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Mitigation of Pb toxicity by Mn in seedling of the cacao clonal CCN 51 genotype grown in soil: physiological, biochemical, nutritional and molecular responses

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Abstract

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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The data contained in this research were the result of the evaluation of the variables and the measurements made by the work team.

References

  • Almeida A-AF, Valle RR (2007) Ecophysiology of the cacao tree. Brazilian J Plant Physiol v 19:425–448

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Baker NR (2008) Chlorophyll florescence: a probe ofphotosynthesis in vivo. Annu Rev Plant Biol 113:59–89

    Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil v 39(n. 1):205–207

    Google Scholar 

  • Bhaduri AM, Fulekar MH (2012) Antioxidant enzyme responses of plants to heavy metal stress. Rev Environ Sc Bio/Technol 11(1):55–69

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Dalcorso G, Manara A, Furini A (2013) An overview of heavy metal challenge in plants: from roots to shoots. Metallomics 5:11–17

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Gupta DK, Huang HG, Corpas FJ (2013) Lead tolerance in plants: strategies for phytoremediation. Environ Sci Pollut Res 20(4):2150–2161

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Millaleo R et al. (2013) Excess manganese differentially inhibits photosystem I versus II in Arabidopsis thaliana. J Exp Botany v 64:343–354

    Google Scholar 

  • Motamayor JC, Risterucci AM, Heath M, Lanaud C (2003) Cacao domestication II: Progenitor germplasm of the Trinitario cacao cultivar. Heredity 91:322–330

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8(3):199–216

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Ovečka M, Takáč T (2014) Managing heavy metal toxicity stress in plants: biological and biotechnological tools. Biotechnol Adv 32(1):73–86

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Sanità Di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Botany 41:105–130

    Google Scholar 

  • 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

    Google Scholar 

  • Siddiq M, Sinha NK, Cash JN (1992) Characterization of polyphenoloxidase from Stanley plums. J Food Sci 57(5):1177–1179

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Sharma P, Dubey RS (2005) Lead toxicity in plants. Brazilian J Plant Physiol 17(1):35–52

    CAS  Google Scholar 

  • Sharma SS, Dietz K-J (2008) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci v 14(1):1360–1385

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R (2014) Abiotic and biotic stress combinations. New Phytol. 203:32–43

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Szabados L, Savoure A (2009) Proline: a multifunctional amino acid. Trends Plant Sci v 15(2):89–97

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

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Acknowledgements

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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JJAP: Collected the data; Contributed data or analysis tools; Performed the analysis; Wrote the paper. AAFA: Contributed data or analysis tools; Performed the analysis; Wrote the paper. CPP: Contributed data or analysis tools. DA: Contributed Performed the analysis. VCP: Contributed data or analysis tools.

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Correspondence to Jose Julian Apraez Muñoz.

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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

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