Lead (Pb) is a highly toxic metal for humans, animals and plants even at low concentrations in the soil. The ingestion of chocolate produced from contaminated beans can contribute to consumer exposure to Pb. While, Mn is an element essential for plants and participates as enzymatic cofactors in several metabolic pathways. The objective of this study was to evaluate the influence of Mn on mitigation of Pb toxicity in seedling of the cacao clonal CCN 51 genotype grown in soils with different doses of Pb, Mn and Mn+Pb, through physiological, biochemical, molecular and nutritional responses. It was found that the seedling of the cacao clonal CCN 51 genotype grown in soils with high Pb, Mn and Mn+Pb contents accumulated these heavy metals in the roots and leaves. Mn doses reduced the Pb uptake by root system and prevented that the Pb accumulated at toxic levels in the roots and leaves of the plants. High doses of Pb applied in soil were highly toxic to the plants, leading, in some cases, them to death. However, no Mn toxicity was observed in cocoa plants, even at high doses in the soil. Uptake of Pb and Mn by the roots and its transport into the aerial part of the plant promoted changes in photosynthesis, leaf gas exchange, respiration, carboxylation and in the instantaneous efficiency of carboxylation, reducing in the treatments with the highest concentrations of Pb, and the emission of chlorophyll fluorescence, affecting the efficiency of photosystem 2 and the production of photoassimilates. Besides that, Pb, Mn and Mn+Pb toxicities activated defense mechanisms in plants that alter the gene expression of met, psbA and psbO, increasing in plants subjected to high concentrations of Pb and the activity of the enzymes involved in the cellular detoxification of excess ROS at the leaf level. In addition, high uptake of Mn by root system was found to reduced Pb uptake in plants grown with Mn+Pb in the soil. Therefore, application of Mn in the soil can be used to mitigate the Pb toxicity in seedling of the cacao clonal CCN 51 genotype grown in contaminated soils.
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Almeida A-AF, Valle RR (2007) Ecophysiology of the cacao tree. Brazilian J Plant Physiol v 19:425–448
Almeida A-AF, Gomes FP, Araujo RP, Santos RC, Valle RR (2014) Leaf gas ex- change in species of the Theobroma genus. Photosynthetica 52:16–21. https://doi.org/10.1007/s11099-013-0048-8
Amako K, Chen G-X, Asada K (1994) Separate assays specific for ascorbate peroxidase and guaiacol peroxidase and for the chloroplastic and cytosolic isozymes of ascorbate peroxidase in plants. Plant Cell Physiol 35(3):497–504
Arévalo-Gardini E, Arévalo-Hernández CO, Baligar VC, He ZL (2017) Heavy metal accumulation in leaves and beans of cacao (Theobroma cacao L.) in major cacao growing regions in Peru. Sci Total Environ v 605/606:792–800
Arguello D, Chavez E, Lauryssen F, Vanderschueren R, Smolders E, Montalvo D (2019) Soil properties and agronomic factors affecting cadmium concentrations in cacao beans: a nationwide survey in Ecuador. Sci. Total Environ. 649:120–127
Auguy F, Fahr M, Moulin P, Brugel A, Laplaze L, El Mzibri M, Smouni A (2013) Lead tolerance and accumulation in Hirschfeldia incana, a Mediterranean Brassicaceae from metalliferous mine spoils. PLoS ONE 8(5):e61932
Ashraf U, Kanu AS, Mo Z, Hussain S, Anjum SA, Khan I, Tang X (2015) Lead toxicity in rice: effects, mechanisms, and mitigation strategies—a mini review. Environ Sci Pollut Res 22(23):18318–18332
Baker NR (2008) Chlorophyll florescence: a probe ofphotosynthesis in vivo. Annu Rev Plant Biol 113:59–89
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil v 39(n. 1):205–207
Bhaduri AM, Fulekar MH (2012) Antioxidant enzyme responses of plants to heavy metal stress. Rev Environ Sc Bio/Technol 11(1):55–69
Boza EJ, Motamayor JC, Amores FM, Amador SC, Tondo CL, Livingstone DS (2014) Genetic characterization of the cacao cultivar CCN 51: its impact and significance on global cacao improvement and production. J Amer Soc Hort Sci 139(2):219–229
CAOBISCO/ECA/FCC. (2015) Cocoa Beans: chocolate and cocoa industry quality requirements. (End, M. J. e Dand, R, Editors)
Caverzan A, Passaia G, Rosa SB, Ribeiro CW, Lazzarotto F, Margis-pinheiro M (2012) Plant responses to stresses: role of ascorbate peroxidase in the antioxidant protection. Genet Mol Biol 35(4):1011–1019
Chávez E, He ZL, Stoffella PJ, Mylavarapu RS, Li YC, Moyano B et al. (2016) Concentration of cadmium in cacao beans and its relationshipwith soil cadmium in southern Ecuador. Sci Total Environ 533:205–214
Chen L, Gao S, Zhu P, Liu Y, Hu T, Zhang J (2014) Comparative study of metal resistance and accumulation of lead and zinc in two poplars. Physiol Plant 151(4):390–405
Clemens S, Aarts MG, Thomine S, Verbruggen N (2013) Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci. 18(2):92–99
Dalcorso G, Manara A, Furini A (2013) An overview of heavy metal challenge in plants: from roots to shoots. Metallomics 5:11–17
De Souza SCR, De Andrade SAL, De Souza LA, Schiavinato MA (2012) Lead tolerance and phytoremediation potential of Brazilian leguminous tree species at the seedling stage. J Environ Manag 110:299–307
Emami AS, Kouchaksaraei MT, Bahramifar N, Salehi A (2016) Gas exchange responses of two poplar clones (Populus euramericana (Dode) Guinier 561/41 and Populus nigra Linnaeus 63/135) to lead toxicity. J For Sci 62(9):422–428
Gill SS, Khana NA, Tujeta N (2012) Cadmium at high dose perturbs growth, photosynthesis and nitrogen metabolism while at low dose it up regulates sulfur assimilation and antioxidant machinery in garden cress (Lepidium sativum L.). Plant Sci v 182:112–120
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem v 48:909–930
Guest CA, Schulze DG, Thompson IA, Huber DM (2002) Correlating manganese X-ray absorption near-edge structure spectra with extractable soil manganese. Soil Sci Soc Am J v 66:1172–1181
Gupta DK, Huang HG, Corpas FJ (2013) Lead tolerance in plants: strategies for phytoremediation. Environ Sci Pollut Res 20(4):2150–2161
Gramlich A, Tandy S, Andres C, Chincheros Paniagua J, Armengot L, Schneider M, Schulin R (2017) Cadmium uptake by cocoa in agroforestry and monoculture systems under conventional and organic management. Sci Total Environ 580:677–686
Gramlich A, Tandy S, Gauggel C, Lopez M, Perla D, Gonzalez V, Schulin R (2018) Soil cadmium uptake by cocoa in Honduras. Sci. Total Environ. 612:370–378
Han Y, Wang L, Zhang X, Korpelainen H, Li C (2013) Sexual differences in photosynthetic activity, ultrastructure and phytoremediation potential of Populus cathayana exposed to lead and drought. Tree Physiol 33(10):1043–1060
Hossain MA, Hasanuzzaman M, Fujita M (2010) Up-regulation of antioxidant and glyoxalase systems by exogenous glycinebetaine and proline in mung bean confer tolerance to cadmium stress. Physiol Mol Biol Plants v 16(3):259–272
ICCO, (2018) Quarterly Bulletin of Cocoa Statistics, Vol. XLIII, No. 3, Cocoa year 2017/18. Disponível em: https://www.icco.org. Acesso em setembro de 2018
IBGE, (2018) Levantamento Sistemático da Produção Agrícola—LSPA. Disponível em: https://sidra.ibge.gov.br/home/lspa/bahia. Acesso em: fevereiro de 2018
Inoue H, Fukuoka D, Tatai Y, Kamachi H, Hayatsu M, Ono M, Suzuki S (2013) Properties of lead deposits in cell walls of radish (Raphanus sativus) roots. J. Plant Res. 126:51e61
Kalaji HM, Goltsev V, Bosa K, Allakhverdiev SI, Strasser RJ, Govindjee (2012) Experimental in vivo measurements of light emission in plants: a perspective dedicated to David Walker. Photosynth Res 114:69–96. https://doi.org/10.1007/s11120-012-9780-3
Khedr AH, Abbas MA, Wahid AA, Quick WP, Abogadallah GM (2003) Proline induces the expression of salt‐stress‐responsive proteins and may improve the adaptation of Pancratium maritimum L. to salt‐stress. J Exp Bot 54:2553–2562. https://doi.org/10.1093/jxb/erg277
Kratz S, Schick J, Schnug E (2016) Trace elements in rock phosphates and P containing mineral and organo-mineral fertilizers sold in Germany. Sci Total Environ v 542:1013–1019
Krzesłowska M, Rabe I, Basinska A, Lewandowski M, Mellerowicz EJ, Napieralska A, Samardakiewicz S, Wozny A (2016) Pectinous cell wall thickenings formation e A common defense strategy of plants to cope with Pb. Environ Pollut 214:354–361
Kumar GH, Kumari JP (2015) Heavy metal lead influative toxicity and its assessment in phytoremediating plants—a review. Water Air Soil Pollut 226(10):324
Le Gall H, Philippe F, Domon JM, Gillet F, Pelloux J, Rayon C (2015) Cell wall metabolism in response to abiotic stress. Plants 4(1):112–166
Lee SH, Ahsan N, Lee KW (2007) Simultaneous overexpression of both Cu-Zn superoxide dismutase and ascorbate peroxidase in transgenic tall fescue plants confers increased tolerance to a wide range of abiotic stresses. Plant Physiol 164:1626–1638
Li P, Song A, Li Z, Fan F, Liang Y (2015) Silicon ameliorates manganese toxicity by regulating both physiological processes and expression of genes associated with photosynthesis in rice (Oryza sativa L.). Plant Soil 397(1-2):289–301
Livak KJ, Schmittgen TD (2013) Analysis of relative gene expression data using real-time quantitative PCR and the 2–DDC T method. Methods v 25:402–408
Millaleo R, Reyes-Díaz M, Ivanov AG, Mora ML, Alberdi M (2010) Manganese as essential and toxic element for plants: transport, accumulation and resistance mechanisms. J. Soil Sci. Plant Nutr. 10:470–481. https://doi.org/10.4067/S0718-95162010000200008
Millaleo R et al. (2013) Excess manganese differentially inhibits photosystem I versus II in Arabidopsis thaliana. J Exp Botany v 64:343–354
Motamayor JC, Risterucci AM, Heath M, Lanaud C (2003) Cacao domestication II: Progenitor germplasm of the Trinitario cacao cultivar. Heredity 91:322–330
Murakami M, Nakagawa F, Aem N, Ito M, Arao T (2009) Phytoextraction by rice capable of accumulating Cd at high levels: reduction ofCd content of rice grain. Environ Sci Technol 43:5878e5883
Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8(3):199–216
Navrot N, Rouhier N, Gelhaye E, Jacquot J-P (2007) Reactive oxygen species generation and antioxidant systems in plant mitochondria. Physiol Plant v 129:185–195
Nakano Y, Asada K (1981) Hydrogen perox-ide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiology 22:867–880
Nelson N, Yocum CF (2006) Structure and function of photosystems I and II Annu Rev Plant Biol 57:521–565
Ovečka M, Takáč T (2014) Managing heavy metal toxicity stress in plants: biological and biotechnological tools. Biotechnol Adv 32(1):73–86
Page V, Weisskopf L, Feller U (2006) Heavy metals in white lupin: uptake, root-to-shoot transfer and redistribution within the plant. N Phytol 171:329–341
Pendias K, Pendias H (1992) Trace elements in soils and plants. CRR Press, USA, p 365
Pourrut B, Shahid M, Dumat C, Winterton P, & Pinelli E (2011) Lead uptake, toxicity, and detoxification in plants. In: Reviews of environmental contamination and toxicology volume 213. Springer, New York, p 113–136
Popelkova H, Yocum CF (2011) PsbO, the manganese-stabilizing protein: analysis of the structure–function relations that provide insights into its role in photosystem II. J Photochem Photobiol B Biol 104(1):179–190
Ramtahal G, Yen IC, Bekele I, Bekele F, Wilson L, Maharaj K, Harrynanan L (2016) Relationships between cadmium in tissues of cacao trees and soils in plantations of Trinidad and Tobago. Food Nutr Sci 07(01):37–43
Reis GSM, De Almeida A-AF, DE Almeida NM, DE Castro AV, Mangabeira PAO, Pirovani CP (2015) Molecular, biochemical and ultrastructural changes induced by Pb toxicity in seedlings of Theobroma cacao L. PLoS ONE 10(7):e0129696
Sanità Di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Botany 41:105–130
Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal‐induced oxidative stress and protection by mycorrhization. J Exp Botany v 53:1351–1365
Siddiq M, Sinha NK, Cash JN (1992) Characterization of polyphenoloxidase from Stanley plums. J Food Sci 57(5):1177–1179
Shahid M, Dumat C, Pourrut B, Sabir M, Pinelli E (2014) Assessing the effect of metal speciation on lead toxicity to Vicia faba pigment contents. J Geochem Explor 144:290–297
Sharma P, Dubey RS (2005) Lead toxicity in plants. Brazilian J Plant Physiol 17(1):35–52
Sharma SS, Dietz K-J (2008) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci v 14(1):1360–1385
Steinberg MK (2002) The globalization of a ceremonial tree: the case of cacao (Theobroma cacao) among the Mopan Maya. Econ Botany v 56:58–65
Souza Júnior JO (2008). Substratos e adubação para mudas clonais de cacaueiro. Tese (Doutorado), ESALQ/USP, Piracicaba.
ST. Clair SB (2004) Mineral stress: the missing link in understanding how global climate change will affect plants in real world soils. Field Crops Res v 90:101–115
Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R (2014) Abiotic and biotic stress combinations. New Phytol. 203:32–43
Sytar O, Kumar A, Latowski D, Kuczynska P, Strzałka K, PRASAD MNV (2013) Heavy metal-induced oxidative damage, defense reactions, and detoxification mechanisms in plants. Acta Physiol Plant 35(4):985–999
Szabados L, Savoure A (2009) Proline: a multifunctional amino acid. Trends Plant Sci v 15(2):89–97
Yanga S-L, Lan S-S, Gong M (2009) Hydrogen peroxide-induced proline and metabolic pathway of its accumulation in maize seedlings. J Plant Physiol v 166:1694–1699
Yao YA, Wang J, Ma X, Lutts S, Sun C, MA J, Yang Y, Achal V, Xu G (2012) Proteomic analysis of Mn-induced resistance to powdery mildew in grapevine. J Exp Bot 63:5155–5170
Zhou J, Wan H, Qin S, He J, Lyu D, Li H (2016) Net cadmiumflux and gene expression in relation to differences in cadmium accumulation and translocation in four apple rootstocks. Environ Exp Bot 130:95–105
The authors of this work thank the UESC Plant Physiology group for their support in setting up and evaluating the experiment, as well as the Organization of American States (OAS) and CAPES.
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Apraez Muñoz, J.J., de Almeida, AA.F., Pirovani, C.P. et al. Mitigation of Pb toxicity by Mn in seedling of the cacao clonal CCN 51 genotype grown in soil: physiological, biochemical, nutritional and molecular responses. Ecotoxicology 30, 240–256 (2021). https://doi.org/10.1007/s10646-021-02348-y
- Heavy metal
- Gene expression
- Mineral nutrients
- Physiological parameters