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Elucidating Cd-mediated distinct rhizospheric and in planta ionomic and physio-biochemical responses of two contrasting Zea mays L. cultivars

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Abstract

Cadmium (Cd) in soil–plant system can abridge plant growth by initiating alterations in root zones. Hydroponics and rhizoboxes are useful techniques to monitor plant responses against various natural and/or induced metal stresses. However, soil based studies are considered more appropriate in order to devise efficient food safety and remediation strategies. The present research evaluated the Cd-mediated variations in elemental dynamics of rhizospheric soil together with in planta ionomics and morpho-physio-biochemical traits of two differentially Cd responsive maize cultivars. Cd-sensitive (31P41) and Cd-tolerant (3062) cultivars were grown in pots filled with 0, 20, 40, 60 and 80 µg/kg CdCl2 supplemented soil. The results depicted that the maize cultivars significantly influenced the elemental dynamics of rhizosphere as well as in planta mineral accumulation under applied Cd stress. The uptake and translocation of N, P, K, Ca, Mg, Zn and Fe from rhizosphere and root cell sap was significantly higher in Cd stressed cv. 3062 as compared to cv. 31P41. In sensitive cultivar (31P41), Cd toxicity resulted in significantly prominent reduction of biomass, leaf area, chlorophyll, carotenoids, protein contents as well as catalase activity in comparison to tolerant one (3062). Analysis of tolerance indexes (TIs) validated that cv. 3062 exhibited advantageous growth and efficient Cd tolerance due to elevated proline, phenolics and activity of antioxidative machinery as compared to cv. 31P41. The cv. 3062 exhibited 54% and 37% less Cd bio-concentration (BCF) and translocation factors (TF), respectively in comparison to cv. 31P41 under highest Cd stress regime. Lower BCF and TF designated a higher Cd stabilization by tolerant cultivar (3062) in rhizospheric zone and its potential use in future remediation plans.

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References

  • Abbas S, Javed MT, Shahid M, Hussain I, Haider MZ, Chaudhary HJ, Maqsood A (2020) Acinetobacter sp. SG-5 inoculation alleviates cadmium toxicity in differentially Cd tolerant maize cultivars as deciphered by improved physio-biochemical attributes, antioxidants and nutrient physiology. Plant Physiol Biochem 155:815–827

    CAS  PubMed  Google Scholar 

  • Akhtar MJ, Ali Q, Javid R, Asghar HN, Ahmad I, Iqbal MZ, Khaliq A (2019) Organic and inorganic amendments immobilized cadmium and improved maize growth and yield in Cd-contaminated soil. Int J Agric Biol 22(6):1497–1506

    Google Scholar 

  • Alba R, Payton P, Fei Z, McQuinn R, Debbie P, Martin GB, Giovannoni JJ (2005) Transcriptome and selected metabolite analyses reveal multiple points of ethylene control during tomato fruit development. Plant Cell 17(11):2954–2965

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ali Q, Ashraf M (2011) Induction of drought tolerance in maize (Zea mays L.) due to exogenous application of trehalose: growth, photosynthesis, water relations and oxidative defense mechanism. J Agron Crop Sci 197:258–271

    CAS  Google Scholar 

  • Alloway BJ (1995) Heavy metals in soil. Blackie and Son Glasgow.

  • Anjum SA, Tanveer M, Hussain S (2016) Osmoregulation and antioxidant production in maize under combined cadmium and arsenic stress. Environ Sci Pollut Res 23:11864–11875

    CAS  Google Scholar 

  • Anjum SA, Tanveer M, Hussain S, Bao M, Wang L, Khan I, Shahzad B (2015) Cadmium toxicity in maize (Zea mays L): consequences on antioxidative systems, reactive oxygen species and cadmium accumulation. Environ Sci Pollut Res 22(21):17022–17030

    CAS  Google Scholar 

  • Armas T, Pinto AP, de Varennes A, Mourato MP, Martins LL, Gonçalves MLS, Mota AM (2015) Comparison of cadmium induced oxidative stress in Brassica juncea in soil and hydroponic cultures. Plant Soil 388(1–2):297–305

    CAS  Google Scholar 

  • Arnon DI, Hoagland DR (1940) Crop production in artificial culture solution, sand and soil with special reference to factors influencing yield and absorption of inorganic nutrient. Soil Sci 50:463–483

    CAS  Google Scholar 

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

    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(1–2):248–254

    CAS  PubMed  Google Scholar 

  • Bremner JM, Keeney DR (1965) Steam distillation methods for determination of ammonium, nitrate and nitrite. Anal Chim Acta 32:485–495

    CAS  Google Scholar 

  • Bui TTX, Lu M, Vu DD, Dinh HN, Ullah N, Rahman SU, Zhang Y (2018) Physiological responses of Toxicodendron vernicifluum (Stokes) FA Barkley to cadmium stress under sufficient-and deficient-nitrogen conditions. Trees 32(5):1457–1471

    CAS  Google Scholar 

  • Cai Y, Zhang S, Cai K, Huang F, Pan B, Wang W (2020) Cd accumulation, biomass and yield of rice are varied with silicon application at different growth phases under high concentration cadmium-contaminated soil. Chemosphere 242:125–128

    Google Scholar 

  • Cakmark I, Strbac D, Marchener H (1993) Activities of hydrogen peroxide-scavenging enzymes in germinating wheat seeds. J Exp Bot 44(1):127–132

    Google Scholar 

  • Chaffei C, Pageau K, Suzuki A, Gouia H, Ghorbel MH, Masclaux-Daubresse C (2004) Cadmium toxicity induced changes in nitrogen management in Lycopersicon esculentum leading to a metabolic safeguard through an amino acid storage strategy. Plant Cell Physiol 45(11):1681–1693

    CAS  PubMed  Google Scholar 

  • Douchiche O, Rihouey C, Schaumann A, Driouich A, Morvan C (2007) Cadmium-induced alterations of the structural features of pectins in flax hypocotyl. Planta 225:1301–1312

    CAS  PubMed  Google Scholar 

  • Ekmekçi Y, Tanyolac D, Ayhan B (2008) Effects of cadmium on antioxidant enzyme and photosynthetic activities in leaves of two maize cultivars. J Plant Physiol 165(6):600–611

    PubMed  Google Scholar 

  • Farid M, Ali S, Shakoor MB, Bharwana SA, Rizvi H, Ehsan S, Hannan F (2013) EDTA assisted phytoremediation of cadmium, lead and zinc. Int J Agron Plant Prod 4(11):2833–2846

    Google Scholar 

  • Gadd GM, Griffith AJ (1978) Microorganisms and heavy metal toxicity. Microb Ecol 4:303–317

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Gong H, Zhu X, Chen K, Wang S, Zhang C (2005) Silicon alleviates oxidative damage of wheat plants in pots under drought. Plant Sci 169(2):313–321

    CAS  Google Scholar 

  • Greger M, Kabir AH, Landberg T, Maity PJ, Lindberg S (2016) Silicate reduces cadmium uptake into cells of wheat. Environ Pollut 211:90–97

    CAS  PubMed  Google Scholar 

  • Hajaji AN, Gouia H, Carrayol H, Chaffei CH (2012) Ammonium alleviates redox state in solanum seedlings under cadmium stress conditions. J Environ Anal Toxicol 2:116–120

    Google Scholar 

  • Han Y, Zhang L, J, Gu J Zhao, J Fu, (2018) Citric acid and EDTA on the growth, photosynthetic properties and heavy metal accumulation of Iris halophila Pall. Cultivated in Pb mine tailings. Int Biodeterior 128:15–21

    CAS  Google Scholar 

  • Handique GK, Handique AK (2009) Proline accumulation in lemongrass (Cymbopogon flexuosus Stapf) due to heavy metal stress. J Environ Biol l30: 299–302

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophy 125(1):189–198

    CAS  Google Scholar 

  • Hossain MA, Piyatida P, Jaime A, Silva TD, Fujita M (2012) 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 872–875.

  • Hussain I, Akhtar S, Ashraf MA, Rasheed R, Siddiqi EH, Ibrahim M (2013). Response of maize seedlings to cadmium application after different time intervals. ISRN Agron, 1–9.

  • Javed MT, Akram MS, Tanwir K, Chaudhary HJ, Ali Q, Stoltz E, Lindberg S (2017) Cadmium spiked soil modulates root organic acids exudation and ionic contents of two differentially Cd tolerant maize (Zea mays L.) cultivars. Ecotoxicol Environ Safe 141:216–225

    CAS  Google Scholar 

  • Javed MT, Lindberg S, Greger M (2014) Cellular proton dynamics in Elodea canadensis leaves induced by cadmium. Plant Physiol Biochem 77:15–22

    Google Scholar 

  • Julkunen-Tiitto R (1985) Phenolic constituents in the leaves of northern willows: methods for the analysis of certain phenolics. J Agric Food Chem 33:213–217

    CAS  Google Scholar 

  • Khan MY, Prakash V, Yadav V, Chauhan DK, Prasad SM, Ramawat N, Sharma S (2019) Regulation of cadmium toxicity in roots of tomato by indole acetic acid with special emphasis on reactive oxygen species production and their scavenging. Plant Physiol Biochem 142:193–201

    CAS  PubMed  Google Scholar 

  • Khanna K, Jamwal VL, Kohli SK, Gandhi SG, Ohri P, Bhardwaj R, Ahmad P (2019) Plant growth promoting rhizobacteria induced Cd tolerance in Lycopersicon esculentum through altered antioxidative defense expression. Chemosphere 217:463–474

    CAS  PubMed  Google Scholar 

  • Kurtyka R, Małkowski E, Kita A, Karcz W (2008) Effect of calcium and cadmium on growth and accumulation of cadmium calcium potassium and sodium in maize seedlings. Pol J Environ Stud, 17(1).

  • Lindberg S, Wingstrand G (1985) Mechanism for Cd2+ inhibition of (K+ + Mg2+) ATPase ac-tivity and K+ (86Rb+) uptake in roots of sugarbeet (Beta vulgaris). Physiol Plant 63:181–185

    CAS  Google Scholar 

  • Lux A, Martinka M, Vaculik M, White PJ (2011) Root responses to cadmium in the rhizo-sphere: a review. J Exp Bot 62:21–37

    CAS  PubMed  Google Scholar 

  • Maggio A, Miyazaki S, Veronese P, Fujita T, Ibeas JI, Damsz B, Narasimhan ML, Hasegawa PM, Joly RJ, Bressan RA (2002) Does proline accumulation play an active role in stress induced growth reduction. Plant J 31:699–712

    CAS  PubMed  Google Scholar 

  • Mahmood A, Malik RN (2014) Human health risk assessment of heavy metals via consumption of contaminated vegetables collected from different irrigation sources in Lahore, Pakistan. Arab J Chem 7:91–99

    CAS  Google Scholar 

  • Minocha R, Martinez G, Lyons B, Long S (2009) Development of a standardized method-ology for quantifying total chlorophyll and carotenoids from foliage of hardwood and conifer tree species. Can J Forest Res 39(4):849–861

    CAS  Google Scholar 

  • Muszyńska E (2017) HanusFajerska E (2017) In vitro multiplication of Dianthus carthusianorum calamine ecotype with the aim to revegetate and stabilize polluted wastes. Plant Cell Tiss Org 128(3):631–640

    Google Scholar 

  • Nazar R, Iqbal N, Masoo A, Khan MIR, Syeed S, Khan NA (2012) Cadmium toxicity in plants and role of mineral nutrients in its alleviation. AJPS 3:1476–1489

    Google Scholar 

  • Perfus-Barbeoch L, Leonhardt N, Vavasseur A, Forestier C (2002) Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status. Plant J 32:539–548

    CAS  PubMed  Google Scholar 

  • Qin S, Liu H, Nie Z, Rengel Z, Gao W, Li C, Zhao P (2020) Toxicity of cadmium and its competition with mineral nutrients for uptake by plants: a review. Pedosphere 30(2):168–180

    Google Scholar 

  • Ran J, Zheng W, Wang H, Wang H, Li Q (2020) Indole-3-acetic acid promotes cadmium (Cd) accumulation in a Cd hyperaccumulator and a non-hyperaccumulator by different physiological responses. Ecotoxicol Environ Safe 191:110213

    CAS  Google Scholar 

  • Redjala T, Sterckeman T, Morel JL (2009) Cadmium uptake by roots: contribution of apo-plast and of high- and low-affinity membrane transport systems. Environ Exp Bot 67:235–242

    CAS  Google Scholar 

  • Sabeen M, Mahmood Q, Irshad M, Fareed I, Khan A, Ullah F, Tabassum S (2013) Cadmium phytoremediation by Arundo donax L. from contaminated soil and water. Biomed Res Int, 324830.

  • Shah AA, Ahmed S, Ali A, Yasin NA (2020) 2-Hydroxymelatonin mitigates cadmium stress in Cucumis sativus seedlings: Modulation of antioxidant enzymes and polyam-ines. Chemosphere 243:125308

    CAS  PubMed  Google Scholar 

  • Shen M, Schneider H, Xu R, Cao G, Zhang H, Li T, Zhao Z (2020) Dark septate endo-phyte enhances maize cadmium (Cd) tolerance by the remodeled host cell walls and the altered Cd subcellular distribution. Environ Exp Bot 172:104000

    Google Scholar 

  • Shi H, Ma W, Song J, Lu M, Rahman SU, Bui TTX, Zhang Y (2017) Physiological and transcriptional responses of Catalpa bungei to drought stress under sufficient-and de-ficient-nitrogen conditions. Tree Physiol 37(11):1457–1468

    CAS  PubMed  Google Scholar 

  • Singh S, Singh VP, Prasad SM, Sharma S, Ramawat N, Dubey NK, Chauhan DK (2019) Interactive Effect of Silicon (Si) and Salicylic Acid (SA) in Maize Seedlings and Their Mechanisms of Cadmium (Cd) Toxicity Alleviation. J Plant Growth Regul 38(4):1587–1597

    CAS  Google Scholar 

  • Sterckeman T, Redjala T, Morel JL (2011) Influence of exposure solution composition and of plant cadmium content on root cadmium short term uptake. Environ Exp Bot 74:131–139

    CAS  Google Scholar 

  • Sun J, Wang R, Zhang X, Yu Y, Zhao R, Li Z, Chen S (2013) Hydrogen sulfide alleviates cadmium toxicity through regulations of cadmium transport across the plasma and vacuolar membranes in Populus euphratica cells. Plant Physiol Biochem 65:67–74

    CAS  PubMed  Google Scholar 

  • Tanwir K, Akram SA, Masood S, Chaudhary HJ, Lindberg S, Javed MT (2015) Cadmium-induced rhizospheric pH dynamics modulated nutrient acquisition and physiological attributes of maize (Zea mays L). Environ Sci Pollut Res 22(12):9193–9203

    CAS  Google Scholar 

  • Tao Q, Zhao J, Li J, Liu Y, Luo J, Yuan S, Huang H (2020) Unique root exudate tartar-ic acid enhanced cadmium mobilization and uptake in Cd-hyperaccumulator Sedum al-fredii. J Hazard Mater 383:121177

    CAS  PubMed  Google Scholar 

  • Vatehová A, Malovíková K, Kollárová D, Kučerová D, Lišková, (2016) Impact of cadmi-um stress on two maize hybrids. Plant Physiol Biochem 108:90–98

    PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Veronica N, Subrahmanyam D, Kiran TV, Yugandhar P, Bhadana VP, Padm V, Voleti SR (2017) Influence of low phosphorus concentration on leaf photosynthetic characteristics and antioxidant response of rice genotypes. Photosynthetica 55(2):285–293

    CAS  Google Scholar 

  • Wang M, Zou J, Duan X, Jiang W, Liu D (2007) Cadmium accumulation and its effects on metal uptake in maize (Zea mays L.). Bioresour Tech 98:82–88

    CAS  Google Scholar 

  • Waseem A, Arshad J, Iqbal F, Sajjad A, Mehmood Z, Murtaza G (2014) Pollution status of Pakistan: a retrospective review on heavy metal contamination of water, soil, and vegetables. BioMed Res Int 2014:813206. https://doi.org/10.1155/2014/813206,29pages

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Nan Z, Zhao Z (2014) Bioaccumulation and translocation of cadmium in wheat (Triticum aestivum L) and maize (Zea mays L) from the polluted oasis soil of Northwestern China. Chem Speciat Bioavailab 26(1):43–51

    CAS  Google Scholar 

  • Zhang C, He Q, Wang M, Gao X, Chen J, Shen C (2020) Exogenous indole acetic acid alleviates Cd toxicity in tea (Camellia sinensis). Ecotoxicol Environ Safe 190:110090

    CAS  Google Scholar 

  • Zhao T, Zhang K, Chen J, Shi X, Li X, Ma Y, Xu S (2019) Changes in heavy metal mobility and availability in contaminated wet-land soil remediated using lignin-based poly (acrylic acid). J Hazard Mater 368:459–467

    CAS  PubMed  Google Scholar 

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Acknowledgments

Provision of financial resources by Higher Education Commission (HEC) of Pakistan (Grant No: 20-4243/NRPU/R&D/HEC/14/885) is highly appreciated.

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Conceptualization, Muhammad Tariq Javed, Muhammad Sohail Akram, Shafaqat Ali, Data curation, Saghir Abbas, Muhammad Tariq Javed and Muhammad Sohail Akram; Formal analysis, Saghir Abbas, Qasim Ali, Naeem Iqbal, Muhammad Sohail Akram and Kashif Tanwir; Funding acquisition, Muhammad Tariq Javed Investigation, Saghir Abbas, Muhammad Sohail Akram and Hassan Javed Chaudhary; Methodology, Saghir Abbas, Muhammad Tariq Javed, Qasim Ali, Muhammad Sohail Akram and Kashif Tanwir; Project administration, Shafaqat Ali; Resources, Muhammad Tariq Javed, Shafaqat Ali, Naeem Iqbal, Hassan Javed Chaudhary; Software, Shafaqat Ali, Hassan Javed Chaudhary; Supervision, Muhammad Tariq Javed; Validation, Qasim Ali and Kashif Tanwir, Naeem Iqbal; Visualization, Saghir Abbas, Qasim Ali and Kashif Tanwir; Writing—original draft, Saghir Abbas, Muhammad Tariq Javed, Shafaqat Ali, Writing—review & editing, Saghir Abbas, Muhammad Tariq Javed, Kashif Tanwir, Naeem Iqbal, Muhammad Sohail Akram. The presented data is the part of MPhil research of Mr. Saghir Abbas.

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Correspondence to Muhammad Tariq Javed.

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Abbas, S., Javed, M.T., Ali, Q. et al. Elucidating Cd-mediated distinct rhizospheric and in planta ionomic and physio-biochemical responses of two contrasting Zea mays L. cultivars. Physiol Mol Biol Plants 27, 297–312 (2021). https://doi.org/10.1007/s12298-021-00936-0

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