulation of Pb and Zn in Bidens triplinervia and Senecio sp. spontaneous species from mine spoils in Peru and their potential use in phytoremediation. - J. Geochem. Explor. 123: 109-113, 2012. Go to original source...
    5. Bhatt I., Tripathi B.N.: Plant peroxiredoxins: catalytic mechanisms, functional significance and future perspectives. - Biotechnol. Adv. 29: 850-859, 2011 Go to original source...
    6. Bradford M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. - Anal. Biochem. 72: 246-254, 1976. Go to original source...
    7. Braga L.F., Sousa M.P., Braga J.F., Delachiave M.E.A.: [Acid scarification, temperature and light on the germination process of Senna alata (L.) Roxb. seeds.]. - Rev. Bras. Plantas Med. 12: 1-7, 2010. [In Portuguese] Go to original source...
    8. Cakmak I., Marschner H.: Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase and glutathione reductase in bean leaves. - Plant Physiol. 98: 1222-1227, 1992. Go to original source...
    9. Cho U., Seo N.: Oxidative stress in Arabidopsis thaliana exposed to cadmium is due to hydrogen peroxide accumulation. - Plant Sci. 168: 113-120, 2005. Go to original source...
    10. Cunha K.P.V., Nascimento C.W.A., Pimentel R.M.M. et al.: [Cadmium and zinc availability, accumulation and toxicity in maize grown in a contaminated soil.]. - Rev. Bras. Cienc. Solo 32: 1319-1328, 2008. [In Portuguese] Go to original source...
    11. Dai Z.Y., Shu W.S., Liao B. et al.: Intraspecific variation in cadmium tolerance and accumulation of a high biomass tropical tree Averrhoa carambola L.: implication for phytoextraction. - J. Environ. Monitor. 13: 1723-1729, 2011. Go to original source...
    12. Degl'Innocenti E., Castagna A., Ranieri A., Guidi L.: Combined effects of cadmium and ozone on photosynthesis of Lycopersicon esculentum. - Photosynthetica 52: 179-185, 2014.
    13. Deng G., Li M., Li H. et al.: Exposure to cadmium causes declines in growth and photosynthesis in the endangered aquatic fern (Ceratopteris pteridoides). - Aquat. Bot. 112: 23-32, 2014. Go to original source...
    14. Ekmekçi Y., Tanyolaç B.D., Ayhan B.: Effects of cadmium on antioxidante enzyme and photosynthetic activities in leaves of two maize cultivars. - J. Plant Physiol. 165: 600-611, 2008. Go to original source...
    15. Faller P., Kienzler K., Krieger-Liszkay A.: Mechanism of Cd2+ toxicity: Cd2+ inhibits photoactivation of Photosystem II by competitive binding to the essential Ca2+ site. - Biochim. Biophys. Acta 1706: 158-164, 2005. Go to original source...
    16. Fan K.C., His H.C., Chen C.W. et al.: Cadmium accumulation and tolerance of mahogany (Swietenia macrophylla) seedlings for phytoextraction applications. - J. Environ. Manage. 92: 2818-2822, 2011. Go to original source...
    17. Fernandes M.S.: [Mineral Nutrition of Plants]. Pp. 432. SBCS, Viçosa 2006. [In Portuguese]
    18. Fernández R., Bertrand A., Reis R. et al.: Growth and physiological responses to cadmium stress of two populations of Dittrichia viscosa (L.) Greuter. - J. Hazard. Mater. 244-245: 555-562, 2013. Go to original source...
    19. Gill S.S., Tuteja N.: Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. - Plant Physiol. Bioch. 48: 909-930, 2010. Go to original source...
    20. Gratão P.L., Monteiro C.C., Tezotto T. et al.: Cadmium stress antioxidant responses and root-to-shoot communication in grafted tomato plants. - Biometals 28: 803-816, 2015. Go to original source...
    21. Hartwig I., Oliveira A.C., Carvalho F.I.F. et al.: [Associated mechanisms of aluminum tolerance in plants.]. - Semin. Cienc. Agrar. 28: 219-228, 2007. [In Portuguese] Go to original source...
    22. Hasan S.A., Hayat S., Ali B., Ahmad A.: 28-homobrassinolide protects chickpea (Cicer arietinum) from cadmium toxicity by stimulating antioxidants. - Environ. Pollut. 151: 60-66, 2008. Go to original source...
    23. Hasan S.A., Hayat S., Ahmad A.: Brassinosteroids protect photosynthetic machinery against the cadmium induced oxidative stress in two tomato cultivars. - Chemosphere 84: 1446-1451, 2011. Go to original source...
    24. Hattab S., Dridi B., Chouba L. et al.: Photosynthesis and growth responses of pea Pisum sativum L. under heavy metals stress. - J. Environ. Sci. 21: 1552-1556, 2009. Go to original source...
    25. Havir E.A., McHale N.A.: Biochemical and development characterization of multiple forms of catalase in tobacco leaves. - Plant Physiol. 84: 450-455, 1987. Go to original source...
    26. Hsu Y.T., Kao C.H.: Heat shock-mediated H2O2 accumulation and protection against Cd toxicity in rice seedlings. - Plant Soil 300: 137-147, 2007. Go to original source...
    27. Jia L., Liu Z., Chen W. et al.: Hormesis effects induced by cadmium on growth and photosynthetic performance in a hyperaccumulator, Lonicera japonica Thunb. - J. Plant Growth Regul. 34: 13-21, 2015. Go to original source...
    28. Krämer U.: Metal hyperaccumulation in plants. - Annu. Rev. Plant Biol. 61: 517-534, 2010. Go to original source...
    29. Liang Y., Zhang W., Chen Q. et al.: Effect of exogenous silicon (Si) on H+-ATPase activity, phospholipids and fluidity of plasma membrane in leaves of salt-stressed barley (Hordeum vulgare L.). - Environ. Exp. Bot. 57: 212-219, 2006. Go to original source...
    30. Lichtenthaler H.K., Buschmann C.: Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. - Curr. Protoc. Food Anal. Chem. 431-438, 2001.
    31. Liu X., Peng K., Wang A. et al.: Cadmium accumulation and distribution in populations of Phytolacca americana L. and the role of transpiration. - Chemosphere 78: 1136-1141, 2010. Go to original source...
    32. Lu Z., Zhang Z., Su Y. et al.: Cultivar variation in morphological response of peanut roots to cadmium stress and its relation to cadmium accumulation. - Ecotox. Environ. Safe. 91: 147-155, 2013. Go to original source...
    33. Ma C.C., Gao Y.B., Guo H.Y., Wang J.L.: Photosynthesis, transpiration and water use efficiency of Caragana microphylla, C. intermedia and C. korshinskii. - Photosynthetica 42: 65-70, 2004. Go to original source...
    34. Macnicol R.D., Beckett P.H.T.: Critical tissue concentrations of potentially toxic elements. - Plant Soil 85: 107-129, 1985. Go to original source...
    35. Melo L.C.A., Alleoni L.R.F., Carvalho G., Azevedo R.A.: Cadmium and barium-toxicity effects on growth and antioxidant capacity of soybean (Glycine max L.) plants, grown in two soil types with different physicochemical properties. - J. Plant. Nutr. Soil Sci. 174: 847-859, 2011. Go to original source...
    36. Mohamed A.A., Castagna A., Ranieri A., Toppi L.S.: Cadmium tolerance in Brassica juncea roots and shoots is affected by antioxidant status and phytochelatin biosynthesis. - Plant Physiol. Bioch. 57: 15-22, 2012. Go to original source...
    37. Najeeb U., Jilani G., Ali S. et al.: Insights into cadmium induced physiological and ultra-structural disorders in Juncus effusus L. and its remediation through exogenous citric acid. - J. Hazard. Mater. 186: 565-574, 2011. Go to original source...
    38. Nakamura S., Suzui N., Nagasaka T. et al.: Application of glutathione to roots selectively inhibits cadmium transport from roots to shoots in oilseed rape. - J. Exp. Bot. 64: 1073-1081, 2013. Go to original source...
    39. Nakano Y., Asada K.: Hydrogen peroxide is scavenged by ascorbate-specific peroxidases in spinach chloroplasts. - Plant Cell Physiol. 22:867-880, 1981.
    40. Paiva H.N., Carvalho J.G., Siqueira J.O.: [Effect of the cadmium application on nutrients content in cedro (Cedrela fissilis VELL.) seedlings.]. - Cienc. Florestal 11: 153-162, 2001. [In Portuguese] Go to original source...
    41. Paiva H.N., Carvalho J.G., Siqueira J.O.: [Effect of the cadmium application on nutrients content in cedro (Cedrela fissilis VELL.) seedlings.]. - Cienc. Florestal 11: 153-162, 2001. [In Portuguese] Go to original source...
    42. Pan J., Plant J.A., Voulvoulis N. et al.: Cadmium levels in Europe: implications for human health. - Environ. Geochem. Hlth. 32: 1-12, 2010. Go to original source...
    43. Parmar P., Kumari N., Sharma V.: Structural and functional alterations in photosynthetic apparatus of plants under cadmium stress. - Bot. Stud. 54: 1-6, 2013. Go to original source...
    44. Pietrini F., Iannelli M.A., Pasqualini S., Massacci A.: Interaction of camium with glutathione and photosynthesis in developing leaves and chloroplasts of Phragmites australis (Cav.) Trin. ex Steudel. - Plant Physiol. 133: 829-837, 2003. Go to original source...
    45. Riaz S., Iqbal M., Hussain I. et al.: Chronic cadmium induced oxidative stress not the DNA fragmentation modulates growth in spring wheat (Triticum aestivum). - Int. J. Agric. Biol. 16: 789-794, 2014.
    46. Sharma P., Jha A.B., Dubey R.S., Pessarakli M.: Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. - J. Bot. 2012: 217037, 2012. Go to original source...
    47. Silva F.A.S., Azevedo C.A.V.: [Assistat computational program version for the Windows operating system.]. - Rev. Bras. Prod. Agroindust. 4: 71-78, 2002. [In Portuguese]
    48. Silva J.R.R., Fernandes A.R., Perez D.V.: Phytoextraction of heavy metals from a landfill in the metropolitan region of Belém-Pará-Brazil. - Rev. Ciênc. Agrar. 57: 429-438, 2014.
    49. Singh S., Khan N.A., Nazar R., Anjum N.A.: Photosynthetic traits and activities of antioxidant enzymes in blackgram (Vigna mungo L. Hepper) under cadmium stress. - Am. J. Plant Phys. 3: 25-32, 2008.
    50. Soares C.R.F.S., Siqueira J.O., Carvalho J.G., Moreira F.M.S.: [Cadmium phytotoxity to Eucalyptus maculata and E. urophylla in nutrient solution.]. - Rev. Árvore 29: 175-183, 2005. [In Portuguese]
    51. Soares C.R.F.S., Grazziotti P.H., Siqueira J.O. et al.: [Zinc toxicity on growth and nutrition of Eucalyptus maculata and Eucalyptus urophylla in nutrient solution.]. - Pesqui. Agropecu. Bras. 36: 339-348, 2001. [In Portuguese] Go to original source...
    52. Steel R.G.D., Torrie J.H., Dickey D.A.: Principles and Procedures of Statistics: a Biometrical Approach. Pp. 666. Academic Internet Publishers, Moorpark 2006.
    53. Sterckeman T., Redjala T., Morel J.L.: Influence of exposure solution composition and of plant cadmium content on root cadmium short-term uptake. - Environ. Exp. Bot. 74:131-139, 2011. Go to original source...
    54. Su Y., Liu J., Lu Z. et al.: Effects of iron deficiency on subcellular distribution and chemical forms of cadmium in peanut roots in relation to its translocation. - Environ. Exp. Bot. 97: 40-48, 2014. Go to original source...
    55. Sun H., Li Y., Ji Y. et al.: Environmental contamination and health hazard of lead and cadmium around Chatian mercury mining deposit in western Hunan Province, China. - T. Nonferr. Metal Soc. 20: 308-314, 2010. Go to original source...
    56. Valentovičová K., Halušková L., Huttová J. et al.: Effect of cadmium on diaphorase activity and nitric oxide production in barley root tips. - J. Plant Physiol. 167: 10-14, 2010. Go to original source...
    57. Velikova V., Yordanov I., Edreva A.: Oxidative stress and some antioxidant system in acid rain treated bean plants: protective role of exogenous polyamines. - Plant Sci. 151: 59-66, 2000. Go to original source...
    58. Wan G., Najeeb U., Jilani G. et al.: Calcium invigorates the cadmium-stressed Brassica napus L. plants by strengthening their photosynthetic system. - Environ. Sci. Pollut. R. 18: 1478-1486, 2011. Go to original source...
    59. Wanat N., Austruy A., Joussein E. et al.: Potentials of Miscanthus × giganteus grown on highly contaminated Technosols. - J. Geochem. Explor. 126-127: 78-84, 2013. Go to original source...
    60. Wang S., Zhang D., Pan X.: Effects of cadmium on the activities of photosystems of Chlorella pyrenoidosa and the protective role of cyclic electron flow. - Chemosphere 93: 230-237, 2013. Go to original source...
    61. Wu J.W., Shi Y., Zhu Y.X. et al.: Mechanisms of enhanced heavy metal tolerance in plants by silicon: a review. - Pedosphere 23: 815-825, 2013. Go to original source...
    62. Wu Q.S., Xia R.X., Zou Y.N.: Reactive oxygen metabolism in mycorrhizal and non-mycorrhizal citrus (Poncirus trifoliate) seedlings subjected to water stress. - J. Plant Physiol. 163: 1101-1110, 2006. Go to original source...
    63. Xiang C., Werner B.L., Christensen E.M., Oliver D.J.: The biological functions of glutathione revisited in Arabidopsis transgenic plants with altered glutathione levels. - Plant Physiol. 126: 564-574, 2001. Go to original source...
    64. Yoon J., Cao X., Zhou Q., Ma L.Q.: Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. - Sci. Total Environ. 368: 456-464, 2006. Go to original source...
    65. Zhou C., Zhang K., Lin J. et al.: Physiological responses and tolerance mechanisms to cadmium in Conyza canadensis. - Int. J. Phytoremediat. 17: 280-289, 2015.

    Return to the content