Tagetes minuta L. Variability in Terms of Lead Phytoextraction from Polluted Soils: Is Historical Exposure a Determining Factor?
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Abstract
Tagetes minuta L. is a plant which accumulates Pb under certain conditions, making it a candidate for phytoextraction projects because it also produces marketable essential oils without detectable Pb levels. Although extraction efficiency has been shown to significantly vary between individuals, these results have been obtained using only historically exposed populations, which leads to the questions: Is the ability to tolerate and accumulate Pb a property of the species? Or is it a characteristic of some individuals from a historically exposed population? In this context, a greenhouse experiment was performed to analyse the intrapopulation and interpopulation variability in response to Pb among individuals from historically unexposed and exposed populations. In addition, we also attempted to identify relationships between certain capabilities (toleration and accumulation of Pb) and the physiological parameters related to oxidative stress or the volatile compounds of the essential oils. The Pb concentration was determined by total reflection X-ray fluorescence, physiological parameters were obtained by spectrophotometry, and essential oils were analysed by gas chromatography. The results demonstrated that adequate tolerance and accumulation capabilities are present in T. minuta, irrespective of the exposure history. These findings may be associated to a hormesis response, which includes enhancement of pigments, biomass production and the uptake of other heavy metals such as micronutrients. Nevertheless, the historically exposed population had a better tolerance to Pb, since it presented defence characteristics reflected in the essential oil composition and in the avoidance of damage at the lipid peroxidation level after Pb uptake.
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Keywords
Pb pollution Phytoremediation Tolerance Essential oilsNotes
Acknowledgements
This work was partially supported by the Secretaría de Ciencia y Técnica de la Universidad Nacional de Córdoba (SECYT-UNC “B” Res. 313/2016), Fondo para la Investigación Científica y Técnica (FONCyT, PICT 2013-0988; 2015-1362). The author M.J. Salazar was funded by CONICET through a postdoctoral scholarship. We would especially like to thank the Brazilian Synchrotron Light Source (LNLS) (partially supported under proposal 20150094). Special thanks are also due to Proof Reading Service and to Dr. P. Hobson (native speaker) for language revision.
Author Contributions
M.J.S. and M.L.P planned and designed the research; M.J.S. and E.M.P. performed the experiments, sample processing and analysis of volatile oils and physiological parameters, M.J.S. and E.D.W performed heavy metal analysis, and M.J.S. wrote the manuscript.
References
- Arimura G, Ozawa R, Nishioka T, Boland W, Koch T, Kühnemann F, Takabayashi J (2002) Herbivore-induced volatiles induce the emission of ethylene in neighboring lima bean plants. Plant J 29(1):87–98. https://doi.org/10.1046/j.1365-313x.2002.01198.x CrossRefGoogle Scholar
- Blaylock MJ, Huang JW (2000) Phytoextraction of metals. In: Ensley BD (ed) Phytoremediation of Toxic Metals: Using Plants to Clean-up the Environment. John Wiley and Sons, Inc, New York, pp 53–70Google Scholar
- Bu-Olayan AH, Thomas BV (2009) Translocation and bioaccumulation of trace metals in desert plants of Kuwait governorates. Res J Environ Sci 3(5):581–587. https://doi.org/10.3923/rjes.2009.581.587 CrossRefGoogle Scholar
- Chaaban A, de Souza ALF, Martins CEN, Bertoldi FC, Molento MB (2017) Chemical composition of the essential oil of Tagetes minuta and its activity against Cochliomyia macellaria (Diptera: Calliphoridae). Eur J Med Plants 18(1):1–10. https://doi.org/10.9734/EJMP/2017/32078 CrossRefGoogle Scholar
- Chalchat JC, Garry RP, Muhayimana A (1995) Essential oil of Tagetes minuta from Rwanda and France: chemical composition according to harvesting location, growth stage and part of plant extracted. J Essent Oil Res 7(4):375–386. https://doi.org/10.1080/10412905.1995.9698544 CrossRefGoogle Scholar
- Danh LT, Truong P, Mammucari R, Foster N (2010) Economic incentive for applying vetiver grass to remediate lead, copper and zinc contaminated soils. Int J Phytoremediat 13(1):47–60. https://doi.org/10.1080/15226511003671338 CrossRefGoogle Scholar
- Dinesh DS, Kumari S, Kumar V, Das P (2014) The potentiality of botanicals and their products as an alternative to chemical insecticides to sandflies (Diptera: Psychodidae): a review. J Vector Borne Dis 51(1):1–7Google Scholar
- Dixit R, Wasiullah, Malaviya D, Pandiyan K, Singh U, Sahu A, Shukla R, Singh B, Rai J, Sharma P, Lade H, Paul D (2015) Bioremediation of heavy metals from soil and aquatic environment: an overview of principles and criteria of fundamental processes. Sustainability 7(2):2189–2212. https://doi.org/10.3390/su7022189 CrossRefGoogle Scholar
- Figueiredo AC, Barroso JG, Pedro LG, Scheffer JJ (2008) Factors affecting secondary metabolite production in plants: volatile components and essential oils. Flavour Fragr J 23(4):213–226. https://doi.org/10.1002/ffj.1875 CrossRefGoogle Scholar
- Foyer CH, Harbinson J (1994) Oxygen metabolism and the regulation of photosynthetic electron transport. In: Foyer CH, Moullineaux PM (eds) Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants. CRC Press, London, pp 1–42Google Scholar
- Gautam M, Agrawal M (2017) Influence of metals on essential oil content and composition of lemongrass (Cymbopogon citratus (D.C.) Stapf.) grown under different levels of red mud in sewage sludge amended soil. Chemosphere 175:315–322. https://doi.org/10.1016/j.chemosphere.2017.02.065 CrossRefGoogle Scholar
- Gil A, Ghersa C, Leicach S (2000) Essential oil yield and composition of Tagetes minuta accessions from Argentina. Biochem Syst Ecol 28(3):261–274. https://doi.org/10.1016/S0305-1978(99)00062-9 CrossRefGoogle Scholar
- Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. Arch Biochem Biophys 125(1):189–198. https://doi.org/10.1016/0003-9861(68)90654-1 CrossRefGoogle Scholar
- Jadia CD, Fulekar M (2009) Phytoremediation of heavy metals: recent techniques. Afr J Biotechnol 8(6). https://doi.org/10.5897/AJB2009.000-9152
- John R, Ahmad P, Gadgil K, Sharma S (2012) Heavy metal toxicity: effect on plant growth, biochemical parameters and metal accumulation by Brassica juncea L. Int J Plant Prod 3(3):65–76. https://doi.org/10.22069/IJPP.2012.653 Google Scholar
- Jones DL, Darrah PR (1994) Role of root derived organic acids in the mobilization of nutrients from the rhizosphere. Plant Soil 166(2):247–257. https://doi.org/10.1007/BF00008338 CrossRefGoogle Scholar
- Kabata-Pendias A, Pendias H (1984) Trace elements in soils and plants. CRC Press, Boca RatonGoogle Scholar
- Kabata-Pendias A, Pendias H (2001) Trace Elements in Soils and Plants. CRC Press, Boca RatonGoogle Scholar
- Karimian P, Kavoosi G, Amirghofran Z (2014) Anti–oxidative and anti–inflammatory effects of Tagetes minuta essential oil in activated macrophages. Asian Pac J Trop Biomed 4(3):219–227. https://doi.org/10.1016/S2221-1691(14)60235-5 CrossRefGoogle Scholar
- Karri V, Schuhmacher M, Kumar V (2016) Heavy metals (Pb, Cd, As and MeHg) as risk factors for cognitive dysfunction: a general review of metal mixture mechanism in brain. Environ Toxicol Pharmacol 48(Supplement C):203–213. https://doi.org/10.1016/j.etap.2016.09.016 CrossRefGoogle Scholar
- Kelepertzis E (2014) Accumulation of heavy metals in agricultural soils of Mediterranean: insights from Argolida basin, Peloponnese, Greece. Geoderma 221-222(Supplement C):82–90. https://doi.org/10.1016/j.geoderma.2014.01.007 CrossRefGoogle Scholar
- Küpper H, Parameswaran A, Leitenmaier B, Trtílek M, Šetlík I (2007) Cadmium-induced inhibition of photosynthesis and long-term acclimation to cadmium stress in the hyperaccumulator Thlaspi caerulescens. New Phytol 175(4):655–674. https://doi.org/10.1111/j.1469-8137.2007.02139.x CrossRefGoogle Scholar
- Leyva A, Quintana A, Sánchez M, Rodríguez EN, Cremata J, Sánchez JC (2008) Rapid and sensitive anthrone–sulfuric acid assay in microplate format to quantify carbohydrate in biopharmaceutical products: method development and validation. Biologicals 36(2):134–141. https://doi.org/10.1016/j.biologicals.2007.09.001 CrossRefGoogle Scholar
- Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. In: Douce R, Packer L (eds) Methods in Enzymology. Academic Press, New York, pp 350–382Google Scholar
- Mani D, Kumar C, Patel NK, Sivakumar D (2015) Enhanced clean-up of lead-contaminated alluvial soil through Chrysanthemum indicum L. Int J Environ Sci Technol 12(4):1211–1222. https://doi.org/10.1007/s13762-013-0488-5 CrossRefGoogle Scholar
- Meyer CL, Kostecka AA, Saumitou-Laprade P, Créach A, Castric V, Pauwels M, Frérot H (2010) Variability of zinc tolerance among and within populations of the pseudometallophyte species Arabidopsis halleri and possible role of directional selection. New Phytol 185(1):130–142. https://doi.org/10.1111/j.1469-8137.2009.03062.x CrossRefGoogle Scholar
- Mihaliak CA, Couvet D, Lincoln DE (1989) Genetic and environmental contributions to variation in leaf mono-and sesquiterpenes of Heterotheca subaxillaris. Biochem Syst Ecol 17(7–8):529–533. https://doi.org/10.1016/0305-1978(89)90095-1 CrossRefGoogle Scholar
- Mlala S (2015) Chemical Constituents and Biological Studies of Tagetes minuta L. and Rauvolfia caffra Sond. Thesis for Master of Science, University of Fort Hare Alice, Alice, South AfricaGoogle Scholar
- Moustakas M, Lanaras T, Symeonidis L, Karataglis S (1994) Growth and some photosynthetic characteristics of field grown Avena sativa under copper and lead stress. Photosynthetica 30:389–396Google Scholar
- Neumann G (2007) Root exudates and nutrient cycling. In: Marschner P, Rengel Z (eds) Soil Biology. Nutrient Cycling in Terrestrial Ecosystem. Springer-Verlag, Berlin, Heidelberg, pp 123–146CrossRefGoogle Scholar
- Niu Z, Sun L, Sun T (2011) The bioadsorption of cadmium and lead by bacteria in root exudates culture. Soil Sediment Contam Int J 20(8):877–891. https://doi.org/10.1080/15320383.2011.620042 CrossRefGoogle Scholar
- Palta JP (1990) Leaf chlorophyll content. Remote Sens Rev 5(1):207–213. https://doi.org/10.1080/02757259009532129 CrossRefGoogle Scholar
- Patel A, Patra DD (2014) Influence of heavy metal rich tannery sludge on soil enzymes vis-à-vis growth of Tagetes minuta, an essential oil bearing crop. Chemosphere 112:323–332. https://doi.org/10.1016/j.chemosphere.2014.04.063 CrossRefGoogle Scholar
- Pinto AP, Mota AM, de Varennes A, Pinto FC (2004) Influence of organic matter on the uptake of cadmium, zinc, copper and iron by sorghum plants. Sci Total Environ 326(1–3): 239–247. doi: https://doi.org/10.1016/j.scitotenv.2004.01.004
- Posthuma L, Hogervorst RF, Joosse EN, Van Straalen NM (1993) Genetic variation and covariation for characteristics associated with cadmium tolerance in natural populations of the springtail Orchesella cincta (L.) Evolution 47:619–631. https://doi.org/10.1111/j.1558-5646.1993.tb02116.x CrossRefGoogle Scholar
- Rai R, Agrawal M, Agrawal SB (2016) Impact of heavy metals on physiological processes of plants: with special reference to photosynthetic system. In: Singh A, Prasad SM, Singh RP (eds) Plant Responses to Xenobiotics. Springer Singapore, Singapore, pp 127–140Google Scholar
- Robert G, Muñoz N, Melchiorre M, Sánchez F, Lascano R (2014) Expression of animal anti-apoptotic gene Ced-9 enhances tolerance during Glycine max L.–Bradyrhizobium japonicum interaction under saline stress but reduces nodule formation. PLoS One 9(7):e101747. https://doi.org/10.1371/journal.pone.0101747 CrossRefGoogle Scholar
- Rocabado G, Gonzáles E, De La Fuente F, Araya P (2011) Estudios de la actividad ansiolitica-sedante de la especie Tagetes minuta L. Revista Med La Paz 17(1): 22–25Google Scholar
- Rodriguez E, da Conceição Santos M, Azevedo R, Correia C, Moutinho-Pereira J, Ferreira de Oliveira JMP, Dias MC (2015) Photosynthesis light-independent reactions are sensitive biomarkers to monitor lead phytotoxicity in a Pb-tolerant Pisum sativum cultivar. Environ Sci Pollut Res 22(1):574–585. https://doi.org/10.1007/s11356-014-3375-9 CrossRefGoogle Scholar
- Salazar MJ, Pignata ML (2014) Lead accumulation in plants grown in polluted soils. Screening of native species for phytoremediation. J Geochem Explor 137(0):29–36. https://doi.org/10.1016/j.gexplo.2013.11.003 CrossRefGoogle Scholar
- Salazar MJ, Rodriguez JH, Cid CV, Bernardelli CE, Donati ER, Pignata ML (2016a) Soil variables that determine lead accumulation in Bidens pilosa L. and Tagetes minuta L. growing in polluted soils. Geoderma 279:97–108. https://doi.org/10.1016/j.geoderma.2016.06.011 CrossRefGoogle Scholar
- Salazar MJ, Rodriguez JH, Cid CV, Pignata ML (2016b) Auxin effects on Pb phytoextraction from polluted soils by Tegetes minuta L. and Bidens pilosa L.: extractive power of their root exudates. J Hazard Mater 311:63–69. https://doi.org/10.1016/j.jhazmat.2016.02.053 CrossRefGoogle Scholar
- Sánchez-Osorio I, López-Pantoja G, Tapias R, Pareja E, Domínguez L (2013) Emisión de monoterpenos foliares en alcornoques afectados por Cerambyx welensii Küster (Coleoptera: Cerambycidae). 6to Congreso Forestal Español. España: Sociedad Española de Ciencias ForestalesGoogle Scholar
- Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Botany 2012:1–26. https://doi.org/10.1155/2012/217037 CrossRefGoogle Scholar
- Shirazi MT, Gholami H, Kavoosi G, Rowshan V, Tafsiry A (2014) Chemical composition, antioxidant, antimicrobial and cytotoxic activities of Tagetes minuta and Ocimum basilicum essential oils. Food Sci Nutr 2(2):146–155. https://doi.org/10.1002/fsn3.85 CrossRefGoogle Scholar
- Sidhu GPS, Singh HP, Batish DR, Kohli RK (2017) Phytoremediation of lead by a wild, non-edible Pb accumulator Coronopus didymus (L.) Brassicaceae. Internat J Phytoreme. (just-accepted), 00–00. https://doi.org/10.1080/15226514.2017.1374331
- Singh RP, Agrawal M (2007) Effects of sewage sludge amendment on heavy metal accumulation and consequent responses of Beta vulgaris plants. Chemosphere 67(11):2229–2240. https://doi.org/10.1016/j.chemosphere.2006.12.019 CrossRefGoogle Scholar
- Singh P, Krishna A, Kumar V, Krishna S, Singh K, Gupta M, Singh S (2016) Chemistry and biology of industrial crop Tagetes species: a review. J Essent Oil Res 28(1):1–14. https://doi.org/10.1080/10412905.2015.1076740 CrossRefGoogle Scholar
- Sosa MC, Salazar MJ, Zygadlo JA, Wannaz ED (2016) Effects of Pb in Tagetes minuta L. (Asteraceae) leaves and its relationship with volatile compounds. Ind Crop Prod 82:37–43. https://doi.org/10.1016/j.indcrop.2015.12.011 CrossRefGoogle Scholar
- Sterckeman T, Duquène L, Perriguey J, Morel J-L (2005) Quantifying the effect of rhizosphere processes on the availability of soil cadmium and zinc. Plant Soil 276(1):335–345. https://doi.org/10.1007/s11104-005-5087-x CrossRefGoogle Scholar
- Vasudevan P, Kashyap S, Sharma S (1997) Tagetes: a multipurpose plant. Bioresour Technol 62(1):29–35. https://doi.org/10.1016/S0960-8524(97)00101-6 CrossRefGoogle Scholar
- Vázquez AM, Demmel GI, Criado SG, Aimar ML, Cantero JJ, Rossi LI, Velasco MI (2011) Phytochemistry of Tagetes minuta L.(Asteraceae) from Córdoba, Argentina: Comparative study between essential oil and HS-SPME analyses. Bol Latinoam Caribe Plant Med Aromat 10:351–362Google Scholar
- Venkatachalam P, Jayaraj M, Manikandan R, Geetha N, Rene ER, Sharma NC, Sahi SV (2017) Zinc oxide nanoparticles (ZnONPs) alleviate heavy metal-induced toxicity in Leucaena leucocephala seedlings: a physiochemical analysis. Plant Physiol Biochem 110:59–69. https://doi.org/10.1016/j.plaphy.2016.08.022 CrossRefGoogle Scholar
- Wannaz ED, Carreras HA, Abril GA, Pignata ML (2011) Maximum values of Ni2+, Cu2+, Pb2+ and Zn2+ in the biomonitor Tillandsia capillaris (Bromeliaceae): relationship with cell membrane damage. Environ Exp Botany 74:296–301. https://doi.org/10.1016/j.envexpbot.2011.06.012 CrossRefGoogle Scholar
- Wanzala W, Hassanali A, Mukabana WR, Takken W (2014) Repellent activities of essential oils of some plants used traditionally to control the brown ear tick, Rhipicephalus appendiculatus. J Parasitol Res 2014:1–10. https://doi.org/10.1155/2014/434506 CrossRefGoogle Scholar
- Wenzel W, Bunkowski M, Puschenreiter M, Horak O (2003) Rhizosphere characteristics of indigenously growing nickel hyperaccumulator and excluder plants on serpentine soil. Environ Pollut 123(1):131–138. https://doi.org/10.1016/S0269-7491(02)00341-X CrossRefGoogle Scholar
- Zheljazkov VD, Craker LE, Xing B (2006) Effects of Cd, Pb, and Cu on growth and essential oil contents in dill, peppermint, and basil. Environ Exp Bot 58(1–3):9–16. https://doi.org/10.1016/j.envexpbot.2005.06.008 CrossRefGoogle Scholar
- Zygadlo JA, Grosso NR, Abburra RE, Guzman CA (1990) Essential oil variation in Tagetes minuta populations. Biochem Syst Ecol 18(6):405–407. https://doi.org/10.1016/0305-1978(90)90084-S CrossRefGoogle Scholar