Abstract
Jatropha curcas has shown to be a bioaccumulator and a tolerant species to different heavy metals (HMs). This study presents an evaluation system for tolerance and accumulation of chromium (Cr) and lead (Pb) in J. curcas using a cell suspension culture (CSC). This CSC was established with callus obtained from hypocotyls segments, onto Murashige-Skoog medium and 2.27 µM 2,4-dichlorophenoxyacetic acid (2,4-D). CSC growth kinetics showed a specific cell growth rate (µ) of 0.092 d−1 and a doubling time of 7.5 d. Exposure of the CSC to HMs (Cr, or Pb at 0.0, 0.5, 1.0, 2.0 and 3.0 mM), resulted in a significant effect (P ≤ 0.05) on biomass accumulation. By adding Cr (0.5 or 1.0 mM) or any Pb concentration, biomass was increased. Maximum biomass production (15.1 g L−1) was shown with Pb (3.0 mM), while all tolerance index values were between 47.8 and 136 %. In addition, the maximum accumulation of Cr (6,368 mg kg−1) and Pb (8,608 mg kg−1) were found by adding the highest concentrations used of Cr or Pb (3 mM). Bioaccumulation factors (BF) were higher (29 and 41) in the high concentrations of 2.0 and 3.0 mM Cr, respectively. In contrast, maximum BF values of Pb (16.6 and 19.4) were observed when low concentrations of Pb were used (1.0 and 0.5 mM, respectively). This is the first study reporting HMs accumulation and tolerance in J. curcas CSC. Therefore, in further studies, this culture system may be used as a model to explore the cellular mechanisms used for tolerance and accumulation of HMs.
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Abbreviations
- 2,4-D:
-
2,4-dichlorophenoxyacetic acid
- BF:
-
Bioaccumulation factor
- Cd:
-
Cadmium
- Cr:
-
Chromium
- CSC:
-
Cell suspension culture
- Cu:
-
Copper
- DW:
-
Dry weight
- FW:
-
Fresh weight
- HDPE:
-
High density polyethylene flasks
- HMs:
-
Heavy metals
- MS:
-
Murashige and Skoog (1968) medium
- Pb:
-
Lead
- PGRs:
-
Plant growth regulators
- Dt:
-
Doubling time
- TI:
-
Tolerance index
- µ:
-
Growth specific rate
- Zn:
-
Zinc
References
Agamuthu P, Abioye OP, Aziz AA (2010) Phytoremediation of soil contaminated with used lubricating oil using Jatropha curcas. J Hazard Mater 179:891–894. doi:10.1016/j.jhazmat.2010.03.088
Agbogidi OM, Mariere AE, Ohwo OA (2013) Metal concentration in plant tissues of Jatropha curcas L. grown in crude oil contaminated soil. J Sustain For 32:404–411. doi:10.1080/10549811.2011.599099
Ahmadpour P, Nawi AM, Abdu A, Abdul-Hamid Z, Singh DK, Hassan A, Majid NM, Jusop S (2010) Uptake of heavy metals by Jatropha curcas L. planted in coils containing sewage sludge. Am J Appl Sci 7:1291–1299
Attaya AS, Geelen D, Belal AEH (2012) Progress in Jatropha curcas tissue culture. Am Eurasian J Sustain Agric 6:6–13
Audet P, Charest C (2007) Heavy metal phytoremediation from a metal-analitycal perspective. Environ Pollut 147:231–237. doi:10.1016/j.envpol.2006.08.011
Bernabé-Antonio A, Estrada-Zuñiga ME, Buendía-González L, Reyes-Chilpa R, Chávez-Avila VM, Cruz-Sosa F (2010) Production of anti-HIV-1 calanolides in a callus culture of Calophyllum brasiliense (Cambes). Plant Cell Tiss Organ Cult 103:33–40. doi:10.1007/s11240-010-9750-4
Bolan N, Kunhikrishnan A, Thangarajan R, Kumpiene J, Park J, Makino T, Kirkham MB, Scheckel K (2014) Remediation of heavy metal(loid)s contaminated soils; To mobilize or to immobilize? J Hazard Mater 266:141–166. doi:10.1016/j.jhazmat.2013.12.018
Buendía-González L, Orozco-Villafuerte J, Cruz-Sosa F, Barrera-Díaz CE, Vernon-Carter EJ (2010) Prosopis laevigata a potential chromium (VI) and cadmium (II) hyperaccumulator desert plant L. Bioresour Technol 101:5862–5867. doi:10.1016/j.biortech.2010.03.027
Buendía-González L, Estrada-Zúñiga ME, Orozco-Villafuerte J, Cruz-Sosa F, Vernon-Carter EJ (2012) Somatic embryogenesis of the heavy metal accumulator Prosopis laevigata. Plant Cell Tiss Organ Cult 108:287–296. doi:10.1007/s11240-011-0042-4
Calabrese EJ, Bachmann KA, Bailer AJ, Bolger PM, Borak J, Cai L, Cedergreen N, Cherian MG, Chiueh CC, Clarkson TW et al (2007) Biological stress response terminology: integrating the concepts of adaptive response and preconditioning stress within a hormetic dose-response framework. Toxicol Appl Pharmacol 222:122–128. doi:10.1016/j.taap.2007.02.015
Couselo JL, Corredoira E, Vieitez AM, Ballester A (2012) Plant tissue culture of fast-growing trees for phytoremediation research. In: Loyola-Vargas VM, Ochoa-Alejo N (eds) Plant cell culture protocols. Methods in molecular biology, Vol 877. Springer, Heidelberg, pp 247–263
Doran PM (2009) Application of plant tissue cultures in phytoremediation research: incentives and limitations. Biotechnol Bioeng 103:60–76. doi:10.1002/bit.22280
Edwards R, Owen WJ (1986) Comparison of glutathione S-transferases of Zea mays responsible for herbicide detoxification in plants and suspension-cultured cells. Planta 169:208–215. doi:10.1007/BF00392316
Fett-Neto AG, DiCosmo F, Reynolds WF, Sakata K (1992) Cell culture of Taxus as a source of the antineoplastic drug taxol and related taxanes. Biotechnology 10:1572–1575
Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11. doi:10.1093/jexbot/53.366.1
Jamil D, Abhilash PC, Singh N, Sharma PN (2009) Jatropha curcas: a potential crop for phytoremediation of coal fly ash. J Hazard Mater 172:269–275. doi:10.1016/j.jhazmat.2009.07.004
Kumar A, Sharma A (2008) An evaluation of multipurpose oil seed crop for industrial uses (Jatropha curcas L.): a review. Ind crop prod 28:1–10. doi:10.1016/j.indcrop.2008.01.001
Kumar GP, Yadav SK, Thawale PR, Singh SK, Juwarkar AA (2008) Growth of Jatropha curcas on heavy metal contaminated soil amended with industrial wastes and Azotobacter: a greenhouse study. Bioresour Technol 99:2078–2082. doi:10.1016/j.biortech.2007.03.032
Kumar V, Makkar JPS, Beker K (2010) Dietary inclusion of detoxified Jatropha curcas kernel meal: effects on growth performance and metabolic efficiency in common carp, Cyprinus carpio L. Fish Physiol Biochem 36:1159–1170
Liang J, Yang Z, Tang L, Xu Y, Wang S, Chen F (2012) Growth performance and tolerance responses of Jatropha (Jatropha curcas) seedling subjected to isolated or combined cadmium and lead stresses. Int J Agric Biol 14:861–869
Lizhong Z, Cullen WR (1995) Effect of some heavy metals on cell suspension cultures of Catharanthus roseus. J Environ Sci 7:60–65
Luhach J, Chaudhry S (2012) Phytoremediation potential of Jatropha curcas for removal of heavy metals from refinery sludge. Int J Sci Eng Res 3:1–5
Maldonado-Magaña A, Orozco-Villafuerte J, Buendía-González L, Estrada-Zuñiga ME, Bernabé-Antonio A, Cruz-Sosa F (2013) Establishment of cell suspension cultures of Prosopis leavigata (Humb. and Bonpl. Ex willd) M.C. Johnst to determine the effect of zinc on the uptake and accumulation of lead. Rev Mex Ing Quím 12:489–498
Mangkoedihardjo S (2008) Jatropha curcas L. for phytoremediation of lead and cadmium polluted soil. World Appl Sci J 4:519–522
Mani D, Kumar C (2014) Biotechnological advances in bioremediation of heavy metals contaminated ecosystems: an overview with special reference to phytoremediation. Int J Environ Sci Technol 11:843–872. doi:10.1007/s13762-013-0299-8
Mench M, Schwitzguébel JP, Schroeder P, Bert V, Gawronski S, Gupta S (2009) Assessment of successful experiments and limitations of phytotechnologies: contaminant uptake, detoxification and sequestration, and consequences for food safety. Environ Sci Pollut Res 16:876–900. doi:10.1007/s11356-009-0252-z
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plantarum 15:473–497. doi:10.1111/j.1399-3054.1962.tb08052.x
Murthy HN, Lee EL, Paek KY (2014) Production of secondary metabolites from cell and organ cultures: strategies and approaches for biomass improvement and metabolite accumulation. Plant Cell Tiss Organ Cult 118:1–16. doi:10.1007/s11240-014-0467-7
Rawat AP, Giri K, Rai JPN (2014) Biosorption kinetics of heavy metals by leaf biomass of Jatropha curcas in single and multi-metal system. Environ Monit Assess 186:1679–1687. doi:10.1007/s10661-013-3485-8
Robinson BG, Banuelos G, Conesa HM, Evangelou MWH, Schulin R (2009) The phytomanagement of trace elements in soil. Crit Rev Plant Sci 28:240–266. doi:10.1080/07352680903035424
Solís-Ramos LY, Carballo LM, Valdez-Melara M (2013) Establishment of cell suspension cultures of two Costa Rican Jatropha species (Euphorbiaceae). Rev Biol Trop 61:1095–1107
Soodan RK, Pakade YB, Nagpal A, Katnoria JK (2014) Analytical techniques for estimation of heavy metals in soil ecosystem: a tabulated review. Talanta 125:405–410. doi:10.1016/j.talanta.2014.02.033
Soomro R, Memon RA (2007) Establishment of callus and suspension culture in Jatropha curcas. Pak J Bot 39:2431–2441
Uysal Y (2013) Removal of chromium ions from wastewater by duckweed, Lemna minor L. by using a pilot system with continuous flow. J Hazard Mater 263:486–492. doi:10.1016/j.jhazmat.2013.10.006
Vangronsveld J, Herzig R, Weyens N, Boulet J, Adriaensen K, Ruttens A, Thewys T, Vassilev A, Meers E, Nehnevajova E, Van der Lelie E, Mench M (2009) Phytoremediation of contaminated soils and groundwater: lessons from the field. Environ Sci Pollut Res 16:765–794. doi:10.1007/s11356-009-0213-6
Vila M, Pascal-Lorber S, Rathahao E, Debrauwer L, Canlet C, Laurent F (2005) Metabolism of [14C]-2,4,6-trinitrotoluene in tobacco cell suspension cultures. Environ Sci Technol 39:663–672
Vrbová M, Kotrba P, Horáček J, Smýkal P, Švábová L, Větrovcová M, Smýkalová I, Griga M (2013) Enhanced accumulation of cadmium in Linum usitatissimum L. plants due to overproduction of metallothionein α-domain as a fusion to β-glucuronidase protein. Plant Cell Tiss Organ Cult 112:321–330. doi:10.1007/s11240-012-0239-1
Wu JW, Shi Y, Zhu YX, Wang YC, Gong HJ (2013) Mechanisms of enhanced heavy metal tolerance in plants by silicon: a review. Pedosphere 23:815–825. doi:10.1016/S1002-0160(13)60073-9
Yadav SK, Juwarkar AA, Kumar GP, Thawale PR, Singh SK, Chakrabarti T (2009) Bioaccumulation and phyto-translocation of arsenic, chromium and zinc by Jatropha curcas L.: impact of dairy sludge and biofertilizer. Bioresour Technol 100:4616–4622. doi:10.1016/j.biortech.2009.04.062
Yadav SK, Dhote M, Kumar P, Sharma J, Chakrabarti T, Juwarkar AA (2010) Differential antioxidative enzyme responses of Jatropha curcas L. to chromium stress. J Hazard Mater 180:609–615. doi:10.1016/j.jhazmat.2010.04.077
Zhang W, Cai Y, Tu C, Ma LQ (2002) Arsenic speciation and distribution in an arsenic hyperaccumulating plant. Sci Total Environ 300:167–177. doi:10.1007/s13762-013-0384-z
Acknowledgments
The study reported here was carried out during a postdoctoral stay supported by the Consejo Nacional de Ciencia y Tecnología (CONACYT) (project 99963: 2012-2014). We are grateful to Ricardo Cruz Huizache for his kind support in Laboratory assistance and Atomic Absorption Spectrometer procedures.
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The authors have no conflicts of interest to declare.
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Authors A. Bernabé-Antonio, L. Álvarez, L. Buendía-González, A. Maldonado-Magaña, F. Cruz-Sosa have contributed equally to this work.
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Bernabé-Antonio, A., Álvarez, L., Buendía-González, L. et al. Accumulation and tolerance of Cr and Pb using a cell suspension culture system of Jatropha curcas . Plant Cell Tiss Organ Cult 120, 221–228 (2015). https://doi.org/10.1007/s11240-014-0597-y
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DOI: https://doi.org/10.1007/s11240-014-0597-y