Biologia plantarum 66:188-200, 2022 | DOI: 10.32615/bp.2022.016
LC-MS/MS shotgun proteomics reveals biochemical mechanisms of Paspalum fasciculatum tolerance to Pb-stress
- 1 Faculty of Basic Sciences, Biology Department, Biosystematic Research Group, Technological University of Chocó, Quibdó, 270002, Colombia
- 2 Department of Biology, Analytical Chemistry and Biomedicine Group, University of Cartagena, Cartagena, 130015, Colombia
- 3 Chemistry Department, Water, Applied and Environmental Chemistry Group, University of Córdoba, Faculty of Basic Sciences, Montería, 230002, Colombia
- 4 Agroforestry and Plant Biochemistry, Proteomics, and Systems Biology Research Group, Department of Biochemistry and Molecular Biology-ETSIAM, University of Cordoba, UCO-CeiA3, 14071, Spain
Paspalum fasciculatum Willd. ex Flüggé grows in mining soils which are Cd- and Pb-contaminated where it exhibits tolerance to Pb and the ability to extract Pb from these soils. To elucidate tolerance mechanisms to Pb-stress, liquid chromatography with tandem mass spectrometry (LC-MS/MS) was used to quantify changes in the accumulation of proteins in leaves. We identified 323 proteins involved in primary metabolism and response to biotic or abiotic stresses. Although proteins involved in the processes of photosynthesis and saccharide and energy metabolism presented the greatest amount of down-regulated proteins, the plant was able to maintain photosynthetic functions and obtain energy to sustain the vital balance. P. fasciculatum based their tolerance on increased antioxidant defenses, improving the protection and repair of proteins and transduction signals to coordinate physiological response to Pb-stress. Our results provide important information to understand the tolerance mechanisms in P. fasciculatum and could be important in future molecular studies on the resistance and accumulation of Pb in plants.
Keywords: Paspalum fasciculatum, Pb-stress, shotgun proteomics, protein accumulation, tolerance mechanism.
Received: August 25, 2021; Revised: February 8, 2022; Accepted: April 1, 2022; Published online: August 8, 2022 Show citation
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References
- Acosta, M.M., Montilla, J.X., Campos, R. (ed.): Evaluation of contamination by cadmium and lead in water, soil, and sediment and analysis of environmental impacts in the sub-basin of the Balsillas River, a tributary of the Bogotá River - Universidad de la Salle, Colombia-Bogotá 2011. [In Spain.]
- Agarwal, P., Reddy, M.K., Sopory, S.K., Agarwal, P.K.: Plant Rabs: characterization, functional diversity, and role in stress tolerance. - Plant mol. Biol. Rep. 27: 417-430, 2009.
Go to original source... - Apel, K., Hirt, H.: Reactive oxygen species: metabolism, oxidative stress, and signal transduction. - Annu. Rev. Plant Biol. 55: 373-399, 2004.
Go to original source... - Arshad, M., Silvestre, J., Pinelli, E., Kallerhoff, J., Kaemmerer, M., Tarigo, A., Shahida, M., Guiresse, M., Pradere, P., Dumat, C.: A field study of lead phytoextraction by various scented Pelargonium cultivars. - Chemosphere 71: 2187-2192, 2008.
Go to original source... - Bah, A.M., Sun, H., Chen, F., Zhou, J., Dai, H., Zhang, G., Wu, F.: Comparative proteomic analysis of Typha angustifolia leaf under chromium, cadmium and lead stress. - J. Hazard. Mater. 184: 191-203, 2010.
Go to original source... - Baig, M.A., Ahmad, J., Bagheri, R., Ali, A.A., Al-Huqail, A.A., Ibrahim, M.M., Qureshi, M.I.: Proteomic and ecophysiological responses of soybean (Glycine max L.) root nodules to Pb and Hg stress. - BMC Plant Biol. 18: 283, 2018.
Go to original source... - Benyó, D., Horváth, E., Németh, E., Leviczky, T., Takács, K., Lehotai, N., Feigl, G., Kolbert, Z., Ördög, A., Gallé, R., Csiszár, J., Szabados, L., Erdei, L., Gallé, Á.: Physiological and molecular responses to heavy metal stresses suggest different detoxification mechanism of Populus deltoides and P. × canadensis. - J. Plant Physiol. 201: 62-70, 2016.
Go to original source... - Bohler, S., Sergeant, K., Jolivet, Y., Hoffmann, L., Hausman, J.F., Dizengremel, P., Renaut, J.: A physiological and proteomic study of poplar leaves during ozone exposure combined with mild drought. - Proteomics 13: 1737-1754, 2013.
Go to original source... - Bowman, S.E.J., Bren, K.L.: The chemistry and biochemistry of heme c : functional bases for covalent attachment. - Nat. Prot. Rep. 26:1118-1130, 2008.
Go to original source... - 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: 248-254. 1976.
Go to original source... - Brandt, U.: Energy Converting NADH: Quinone oxidoreductase (Complex I). - Annu. Rev. Biochem. 75: 69-92, 2006.
Go to original source... - Cao, H., Xu, Y., Yuan, L., Bian, Y., Wang, L., Zhen, S., Hu, Y., Yan, Y.: Molecular characterization of the 14-3-3 gene family in Brachypodium distachyon L. reveals high evolutionary conservation and diverse responses to abiotic stresses. - Front. Plant Sci. 7: 1099, 2016.
Go to original source... - Castillejo, M.Á., Bani, M., Rubiales, D.: Understanding pea resistance mechanisms in response to Fusarium oxysporum through proteomic analysis. - Phytochemistry 115: 44-58. 2015.
Go to original source... - Chen, T., Zhang, L., Shang, H., Liu, S., Peng, J., Gong, W., Shi, Y., Zhang, S., Li, J., Gong, J., Ge, Q., Liu, A., Ma, H., Zhao, X., Yuan, Y.: ITRAQ-based quantitative proteomic analysis of cotton roots and leaves reveals pathways associated with salt stress. - PLoS ONE 11: 1-15, 2016.
Go to original source... - Chen, Z., Zhu, D., Wu, J., Cheng, Z., Yan, X., Deng, X., Yan, Y.: Identification of differentially accumulated proteins involved in regulating independent and combined osmosis and cadmium stress response in Brachypodium seedling roots. - Sci. Rep. 8: 1-17, 2018.
Go to original source... - Cheng, L., Gao, X., Li, S., He, G.Y.Á.G.: Proteomic analysis of soybean [Glycine max ( L .) Meer] seeds during imbibition at chilling temperature. - Mol. Breed. 26:1-17, 2010.
Go to original source... - Cravatt, B.F., Simon, G.M., Yates, J.R.Y.: The biological impact of mass-spectrometry-based proteomics. - Nature 450: 991-1000, 2007.
Go to original source... - Dietz, K.J.: The dual function of plant peroxiredoxins in antioxidant defence and redox signaling. - Subcell. Biochem. 44: 267-294, 2007.
Go to original source... - Driedonks, N., Xu, J., Peters, J.L., Park, S., Rieu, I.: Multi-level interactions between heat shock factors, heat shock proteins, and the redox system regulate acclimation to heat. - Front. Plant Sci. 6: 1-9, 2015.
Go to original source... - Falhof, J., Pedersen, J.T., Fuglsang, A.T., Palmgren, M.: Plasma membrane H+-ATPase regulation in the center of plant physiology. - Mol. Plants 9: 323-337, 2016.
Go to original source... - 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. - BBA Bioenergetics 1706: 158-164, 2005.
Go to original source... - Farooq, M.A., Zhang, K., Islam, F., Wang, J., Athar, H.U.R., Nawaz, A., Zafar, Z.U., Xu, J., Zhou, W.: Physiological and iTRAQ-based quantitative proteomics analysis of methyl jasmonate-induced tolerance in Brassica napus under arsenic stress. - Proteomics 18: 1-13, 2018.
Go to original source... - Ge, P., Ma, C., Wang, S., Gao, L., Li, X., Guo, G., Ma, W., Yan, Y.: Comparative proteomic analysis of grain development in two spring wheat varieties under drought stress. - Anal. Bioanal. Chem. 402: 1297-1313, 2012.
Go to original source... - Goodwin, S.B., Sutter, T.R..: Microarray analysis of Arabidopsis genome response to aluminum stress. - Biol. Plant. 53: 85-99, 2009.
Go to original source... - Han, H., Zhang, H., Qin, S., Zhang, J., Yao, L., Chen, Z., Yang, J.: Mechanisms of Enterobacter bugandensis TJ6 immobilization of heavy metals and inhibition of Cd and Pb uptake by wheat based on metabolomics and proteomics. - Chemosphere 276: 130157, 2021.
Go to original source... - Haq, S., Khan, A., Ali, M., Khattak, A.M., Gai, W., Zhang, H., Wei, A., Gong, Z.: Heat shock proteins : dynamic biomolecules to counter plant biotic and abiotic stresses. - Int. J. mol. Sci. 20: 5321, 2019.
Go to original source... - Hasan, M.K., Cheng, Y., Kanwar, M.K., Chu, X.Y., Ahammed, G.J., Qi, Z.Y.: Responses of plant proteins to heavy metal stress - a review. - Front. Plant Sci. 8: 1-16, 2017.
Go to original source... - Hossain, M.A., Piyatida, P., Da Silva, J.A.T., Fujita, M.: Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. - J. Bot. 2012: 1-37, 2012.
Go to original source... - Janicka-Russak, M.: Plant plasma membrane H+-ATPase in adaptation of plants to abiotic stresses. -In: Shanker, A. (ed.): Abiotic Stress Response in Plants. Physiological, Biochemical and Genetic Perspectives. Pp. 197-218. InTech, Rijeka 2016.
- Jedrzejczak, R.: Determination of total mercury in foods of plant origin in Poland by cold vapour atomic absorption spectrometry. - Food Additives and Contaminants 19: 996-1002, 2002.
Go to original source... - Jiang, L., Wang, W., Chen, Z., Gao, Q., Xu, Q., Cao, H.: A role for APX1 gene in lead tolerance in Arabidopsis thaliana. - Plant Sci. 256: 94-102, 2017.
Go to original source... - Kabala, K., Janicka-Russak, M., Reda, M., Migocka, M. Transcriptional regulation of the V-ATPase subunit c and V-PPase isoforms in Cucumis sativus under heavy metal stress. Physiol. Plant. 150: 32-45, 2014.
Go to original source... - Kato, Y., Sakamoto, W.: FtsH protease in the thylakoid membrane: physiological functions and the regulation of protease activity. - Front. Plant Sci. 9: 1-8, 2018.
Go to original source... - Khan, M.M., Islam, E., Irem, S., Akhtar, K., Ashraf, M.Y., Iqbal, J., Liu, D.: Pb-induced phytotoxicity in para grass (Brachiaria mutica) and castorbean (Ricinus communis L.): antioxidant and ultrastructural studies. - Chemosphere 200: 257-265, 2018.
Go to original source... - Kosová, K., Vítámvás, P., Planchon, S., Renaut, J., Vaňková, R., Práąil, I.T.: Proteome analysis of cold response in spring and winter wheat (Triticum aestivum) crowns reveals similarities in stress adaptation and differences in regulatory processes between the growth habits. - J. Proteome Res. 12: 4830-4845, 2013.
Go to original source... - Kosová, K., Vítámvás, P., Práąil, I.T., Renaut, J.: Plant proteome changes under abiotic stress - Contribution of proteomics studies to understanding plant stress response. - J. Proteom. 74: 1301-1322, 2011.
Go to original source... - Kumar, A., Narasimha, M., Prasad, V.: Plant-lead interactions : transport, toxicity, tolerance, and detoxification mechanisms. - Ecotoxicol. Environ. Safety 166: 401-418, 2018.
Go to original source... - Kumar, S.P., Arun, P., Varman, M., Kumari, B.D.R.: Identification of differentially expressed proteins in response to Pb stress in Catharanthus roseus. - Afr. J. environ. Sci. Technol. 5: 689-699, 2011.
- Kuppusamy, S., Palanisami, T., Megharaj, M., Venkateswarlu, K., Naidu, R.: In-situ remediation approaches for the management of contaminated sites: a comprehensive overview. In: De Voogt, P. (ed.): Reviews of environmental contamination and toxicology. 236. Cham: Springer. Pp. 1-115, 2016.
Go to original source... - Lan, X.Y., Yan, Y.Y., Yang, B., Li, X.Y., Xu, F.L.: Differential expression of proteins in the leaves and roots of cadmium-stressed Microsorum pteropus, a novel potential aquatic cadmium hyperaccumulator. - Sci. total Environ. 642: 1369-1377, 2018.
Go to original source... - Li, X., Zhou, Y., Yang, Y., Yang, S., Sun, X., Yang, Y.: Physiological and proteomics analyses reveal the mechanism of Eichhornia crassipes tolerance to high-concentration cadmium stress compared with Pistia stratiotes. - PLoS ONE 10: 1-22, 2015.
Go to original source... - López-Orenes, A., Dias, M.C., Ferrer, M.Á., Calderón, A., Moutinho-Pereira, J., Correia, C., Santos, C.: Different mechanisms of the metalliferous Zygophyllum fabago shoots and roots to cope with Pb toxicity. - Environ. Sci. Pollut. Res. 25: 1319-1330, 2018.
Go to original source... - Ludwig, A., Rehberg, S., Wegner, M.: Melanocyte-specific expression of dopachrome tautomerase is dependent on synergistic gene activation by the Sox10 and Mitf transcription factors. - FEBS Lett. 556: 236-244, 2004.
Go to original source... - Ma, Y., Egodawatta, P., McGree, J., Liu, A., Goonetilleke, A.: Human health risk assessment of heavy metals in urban stormwater. - Sci. Total Environ. 557-558: 764-772, 2016.
Go to original source... - Mahdavian, K., Ghaderian, S.M., Torkzadeh-Mahani, M.: Accumulation and phytoremediation of Pb, Zn, and Ag by plants growing on Koshk lead-zinc mining area, Iran. - J. Soils Sediments 17: 1310-1320, 2017.
Go to original source... - McCarthy, F.M., Gresham, C.R., Buza, T.J., Chouvarine, P., Pillai, L.R., Kumar, R., Ozkan, S., Wang, H., Manda, P., Arick, T., Bridges, S.M., Burgess, S.C.: AgBase: supporting functional modeling in agricultural organisms. - Nucleic Acids Res. 39(Suppl. 1): D497-D506, 2010.
Go to original source... - Nikkanen, L., Rintamäki, E.: Chloroplast thioredoxin systems dynamically regulate photosynthesis in plants. - Biochem. J. 476: 1159-1172, 2019.
Go to original source... - Obiora, S.C., Chukwu, A., Toteu, S.F., Davies, T.C.: Assessment of heavy metal contamination in soils around lead (Pb)-zinc (Zn) mining areas in Enyigba, southeastern Nigeria. - J. geol. Soc. India 87: 453-462, 2016.
Go to original source... - Pang, M., Bai, X.Y., Li, Y., Bai, J.Z., Yuan, L.R., Ren, S.A., Hu, X.Y., Zhang, X.R., Yu, B.F., Guo, R., Wang, H.L.: Label-free LC-MS/MS shotgun proteomics to investigate the anti-inflammatory effect of rCC16. - Mol. Med. Rep. 14: 4496-4504, 2016.
Go to original source... - Pascual, J., Canal, M.J., Escandon, M., Meijon, M.,Weckwerth, W., Valledor, L.: Integrated physiological, proteomic, and metabolomic analysis of ultra violet (UV) stress responses and adaptation mechanisms in pinus radiata. - Mol. Cell. Proteomics 16: 485-501, 2017.
Go to original source... - Peng, W., Li, X., Xiao, S., Fan, W.: Review of remediation technologies for sediments contaminated by heavy metals. - J. Soils Sediments 18: 1701-1719, 2018.
Go to original source... - Potocký, M., Jones, M.A., Bezvoda, R., Smirnoff, N., ®árský, V.: Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growth. - New Phytol. 174: 742-751, 2007.
Go to original source... - Pourrut, B., Perchet, G., Silvestre, J., Cecchi; M., Guiresse, M., Pinelli, E.: Potential role of NADPH-oxidase in early steps of lead-induced oxidative burst in Vicia faba roots. - J. Integr. Plant Biol. 165: 571-579, 2008.
Go to original source... - Pourrut, B., Shahid, M., Douay, F., Dumat, C., Pinelli, E.: Molecular Mechanisms Involved in Lead Uptake, Toxicity and Detoxification in Higher Plants. - In: D. K. Gupta et al. (eds.), Heavy Metal Stress in Plants, Heavy Metal Stress in Plants, 121-147, Springer-Verlag Berlin Heidelberg, 2013.
Go to original source... - Prasad, A., Kumar, A., Suzuki, M., Kikuchi, H., Sugai, T., Kobayashi, M., Pospíąil, P., Tada, M., Kasai, S.: Detection of hydrogen peroxide in photosystem II (PSII) using catalytic amperometric biosensor. - Front. Plant Sci. 6: 1-10, 2015.
Go to original source... - Price, A.H., Taylor, A., Ripley, S.J., Griffiths, A., Trewavas, A.J., Knight, M.R.: Oxidative signals in tobacco increase cytosolic calcium. - Plant Cell 6: 1301-1310, 1994.
Go to original source... - Rey, P., Sanz-Barrio, R., Innocenti, G., Ksas, B., Courteille, A., Rumeau, D., Issakidis-Bourguet, E., Farran, I.: Overexpression of plastidial thioredoxins f and m differentially alters photosynthetic activity and response to oxidative stress in tobacco plants. - Front. Plant Sci. 4: 390, 2013.
Go to original source... - Riva-Roveda, L., Escale, B., Giauffret, C., Périlleux, C.: Maize plants can enter a standby mode to cope with chilling stress. - BMC Plant Biol. 16: 212, 2016.
Go to original source... - Rodriguez, E., Da Conceição, S.M., Azevedo, R., Correia, C., Moutinho-Pereira, J., De Ferreira, O.J.M., Dias, M.C.: Photosynthesis light-independent reactions are sensitive biomarkers to monitor lead phytotoxicity in a Pb-tolerant Pisum sativum cultivar. - Environ. Sci. Pollut. Res. 22: 574-585, 2015.
Go to original source... - Sahi, S.V., Sharma, N.C.: Phytoremadiation of lead. In: Shtangevaa I (Eds) Trace and ultrace elements in plants and soil. Series advanceds in ecological research. - Witpress Southampton Pp. 209-222, 2005.
- Salas-Moreno, M., Contreras-Puentes, N., Rodríguez-Cavallo, E., Jorrín-Novo, J.: Protein carbonylation as a biomarker of heavy metal, Cd and Pb, damage in Paspalum fasciculatum Willd. ex Flüggé. - Plant 8: 1-18, 2019.
Go to original source... - Salas-Moreno, M., Marrugo-Negrete, J.: Phytoremediation potential of Cd and Pb-contaminated soils by Paspalum fasciculatum Willd. ex Flüggé. - Int. J. Phytoremediation. 6514: 1-11, 2019.
Go to original source... - Shahid, M., Pourrut, B., Dumat, C., Nadeem, M., Aslam, M., Pinelli, E.: Heavy-Metal-Induced Reactive Oxygen Species: Phytotoxicity and Physicochemical Changes in Plants. - In: D.M. Whitacre (ed.), Reviews of Environmental Contamination and Toxicology, Volume 232, Pp 1-44, Springer International, Publishing, Switzerland, 2014.
Go to original source... - Siedlecka, A., BaszyńAski, T.: Inhibition of electron flow around photosystem I in chloroplasts of Cd-treated maize plants is due to Cd-induced iron deficiency. - Physiol. Plant. 87: 199-202, 1993.
Go to original source... - Simiele, M., Sferra, G., Lebrun, M., Renzone, G., Bourgerie, S., Scippa, G.S., Morabito, D., Scaloni, A., Trupiano, D.: In-depth study to decipher mechanisms underlying Arabidopsis thaliana tolerance to metal(loid) soil contamination in association with biochar and/or bacteria. - Environ. Exp. Bot. 182: 104335, 2021.
Go to original source... - Singh, S., Parihar, P., Singh, R., Singh, V.P., Prasad, S.M.: Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. - Front. Plant Sci. 6: 1-36, 2016.
Go to original source... - Singh, S., Singh, A.: Phytoremediation : a sustainable approach for restoration of metal-contaminated sites. - Int. J. Sci. Res. 5: 2171-2174, 2016.
Go to original source... - Shen, C.-C., Chen, M.-X., Xiao, T., Zhang, C., Shang, J., Zhang, K.-L., Zhu, F.-Y.: Global proteome response to Pb(II) toxicity in poplar using SWATH-MS-based quantitative proteomics investigation. - Ecotoxicol. Environ. Safety 220:112410, 2021.
Go to original source... - Smolińska, B., Cedzyńska, K.: EDTA and urease effects on Hg accumulation by Lepidium sativum. - Chemosphere 69: 1388-1395, 2007.
Go to original source... - Su, T., Si, M., Zhao, Y., Liu, Y., Yao, S., Che, C., Chen, C.: A thioredoxin-dependent peroxiredoxin Q from Corynebacterium glutamicum plays an important role in defense against oxidative stress. - PLoS ONE 13: 1-23, 2018.
Go to original source... - Szuba, A., Marczak, Ł., Kozłowski, R.: Pb stress and ectomycorrhizas: strong protective proteomic responses in poplar roots inoculated with Paxillus involutus isolate and characterized by low root colonization intensity. - Int. J. mol. Sci. 22: 4300, 2021.
Go to original source... - Taiwo, A.M., Gbadebo, A.M., Oyedepo, J.A., Ojekunle, Z.O., Alo, O.M., Oyeniran, A.A., Onalaja, O.J.; Ogunjimi, D., Taiwo, O.T.: Bioremediation of industrially contaminated soil using compost and plant technology. - J. Hazard Mater. 304: 166-172, 2016.
Go to original source... - Takahashi, S., Murata, N.: How do environmental stresses accelerate photoinhibition? - Trends Plant Sci. 13: 178-182, 2008.
Go to original source... - Valko, M., Rhodes, C.J., Moncol, J., Izakovic, M., Mazur, M.: Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem. biol. Interact. 160: 1-40, 2006.
Go to original source... - Venkatachalam, P., Jayalakshmi, N., Geetha, N., Shivendra, V., Sharma, N.C., Rene, E.R., Sarkar, S.K., Favas, P.J.C.: Accumulation efficiency, genotoxicity and antioxidant defense mechanisms in medicinal plant Acalypha indica L. under lead stress. - Chemosphere 171: 544-553, 2017.
Go to original source... - Wang, C.Y., Shen, R.F., Wang, C., Wang, W.: Root protein profile changes induced by Al exposure in two rice cultivars differing in Al tolerance. - J. Proteom. 78: 281-293, 2013.
Go to original source... - Wang, L., Yang, H., Liu, R., Fan, G.: Detoxification strategies and regulation of oxygen production and flowering of Platanus acerifolia under lead (Pb) stress by transcriptome analysis. - Environ. Sci. Pollut. Res. 22: 12747-12758, 2015.
Go to original source... - Wang, M., Zhang, C., Zhang, Z., Li, F., Guo, G.: Distribution and integrated assessment of lead in an abandoned lead-acid battery site in Southwest China before redevelopment. - Ecotoxicol. Environ. Safety 128: 126-132, 2016.
Go to original source... - Wang, W.: Vignani, R., Scali, M.., Cresti, M.: A universal and rapid protocol for protein extraction from recalcitrant plant tissues for proteomic analysis. - Electrophoresis 27: 2782-2786, 2006.
Go to original source... - Weckwerth, P., Ehlert, B., Romeis, T. : ZmCPK1, a calcium-independent kinase member of the Zea mays CDPK gene family, functions as a negative regulator in cold stress signalling. - Plant Cell Environ. 38: 544-558, 2014.
Go to original source... - Wientjes, E., Philippi, J., Borst, J.W., Van Amerongen, H.: Imaging the photosystem I/photosystem II chlorophyll ratio inside the leaf. - BBA - Bioenergetics 1858: 259-265, 2017.
Go to original source... - Wuana, R.A., Okieimen, F.E.: Heavy metals in contaminated soil. heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. - Int.Scholar Res. Notes Ecol., Pp 1-20, 2011.
Go to original source... - Weyemi, U., Dupuy, C.: The emerging role of ROS-generating NADPH oxidase NOX4 in DNA-damage responses. - Mutat. Res. 751: 77-81, 2012.
Go to original source... - Xia, C., Hong, L., Yang, Y., Yanping, X., Xing, H., Gang, D.: Protein changes in response to lead stress of lead-tolerant and lead-sensitive industrial hemp using SWATH technology. - Genes 10: 396, 2019.
Go to original source... - Yang, G., Wang, C., Wang, Y., Guo, Y., Zhao, Y., Yang, C., Gao, C.: Overexpression of ThVHAc1 and its potential upstream regulator, ThWRKY7, improved plant tolerance of cadmium stress. - Sci. Rep. 6: 1-17, 2016.
Go to original source... - Yao, Y., Ni, Z., Du, J., Wang, X., Wu, H., Sun, Q.: Isolation and characterization of 15 genes encoding ribosomal proteins in wheat (Triticum aestivum L.). - Plant Sci. 170: 579-586, 2006.
Go to original source... - Zhang, J., Wei, J., Li, D., Kong, X., Rengel, Z., Chen, L., Yang, Y., Cui, X., Chen, Q.: The role of the plasma membrane H+-ATPase in plant responses to aluminum toxicity. - Front. Plant Sci. 8: 1-9, 2017.
Go to original source...



