Abstract
Background and Aims
Environmental fluctuations due to anthropogenic activities show negative effects on plant growth and crop production. Among the heavy metals, cadmium (Cd) pollution is most dangerous and is devastating most of the cultivable land. The current study evaluated the Cd induced toxicity in Lycopersicon esculentum plants and the mitigating role of rhizobacteria.
Methods
Different parameters such as metal uptake, metal chelators, oxidative stress markers, antioxidative defense expression, secondary metabolites, H2O2 tagging, MDA localization and cell viability has been assessed.
Results
Cd accumulation enhanced by 64.7% in roots and 267.1% in shoots, which resulted in generating oxidative burst measured in the terms of superoxide content (54.5%), H2O2 (255.1%), and MDA (202.2%) content. Moreover, the Cd stress also modulated the activities of enzymatic antioxidants and non-enzymatic antioxidants. In addition, organic acids and metal chelators were also enhanced in plants under the influence of Cd. Inoculation of rhizobacterial strains reduced the Cd uptake in plant parts (roots and shoots), increased heavy metal tolerance index (HMTI) and reduced oxidative stress markers. Also, enzymatic antioxidants such as, SOD, POD, PPO were increased in microbe inoculated plants whereas CAT, GPOX, APOX, GST, DHAR and GR were reduced. In situ immobilization studies were also conducted in root sections of L. esculentum in which Cd localization, H2O2 accumulation, cell viability and MDA accumulation were observed using confocal and visible microscopy.
Conclusions
Reduction in the levels of H2O2, MDA and Cd accumulation along with improved cell viability was observed in the rhizobacterial inoculated plants.
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References
Aebi H (1984) Catalase in vitro methods. Enzymol 105:121–126
Al-Amri SM (2013) Improved growth, productivity and quality of tomato (Solanum lycopersicum L.) plants through application of shikimic acid. Saudi J Biol Sci 20(4):339–345
Alissa EM, Ferns GA (2011) Heavy metal poisoning and cardiovascular disease. J Toxicol 2011
Allen SE, Grimshaw HM, Rowland AP (1976) Chemical analysis. In: Chapman SB (ed) Methods in plant ecology. Blackwell Scientific Publications, Oxford, pp 335–335
Amin H, Ahmed Arain B, Abbasi MS, Amin F, Jahangir TM, Soomro NUA (2019) Evaluation of chromium phyto-toxicity, phyto-tolerance, and phyto-accumulation using biofuel plants for effective phytoremediation. Int J Phytoremed 21(4):352–363
Awasthi S, Chauhan R, Dwivedi S, Srivastava S, Srivastava S, Tripathi RD (2018) A consortium of alga (Chlorella vulgaris) and bacterium (Pseudomonas putida) for amelioration of arsenic toxicity in rice: A promising and feasible approach. Environ Exp Bot 150:115–126
Balint AF, Kovács G, Sutka J (2002) Copper tolerance of Aegilops, Triticum, Secale and triticale seedlings and copper and iron contents in their shoots. Acta Biol Szeged 46:77–78
Bashri G, Prasad SM (2015) Indole acetic acid modulates changes in growth, chlorophyll a fluorescence and antioxidant potential of Trigonella foenum-graecum L. grown under cadmium stress. Acta Physiol Plant 37(3):49
Benavides MP, Gallego SM, Tomaro ML (2005) Cadmium toxicity in plants. Braz J Plant Physiol 17(1):21–34
Bradford M.M (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
Carlberg INCER, Mannervik BENGT (1975) Purification and characterization of the flavoenzyme glutathione reductase from rat liver. J Biol Chem 250(14):5475–5480
Chen MC, Wang MK, Chiu CY, Huang PM, King HB (2001) Determination of low molecular weight dicarboxylic acids and organic functional groups in rhizosphere and bulk soils of Tsuga and Yushania in a temperate rain forest. Plant Soil 231:37–44
Chen D, Chen D, Xue R, Long J, Lin X, Lin Y, Jia L, Zeng R, Song Y (2019) Effects of boron, silicon and their interactions on cadmium accumulation and toxicity in rice plants. J Hazard Mater 367:447–455
Choudhury S, Panda P, Sahoo L, Panda SK (2013) Reactive oxygen species signaling in plants under abiotic stress. Plant Signal Behav 8(4):e23681
Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo-and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42(5):669–678
DalCorso G, Farinati S, Furini A (2010) Regulatory networks of cadmium stress in plants. Plant Signal Behav 5(6):663–667
Dalton DA, Russell SA, Hanus FJ, Pascoe GA, Evans HJ (1986) Enzymatic reactions of ascorbate and glutathione that prevent peroxide damage in soybean root nodules. Proc Natl Acad Sci 83(11):3811–3815
de Araújo RP, de Almeida AAF, Pereira LS, Mangabeira PA, Souza JO, Pirovani CP, Ahnert D, Baligar VC (2017) Photosynthetic, antioxidative, molecular and ultrastructural responses of young cacao plants to Cd toxicity in the soil. Ecotoxicol Environ Saf 144:148–157
Del Longo OT, Gonzalez CA, Pastori GM, Trippi VS (1993) Antioxidant defences under hyperoxygenic and hyperosmotic conditions in leaves of two lines of maize with differential sensitivity to drought. Plant Cell Physiol 34:1023–1028
Dhir B, Sharmila P, Saradhi PP, Nasim SA (2009) Physiological and antioxidant responses of Salvinia natans exposed to chromium-rich wastewater. Ecotoxicol Environ Saf 72(6):1790–1797
do Nascimento JL, de Almeida AAF, Barroso JP, Mangabeira PA, Ahnert D, Sousa AG, Silva JVS, Baligar VC (2018) Physiological, ultrastructural, biochemical and molecular responses of young cocoa plants to the toxicity of Cr (III) in soil. Ecotoxicol Environ Saf 159:272–283
Dourado MN, Souza LA, Martins PF, Peters LP, Piotto FA, Azevedo RA (2014) Burkholderia sp. SCMS54 triggers a global stress defense in tomato enhancing cadmium tolerance. Water Air Soil Pollut 225:2159
Fasim F, Ahmed N, Parsons R, Gadd GM (2002) Solubilization of zinc salts by bacterium isolated by the air environment of tannery. FEMS Microb Lett 213:1–6
Fleming EJ, Langdon AE, Martinez-Garcia M, Stepanauskas R, Poulton NJ, Masland EDP, Emerson D (2011) What's new is old: resolving the identity of Leptothrix ochracea using single cell genomics, pyrosequencing and FISH. PLoS One 6(3):e17769
Flohé L, Günzler WA (1984) [12] Assays of glutathione peroxidase. In: Methods in enzymology, vol 105. Academic Press, Cambridge, pp 114–120
Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155(1):2–18
Fusconi A, Repetto O, Bona E, Massa N, Gallo C, Dumas-Gaudot E, Berta G (2006) Effects of cadmium on meristem activity and nucleus ploidy in roots of Pisum sativum L. cv. Frisson seedlings. Environ Exp Bot 58(1–3):253–260
Gao Y, Miao C, Xia J, Luo C, Mao L, Zhou P, Shi W (2012) Effect of citric acid on phytoextraction and antioxidative defense in Solanum nigrum L. as a hyperaccumulator under Cd and Pb combined pollution. Environ Earth Sci 65(7):1923–1932
Ghani A, Shah AU, Akhtar U (2010) Effect of lead toxicity on growth, chlorophyll and lead (Pb^). Pak J Nutr 9(9):887–891
Ghosh M, Singh SP (2005) A review on phytoremediation of heavy metals and utilization of it’s by products. Asian J Energy Environ 6(4):18
Gielen H, Vangronsveld J, Cuypers A (2017) Cd-induced Cu deficiency responses in Arabidopsis thaliana: are phytochelatins involved? Plant Cell Environ 40(3):390–400
Göhre V, Paszkowski U (2006) Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta 223(6):1115–1122
Habig WH, Jakoby WB (1981) [51] assays for differentiation of glutathione S-Transferases. In: Methods in enzymology, vol 77. Academic Press, Cambridge, pp 398–405
Han Y, Fan T, Zhu X, Wu X, Ouyang J, Jiang L, Cao S (2019) WRKY12 represses GSH1 expression to negatively regulate cadmium tolerance in Arabidopsis. Plant Mol Biol 99(1–2):149–159
Harzalli Jebara S, Fatnassi IC, Abdelkrim Ayed S, Saadani O, Chiboub M, Abid G, Jebara M (2017) Potentialities and limit of legume-plant growth promoting bacteria symbioses use in phytoremediation of heavy metal contaminated soils. Int J Plant Biol Res 5:4–8
Hashem A, Abd_Allah EF, Alqarawi AA, Al Huqail AA, Egamberdieva D, Wirth S (2016) Alleviation of cadmium stress in Solanum lycopersicum L. by arbuscular mycorrhizal fungi via induction of acquired systemic tolerance. Saudi J Biol Sci 23(2):272–281
He X, Richmond ME, Williams DV, Zheng W, Wu F (2019) Exogenous Glycine betaine reduces cadmium uptake and mitigates cadmium toxicity in two tobacco genotypes differing in cadmium tolerance. Int J Mol Sci 20(7):1612
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125(1):189–198
Heyno E, Klose C, Krieger-Liszkay A (2008) Origin of cadmium-induced reactive oxygen species production: mitochondrial electron transfer versus plasma membrane NADPH oxidase. New Phytol 179(3):687–699
Hou M, Li M, Yang X, Pan R (2019a) Responses of nonprotein Thiols to stress of vanadium and mercury in maize (Zea mays L.) seedlings. Bull Environ Contam Toxicol 102(3):1–7
Hou S, Wang X, Shafi M, Penttinen P, Xu W, Ma J, Zhong B, Guo J, Xu M, Ye Z, Liu D (2019b) Remediation efficacy of Sedum plumbizincicola as affected by intercropping of landscape plants and oxalic acid in urban cadmium contaminated soil. J Soils Sed 109(3):1–9
Jiang QY, Tan SY, Zhuo F, Yang DJ, Ye ZH, Jing YX (2016) Effect of Funneliformis mosseae on the growth, cadmium accumulation and antioxidant activities of Solanum nigrum. Appl Soil Ecol 98:112e120
Kapoor D, Rattan A, Gautam V, Kapoor N, Bhardwaj R (2014) 24-Epibrassinolide mediated changes in photosynthetic pigments and antioxidative defence system of radish seedlings under cadmium and mercury stress. J Stress Physiol Biochem 10:3
Khanna K, Jamwal VL, Gandhi SG, Ohri P, Bhardwaj R (2019a) Metal resistant PGPR lowered Cd uptake and expression of metal transporter genes with improved growth and photosynthetic pigments in Lycopersicon esculentum under metal toxicity. Sci Rep 9(1):5855
Khanna K, Jamwal VL, Kohli SK, Gandhi SG, Ohri P, Bhardwaj R, Abd_Allah EF, Hashem A, Ahmad P (2019b) Plant growth promoting rhizobacteria induced Cd tolerance in Lycopersicon esculentum through altered antioxidative defense expression. Chemosphere 217:463–474
Kohli SK, Bali S, Tejpal R, Bhalla V, Verma V, Bhardwaj R, Alqarawi AA, Abd_Allah EF, Ahmad P (2019) In-situ localization and biochemical analysis of bio-molecules reveals Pb-stress amelioration in Brassica juncea L. by co-application of 24-Epibrassinolide and Salicylic Acid. Sci Rep 9(1):3524
Kono Y (1978) Generation of superoxide radical during autoxidation of hydroxylamine and an assay for superoxide dismutase. Arch Biochem Biophys 186(1):189–195
Kumar KB, Khan PA (1982) Peroxidase and polyphenol oxidase in excised ragi (Eleusine corocana cv PR 202) leaves during senescence. Indian J Exp Biol 20(5):412–416
Latef AAHA (2011) Influence of arbuscular mycorrhizal fungi and copper on growth, accumulation of osmolyte, mineral nutrition and antioxidant enzyme activity of pepper (Capsicum annuum L.). Mycorrhiza 21:495e503
Li Q, Guo J, Zhang X, Yu H, Huang F, Zhang L, Zhang M, Li T (2019) Changes of non-protein thiols in root and organic acids in xylem sap involved in cadmium translocation of cadmium-safe rice line (Oryza Sative L.). Plant Soil 439:475–486
Madhaiyan M, Poonguzhali S, Sa T (2007) Metal tolerating methylotrophic bacteria reduces nickel and cadmium toxicity and promotes plant growth of tomato (Lycopersicon esculentum L.). Chemosphere 69(2):220–228
Mahmood T, Islam KR, Muhammad S (2007) Toxic effects of heavy metals on early growth and tolerance of cereal crops. Pak J Bot 39(2):451
Manzoor M, Abid R, Rathinasabapathi B, De Oliveira LM, da Silva E, Deng F, Rensing C, Arshad M, Gul I, Xiang P, Ma LQ (2019) Metal tolerance of arsenic-resistant bacteria and their ability to promote plant growth of Pteris vittata in Pb-contaminated soil. Sci Total Environ 660:18–24
Martinek RG (1964) Method for the determination of vitamin E (total tocopherols) in serum. Clin Chem 10(12):1078–1086
Mishra S, Srivastava S, Tripathi RD, Govindarajan R, Kuriakose SV, Prasad MNV (2006) Phytochelatin synthesis and response of antioxidants during cadmium stress in Bacopa monnieri L◊. Plant Physiol Biochem 44(1):25–37
Mittler R (2017) ROS are good. Trends Plant Sci 22(1):11–19
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22(5):867–880
Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Biol 49(1):249–279
Noh YD, Park HJ, Kim KR, Kim WI, Jung KY, Kim SU, Owens VN, Moon JS, Yun SW, Kim SY, Hong CO (2017) Contrasting effect of phosphate on phytoavailability of arsenic and cadmium in soils supporting medicinal plants. Appl Biol Chem 60(2):119–128
Ortega Villasante C, Hernández LE, Rellán Álvarez R, Del Campo FF, Carpena Ruiz RO (2007) Rapid alteration of cellular redox homeostasis upon exposure to cadmium and mercury in alfalfa seedlings. New Phytol 176(1):96–107
Pal R, Kaur R, Rajwar D, Narayan Rai JP (2019) Induction of non-protein thiols and phytochelatins by cadmium in Eichhornia crassipes. Int J Phytorem 21(8):1–9
Pandey AK, Gautam A, Dubey RS (2019) Transport and detoxification of metalloids in plants in relation to plant-metalloid tolerance. Plant Gene 17:100171
Piri M, Sepehr E, Rengel Z (2019) Citric acid decreased and humic acid increased Zn sorption in soils. Geoderma 341:39–45
Putter J (1974) In: U Bergmeyer, H. (Ed.), Peroxidase. In Methods of Enzymatic Analysis. Weinhan, Verlag Chemie, pp. 685e690
Rajkumar M, Sandhya S, Prasad MNV, Freitas H (2012) Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol Adv 30(6):1562–1574
Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180(2):169–181
Rathod DP, Brestic M, Shao HB (2011) Chlorophyll a fluorescence determines the drought resistance capabilities in two varieties of mycorrhized and non-mycorrhized Glycine max Linn. Afr J Microbiol Res 5(24):4197–4206
Rizvi A, Khan MS (2018) Heavy metal induced oxidative damage and root morphology alterations of maize (Zea mays L.) plants and stress mitigation by metal tolerant nitrogen fixing Azotobacter chroococcum. Ecotoxicol Environ Saf 157:9–20
Rizvi A, Ahmed B, Zaidi A, Khan MS (2019) Heavy metal mediated phytotoxic impact on winter wheat: oxidative stress and microbial management of toxicity by Bacillus subtilis BM2. RSC Adv 9(11):6125–6142
Roe JH, Kuether CA (1943) The determination of ascorbic acid in whole blood and urine through the 2, 4-dinitrophenylhydrazine derivative of dehydroascorbic acid. J Biol Chem 147:399–407
Romero-Puertas MC, Rodríguez-Serrano M, Corpas FJ, Gomez MD, Del Rio LA, Sandalio LM (2004) Cadmium-induced subcellular accumulation of O2·− and H2O2 in pea leaves. Plant Cell Environ 27(9):1122–1134
Rufino RD, Sarubbo LA, Campos-Takaki GM (2007) Enhancement of stability of biosurfactant produced by Candida lipolytica using industrial residue as substrate. World J Microbiol Biotechnol 23(5):729–734
Sanita di Toppi L, Castagna A, Andreozzi E, Careri M, Predieri G, Vurro E, Ranieri A (2009) Occurrence of different inter-varietal and inter-organ defence strategies towards supra-optimal zinc concentrations in two cultivars of Triticum aestivum L. Environ Exp Bot 66:220e229
Sathyapriya H, Sariah M, Siti Nor Akmar A, Wong M (2012) Root colonisation of Pseudomonas aeruginosa strain UPMP 3 and induction of defence related genes in oil palm (Elaeis guineensis). Ann Appl Biol 160(2):137–144
Sedlak J, Lindsay RH (1968) Estimation of total, protein bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 25:192–205
Sessitsch A, Kuffner M, Kidd P, Vangronsveld J, Wenzel WW, Fallmann K, Puschenreiter M (2013) The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biol Biochem 60:182–194
Sidhu GPS, Bali AS, Bhardwaj R (2019) Role of organic acids in mitigating cadmium toxicity in plants. In: Cadmium Tolerance in Plants. Academic Press, Cambridge, pp 255–279
Singh S, Singh A, Bashri G, Prasad SM (2016) Impact of Cd stress on cellular functioning and its amelioration by phytohormones: an overview on regulatory network. Plant Growth Regul 80(3):253–263
Šiukšta R, Bondzinskaitė S, Kleizaitė V, Žvingila D, Taraškevičius R, Mockeliūnas L, Stapulionytė A, Mak K, Čėsnienė T (2019) Response of Tradescantia plants to oxidative stress induced by heavy metal pollution of soils from industrial areas. Environ Sci Pollut Res 26(1):44–61
Song WY, Yang HC, Shao HB, Zheng AZ, Brestic M (2014) The alleviative effects of salicylic acid on the activities of catalase and superoxide dismutase in malting barley (Hordeum uhulgare L.) seedling leaves stressed by heavy metals. CLEAN–Soil, Air, Water 42(1):88–97
Sybhashini V, Swamy AVVS (2013) Phytoremediation of cadmium and chromium from contaminated soils using Physalis minima Linn. Am Int J Res Formal Appl Nat Sci 3(1):13–260
Sytar O, Kumari P, Yadav S, Brestic M, Rastogi A (2019) Phytohormone priming: regulator for heavy metal stress in plants. J Plant Growth Regul 38(2):739–752
Thangavel P, Long S, Minocha R (2007) Changes in phytochelatins and their biosynthetic intermediates in red spruce (Picea rubens Sarg.) cell suspension cultures under cadmium and zinc stress. Plant Cell Tissue Organ Cult 88(2):201–216
Thongnok S, Siripornadulsil W, Siripornadulsil S (2018) Mitigation of arsenic toxicity and accumulation in hydroponically grown rice seedlings by co-inoculation with arsenite-oxidizing and cadmium-tolerant bacteria. Ecotoxicol Environ Saf 162:591–602
Tudoreanu L, Phillips CJC (2004) Modeling cadmium uptake and accumulation in plants. Adv Agron 84(4):121–157
Ullah I, Al-Johny BO, AL-Ghamdi KM, Al-Zahrani HA, Anwar Y, Firoz A, Naser AK, Almatry MAA (2019) Endophytic bacteria isolated from Solanum nigrum L., alleviate cadmium (Cd) stress response by their antioxidant potentials, including SOD synthesis by sodA gene. Ecotoxicol Environ Saf 174:197–207
Upadhyay SK, Singh JS, Saxena AK, Singh DP (2012) Impact of PGPR inoculation on growth and antioxidant status of wheat under saline conditions. Plant Biol 14(4):605–611
Vaahtera L, Brosché M, Wrzaczek M, Kangasjärvi J (2014) Specificity in ROS signaling and transcript signatures. Antioxid Redox Signal 21(9):1422–1441
Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151(1):59–66
Wang YS, Yang ZM (2005) Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L. Plant Cell Physiol 46(12):1915–1923
Weber M, Trampczynska A, Clemens S (2006) Comparative transcriptome analysis of toxic metal responses in Arabidopsis thaliana and the Cd2+−hypertolerant facultative metallophyte Arabidopsis halleri. Plant Cell Environ 29(5):950–963
Wu GL, Cui J, Tao L, Yang H (2010) Fluroxypyr triggers oxidative damage by producing superoxide and hydrogen peroxide in rice (Oryza sativa). Ecotoxicology 19(1):124–132
Xiu W, Guo H, Liu Q, Liu Z, Zhang B (2015) Arsenic removal and transformation by Pseudomonas sp. strain GE-1-induced ferrihydrite: co-precipitation versus adsorption. Water Air Soil Pollut 226(6):167
Xu H, Yu C, Xia X, Li M, Li H, Wang Y, Wang S, Wang C, Ma Y, Zhou G (2018) Comparative transcriptome analysis of duckweed (Landoltia punctata) in response to cadmium provides insights into molecular mechanisms underlying hyperaccumulation. Chemosphere 190:154–165
Yan K, Chen P, Shao H, Zhang L, Xu G (2011) Effects of short-term high temperature on photosynthesis and photosystem II performance in sorghum. J Agron Crop Sci 197(5):400–408
Yasin NA, Khan WU, Ahmad SR, Ahmad A, Akram W, Ijaz M (2019) Role of Acinetobacter sp. CS9 in improving growth and phytoremediation potential of Catharanthus longifolius under cadmium stress. Pol J Environ Stud 28(1):435–443
Yu R, Tang Y, Liu C, Du X, Miao C, Shi G (2017) Comparative transcriptomic analysis reveals the roles of ROS scavenging genes in response to cadmium in two pak choi cultivars. Sci Rep 7(1):9217
Zhao Y, Hu C, Wang X, Qing X, Wang P, Zhang Y, Zhang X, Zhao X (2019) Selenium alleviated chromium stress in Chinese cabbage (Brassica campestris L. ssp. Pekinensis) by regulating root morphology and metal element uptake. Ecotoxicol Environ Saf 173:314–321
Zhou J, Wan H, He J, Lyu D, Li H (2017) Integration of cadmium accumulation, subcellular distribution, and physiological responses to understand cadmium tolerance in apple rootstocks. Front Plant Sci 8:966
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The authors are grateful to the Deanship of Scientific Research, King Saud University for funding through the Vice Deanship of Scientific Research Chairs.
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Renu Bhardwaj, Kanika Khanna and Parvaiz Ahmad outlined the experimental work. Kanika Khanna and Sukhmeen Kaur Kohli performed the experimental work. Anket Sharma, Asma A. Al-Huqail, Manzer H. Siddiqui helped in data analysis. Parvaiz Ahmad and Renu Bhardwaj revised the manuscript to the present form.
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Khanna, K., Kohli, S.K., Sharma, A. et al. Histochemical and physicochemical studies reveal improved defense in tomato under Cd stress with rhizobacterial supplementation. Plant Soil 446, 393–411 (2020). https://doi.org/10.1007/s11104-019-04356-8
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DOI: https://doi.org/10.1007/s11104-019-04356-8