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Enhancing the potential for cadmium phytoremediation by introducing Perilla frutescens genes in tobacco

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Abstract

To improve the potential of cadmium phytoremediation, distant hybridization between tobacco (Nicotiana tabacum L. var. 78–04), a high-biomass crop, and Perilla frutescens var. frutescens, a wild Cd-hyperaccumulator, was carried out, developing a new variety N. tabacum L. var. ZSY. Seedlings at the six-leaf stage were grown in hydroponics and treated with 0 (control), 10 µM, 180 µM, and 360 µM CdCl2 for 7 days; then, the differences in Cd tolerance and accumulation and physiological and metabolic responses were evaluated among “ZSY” and its parents. At high Cd dose, the growth of “ZSY,” such as fresh weight, plant height, and root length, was evidently better than “78–04.” In contrast to P. frutescens and “78–04,” “ZSY” could accumulate more Cd in shoots than roots. Under the same treatment, “ZSY” accumulated greater amounts of Cd in both shoots (195–1523 mg kg−1) and roots (140–1281 mg kg−1) than “78–04” (shoots: 35–89 mg kg−1, roots: 39–252 mg kg−1), followed by P. frutescens (shoots: 156–454 mg kg−1, roots: 103–761 mg kg−1). BCF and TF values of “ZSY” reached 38–195 and 1.2–1.4, which were far higher than those of “78–04” (BCF: 2.2–35.3, TF: 0.35–0.9). Perilla frutescens was found with BCF and TF of 11–156 and 0.5–1.5. Cd stress obviously promoted the production of ROS and MDA in seedlings but reduced chlorophyll contents, especially in “78–04.” As a response to Cd stress, “ZSY” had higher SOD and CAT activities when compared to P. frutescens and “78–04,” while “78–04” produced more POD and proline than those of P. frutescens and “ZSY.” Cd stress could affect the production and accumulation of alkaloids and phenolic compounds in root (endodermis and cortex) and mesophyll. At high Cd doses, P. frutescens and “ZSY” had more alkaloids in tissues than “78–04.” Phenolic compounds in “78–04” were more obviously inhibited compared with P. frutescens and “ZSY.” These secondary metabolites may play an important role in eliminating oxidative damage and enhancing Cd tolerance and accumulation in “ZSY” and P. frutescens. Results indicated that distant hybridization could be one of effective methods for introducing excellent genes from metal-hyperaccumulators into high biomass species, creating plants with superior phytoremediation potential.

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References

  • Alkorta I, Hernandez-Allica J, Becerril JM, Amezaga I, Albizu I, Garbisu C (2004) Recent findings on the phytoremediation of soils contaminated with environmentally toxic heavy metals and metalloids such as zinc, cadmium, lead, and arsenic. Rev Environ Sci Bio-Technol 3:71–90

    Article  CAS  Google Scholar 

  • Argyropoulou C, Akoumianaki-Ioannidou A, Christodoulakis NS, Fasseas C (2010) Leaf anatomy and histochemistry of Lippia citriodora (Verbenaceae). Aust J Bot 58:398–409

    Article  Google Scholar 

  • Assunção AG, Pieper B, Vromans J, Lindhout P, Aarts MG, Schat H (2006) Construction of a genetic linkage map of Thlaspi caerulescens and quantitative trait loci analysis of zinc accumulation. New Phytol 1:21–32

    Article  Google Scholar 

  • Bhargava A, Carmona FF, Bhargava M, Srivastava S (2012) Approaches for enhanced phytoextraction of heavy metals. J Environ Manage 105:103–120

    Article  CAS  Google Scholar 

  • Boojar MMA, Goodarzi F (2007) The copper tolerance strategies and the role of antioxidative enzymes in three plant species grown on copper mine. Chemosphere 67(11):2138–2147

    Article  CAS  Google Scholar 

  • Boudet AM (2007) Evolution and current status of research in phenolic compounds. Phytochemistry 68:2722–2735

    Article  CAS  Google Scholar 

  • Bradford MM (1976) 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

    Article  CAS  Google Scholar 

  • Chen SH, Chen X, Dou WH, Wang L, Yin HB, Guo SL (2016) GST (phi) gene from Macrophyte Lemna minor is involved in cadmium exposure responses. Chin J Oceanol Limnol 34:342–351 (in Chinese)

    Article  CAS  Google Scholar 

  • Chen Q, Lu XY, Guo XR, Pan YJ, Yu BF, Tang ZH, Guo QX (2018) Differential responses to Cd stress induced by exogenous application of Cu, Zn or Ca in the medicinal plant Catharanthus roseus. Ecotoxicol Environ Saf 157:266–275

    Article  CAS  Google Scholar 

  • Deng X, Yan X, Wei H, Zhang H, Shen Z (2010) Cadmium-induced oxidative damage and protective effects of N-acetyl-L-cysteine against cadmium toxicity in Solanum nigrum L. J Hazard Mater 180(1–3):722–729

    Article  CAS  Google Scholar 

  • Deniau AX, Pieper B, Ten Bookum WM, Lindhout P, Aarts MGM, Schat H (2006) QTL analysis of cadmium and zinc accumulation in the heavy metal hyperaccumulator Thlaspi caerulescens. Theor Appl Genet 113:907–920

    Article  CAS  Google Scholar 

  • Eapen S, D’Souza SF (2005) Prospects of genetic engineering of plants for phytoremediation of toxic metals. Biotechnol Adv 23(2):97–114

    Article  CAS  Google Scholar 

  • Emamverdian A, Ding YL, Mokhberdoran F, Xie YF (2015) Heavy metal stress and some mechanisms of plant defense response. Sci World J. https://doi.org/10.1155/2015/756120

    Article  Google Scholar 

  • Gallego SM, Pena LB, Barcia RA, Azpilicueta CE, Iannone MF, Rosales EP, Zawoznik MS, Groppa MD, Benavides MP (2012) Unravelling cadmium toxicity and tolerance in plants: Insight into regulatory mechanisms. Environ Exp Bot 83:33–46

    Article  CAS  Google Scholar 

  • Gomez AA, Mercado MI, Belizán MME, Ponessa G, Vattuone MA, Diego A, Sampietro DA (2019) In situ histochemical localization of alkaloids in leaves and pods of Prosopis ruscifolia. Flora 256:1–6

    Article  Google Scholar 

  • Gorinova N, Nedkovska M, Todorovska E, Simova-Stoilova L, Stoyanova Z, Georgieva K, Demirevska-Kepova K, Atanassov A, Herzig R (2007) Improved phytoaccumulation of cadmium by genetically modified tobacco plants (Nicotiana tabacum L.). Physiological and biochemical response of the transformants to cadmium toxicity. Environ Pollut 145(1):161–170

    Article  CAS  Google Scholar 

  • Grispen VMJ, Hakvoort HWJ, Bliek T, Verkleij JAC, Schat H (2011) Combined expression of the Arabidopsis metallothionein MT2b and the heavy metal transporting ATPase HMA4 enhances cadmium tolerance and the root to shoot translocation of cadmium and zinc in tobacco. Environ Exp Bot 72:71–76

    Article  CAS  Google Scholar 

  • Guo B, Liang YC, Zhu YG, Zhao FJ (2007) Role of salicylic acid in alleviating oxidative damage in rice roots (Oryza sativa) subjected to cadmium stress. Environ Pollut 147(3):743–749

    Article  CAS  Google Scholar 

  • Han T, Liang YP, Wu ZN, Zhang L, Liu ZW, Li QF, Chen XJ, Guo WL, Jiang LN, Pan FF, Ge SD, Mi ZR, Liu ZC, Huang H, Li XZ, Zhou JG, Li Y, Wang JL, Zhang Z, Tang YY, Yang LR, Wu MD (2019) Effects of tetracycline on growth, oxidative stress response, and metabolite pattern of ryegrass. J Hazard Mater 380:120885

    Article  CAS  Google Scholar 

  • Hassanzadeh M, Ebadi A, Panahyan-e-Kivi M, Eshghi AG, Jamaati-e-Somarin S, Saeidi M, Zabihi-e-Mahmoodabad R (2009) Evaluation of drought stress on relative water content and chlorophyll content of sesame (Sesamum indicum L) genotypes at early flowering stage. Res J Environ Sci 3(3):345–350

    Article  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplast. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  Google Scholar 

  • Hou TY, Netala VR, Zhang HJ, Xing Y, Li HZ, Zhang ZJ (2022) Perilla frutescens: a rich source of pharmacological active compounds. Molecules 27:3578

    Article  CAS  Google Scholar 

  • Iannone MF, Groppa MD, Benavides MP (2015) Cadmium induces different biochemical responses in wild type and catalase-deficient tobacco plants. Environ Exp Bot 109:201–211

    Article  CAS  Google Scholar 

  • Janošević D, Budimir S, Alimpić A, Marin P, Sheef NA, Giweli A, Duletić-Laušević S (2016) Micromorphology and histochemistry of leaf trichomes of Salvia aegyptiaca (Lamiaceae). Arch Biol Sci 68(2):291–301

    Article  Google Scholar 

  • Joo JH, Wang SY, Chen JG, Jones AM, Fedoroff NV (2005) Different signaling and cell death roles of heterotrimeric G protein α and β subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell 17:957–970

    Article  CAS  Google Scholar 

  • Katoh A, Ohki H, Inai K, Hashimoto T (2005) Molecular regulation of nicotine biosynthesis. Plant Biotechnol 22:389–392

    Article  CAS  Google Scholar 

  • Khator K, Saxena I, Shekhawat GS (2021) Nitric oxide induced Cd tolerance and phytoremediation potential of B. juncea by the modulation of antioxidant defense system and ROS detoxification. Biometals 34:15–32

    Article  CAS  Google Scholar 

  • Kim KH, Lee YH, Kim D, Park YH, Lee JY, Hwang YS, Kim YH (2004) Agrobacterium-mediated genetic transformation of Perilla frutescens. Plant Cell Rep 6:386–390

    Article  Google Scholar 

  • Liang HM, Lin TH, Chiou JM, Yeh KC (2009) Model evaluation of the phytoextraction potential of heavy metal hyperaccumulators and non-hyperaccumulators. Environ Pollut 157(6):1945–1952

    Article  CAS  Google Scholar 

  • Liu X, Zhang SR, Zhu R, Xu XX, Fan XW (2009) Effect of cadmium and copper stress on the growth response and accumulation characteristics of Perilla frutescens (L.) Britt. J Agro-Environ Sci 11:2264–2269 (in Chinese)

    Google Scholar 

  • Liu WX, Shang SH, Feng X, Zhang GP, Wu FB (2015) Modulation of exogenous selenium in cadmium-induced changes in antioxidative metabolism, cadmium uptake, and photosynthetic performance in the 2 tobacco genotypes differing in cadmium tolerance. Environ Toxicol Chem 34(1):92–99

    Article  Google Scholar 

  • Lugon-Moulin N, Martin F, Krauss MR, Ramey PB, Rossi L (2006) Cadmium concentration in tobacco (Nicotiana tabacum L.) from different countries and its relationship with other elements. Chemosphere 63(7):1074–1086

    Article  CAS  Google Scholar 

  • Manquián-Cerda K, Escudey M, Zúñiga G, Arancibia-Miranda N, Molina M, Cruces E (2016) Effect of cadmium on phenolic compounds, antioxidant enzyme activity and oxidative stress in blueberry (Vaccinium corymbosum L.) plantlets grown in vitro. Ecotoxicol Environ Saf 133:316–326

    Article  Google Scholar 

  • Martin F, Bovet L, Cordier A, Stanke M, Gunduz I, Peitsch MC, Ivanov NV (2012) Design of a tobacco exon array with application to investigate the differential cadmium accumulation property in two tobacco varieties. BMC Genomics 13(1):1–16

    Article  Google Scholar 

  • Matias LJ, Mercadante-Simões MO, Royo VA, Ribeiro LM, Santos AC, Fonseca JMS (2016) Structure and histochemistry of medicinal species of Solanum. Rev Bras 26:147–160

    CAS  Google Scholar 

  • Mesjasz-Przybylowicz J, Barnabas A, Przybyiowicz W (2007) Comparison of cytology and distribution of nickel in roots of Ni-hyperaccumulating and non-hyperaccumulating genotypes of Senecio coronatus. Plant Soil 293:61–78

    Article  CAS  Google Scholar 

  • Michalak A (2006) Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Pol J Environ Stud 15(4):523–530

    CAS  Google Scholar 

  • Qiu RL, Zhao X, Tang YT, Yu FM, Hu PJ (2009) Antioxidative response to Cd in a newly discovered cadmium hyperaccumulator, Arabis paniculata F. Chemosphere 74(1):6–12

    Article  Google Scholar 

  • Rasheed R, Ashraf MA, Arshad A, Iqbal M, Hussain I (2020) Interactive effects of chitosan and cadmium on growth, secondary metabolism, oxidative defense, and element uptake in pea (Pisum sativum L.). Arab J Geosci 13:847

    Article  CAS  Google Scholar 

  • Sa KJ, Kim JA, Lee JK (2012) Comparison of seed characteristics between the cultivated and the weedy types of Perilla species. Hortic Environ Biotechnol 4:310–315

    Article  Google Scholar 

  • Sakihama Y, Cohen MF, Grace SC, Yamasaki H (2002) Plant phenolic antioxidant and prooxidant activities: phenolics induced oxidative damage mediated by metals in plants. Toxicology 177:67–80

    Article  CAS  Google Scholar 

  • Shukla D, Huda KMK, Banu MSA, Gill SS, Tuteja R, Tuteja N (2014) OsACA6, a P-type 2B Ca2+ ATPase functions in cadmium stress tolerance in tobacco by reducing the oxidative stress load. Planta 240(4):809–824

    Article  CAS  Google Scholar 

  • Soukupová J, Cvikrová M, Albrechtová J, Rock BN, Eder J (2000) Histochemical and biochemical approaches to the study of phenolic compounds and peroxidases in needles of Norway spruce (Picea abies). New Phytol 146(3):403–414

    Article  Google Scholar 

  • Tajik S, Zarinkamar F, Soltani BM, Nazari M (2019) Induction of phenolic and flavonoid compounds in leaves of saffron (Crocus sativus L.) by salicylic acid. Sci Hortic 257:108751

    Article  CAS  Google Scholar 

  • Touati M, Bottega S, Castiglione MR, Sorce C, Béjaoui Z, Spanò C (2019) Modulation of the defence responses against Cd in willow species through a multifaceted analysis. Plant Physiol Biochem 142:125–136

    Article  CAS  Google Scholar 

  • Tozin LRS, Rodrigues TM (2017) Morphology and histochemistry of glandular trichomes in Hyptis villosa Pohl ex Benth. (Lamiaceae) and differential labeling of cytoskeletal elements. Acta Bot Bras 31(3):330–343

    Article  Google Scholar 

  • Vamerali T, Bandiera M, Mosca G (2010) Field crops for phytoremediation of metal-contaminated land. A review. Environ Chem Lett 8:1–17

    Article  CAS  Google Scholar 

  • Wang P, Liang Z, Zeng J, Li W, Sun X, Miao Z, Tang K (2008a) Generation of tobacco lines with widely different reduction in nicotine levels via RNA silencing approaches. J Biosci 2:177–184

    Article  Google Scholar 

  • Wang Z, Zhang YX, Huang ZB, Huang L (2008b) Antioxidative response of metal-accumulator and non-accumulator plants under cadmium stress. Plant Soil 310:137–149

    Article  CAS  Google Scholar 

  • Wang JB, Su LY, Yang JZ, Yuan JG, Ag Y, Qiu Q, Zhang K, Yang ZY (2015) Comparisons of cadmium subcellular distribution and chemical forms between low-Cd and high-Cd accumulation genotypes of watercress (Nasturtium officinale L. R. Br.). Plant Soil 396:325–337

    Article  CAS  Google Scholar 

  • Wei ZZ, Wei KQ (2008) Distant hybridization breeding of tobacco. China Agricultural Science and Technology Press, Beijing (in Chinese)

    Google Scholar 

  • Wei ZZ, Yan XP, Deng ZF, Yang JX, Wang YT (2005) Research on distant hybridization between tobacco and D. stramonium. Chin Tob Sci 1:1–5 (in Chinese)

    CAS  Google Scholar 

  • Wei KQ, Yang JX, Wei ZZ (2010) Chemical components and medicine ingredients in the hybrid of families between tobacco and medicinal plant Perilla frutescens (L.) Britt. Nat Prod Res Dev 22:801–806 (in Chinese)

    CAS  Google Scholar 

  • Wei KQ, Pang SX, Yang JX, Wei ZZ (2015) Enhancement of cadmium tolerance and accumulation by introducing Perilla frutescens (L.) Britt var. frutescens genes in Nicotiana tabacum L. plants. Environ Sci Pollut Res 22:5405–5416

    Article  CAS  Google Scholar 

  • Xie HL, Chen AP, Zhang FY, Xiong Y, Chen YL, Liu J, Zhou LY, Lin RY (2011) Physiological response of Perilla frutescens (L.) Britt. to cadmium. Chin J Eco-Agric 3:672–675 (in Chinese)

    Article  Google Scholar 

  • Xie LP, He XY, Shang SH, Zheng WT, Liu WX, Zhang GP, Wu FB (2014) Comparative proteomic analysis of two tobacco (Nicotiana tabacum) genotypes differing in Cd tolerance. Biometals 27:1277–1289

    Article  CAS  Google Scholar 

  • Yang XE, Feng Y, He ZL, Stoffella PJ (2005) Molecular mechanisms of heavy metal hyperaccumulation and phytoremediation. J Trace Elem Med Biol 18(4):339–353

    Article  CAS  Google Scholar 

  • Yılmaza DD, Parlak KU (2011) Changes in proline accumulation and antioxidative enzyme activities in Groenlandia densa under cadmium stress. Ecol Ind 11(2):417–423

    Article  Google Scholar 

  • Zhan XR, Chen ZH, Chen R, Shen CJ (2022) Environmental and genetic factors involved in plant protection-associated secondary metabolite biosynthesis pathways. Front Plant Sci 13:877304

    Article  Google Scholar 

  • Zhang DZ, Wang PH, Zhao HX (1990) Determination of the content of free proline in wheat leaves. Plant Physiol Commun 4:62–65

    Google Scholar 

  • Zhang QH, Yang FJ, Li BX, Zhou GZ (2007) Analysis and evaluation of heavy metals in the soil and plant system in some mining area of southwest China. J Shandong Univ Sci Technol 3:15–18 (in Chinese)

    Google Scholar 

  • Zhang X, Wu W, Zheng YL, Chen L, Cai QR (2009) Essential oil variations in different Perilla L. accessions: chemotaxonomic implications. Plant Syst Evol 281:1–10

    Article  CAS  Google Scholar 

  • Zhang J, Zhang M, Shohag MJI, Tian SK, Song HY, Feng Y, Yang XE (2016) Enhanced expression of SaHMA3 plays critical roles in Cd hyperaccumulation and hypertolerance in Cd hyperaccumulator Sedum alfredii Hance. Planta 243:577–589

    Article  CAS  Google Scholar 

  • Zheng ZG, Wu M (2004) Cadmium treatment enhances the production of alkaloid secondary metabolites in Catharanthus roseus. Plant Sci 166(2):507–514

    Article  CAS  Google Scholar 

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Funding

This work was supported by the Shanxi Provincial Key Technologies Research and Development Program (201603D321002).

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Authors and Affiliations

  1. School of Life Science, Shanxi University, 63 Nanzhonghuan East Street, Taiyuan, 030006, People’s Republic of China

    Keqiang Wei & Tingting Guo

  2. Division of Radiology and Environmental Medicine, China Institute for Radiation Protection, Taiyuan, 030006, China

    Tingting Guo

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  1. Keqiang Wei
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All authors contributed to the study conception and design. Keqiang Wei: conceptualization, methodology, supervision, writing, and funding acquisition; Tingting Guo: methodology, experiments and data analysis.

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Correspondence to Keqiang Wei.

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Highlights

• Hybrid tobacco displayed larger biomass, stronger tolerance, and higher accumulation than female parent.

• Introducing Perilla frutescens genes changed Cd distribution and accumulation in tobacco tissues.

• Introducing Perilla frutescens genes alleviated Cd-induced oxidative stress in tobacco.

• Introducing Perilla frutescens genes changed metabolic response of tobacco to Cd.

• Distant hybridization could create plant with superior phytoremediation potential.

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Wei, K., Guo, T. Enhancing the potential for cadmium phytoremediation by introducing Perilla frutescens genes in tobacco. Environ Sci Pollut Res 30, 70039–70053 (2023). https://doi.org/10.1007/s11356-023-27392-5

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