Skip to main content
Log in

Endogenous trans-zeatin content in plants with different metal-accumulating ability: a field survey

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

A field survey was conducted to evaluate soil metal pollution and endogenous trans-zeatin content in the leaves of plants growing at six sites in a metal-polluted area located in Gejiu, Yunnan, China. Five plant species were collected, and the physicochemical properties and concentrations of five metals in the soil were analyzed. The trans-zeatin content in plant leaves was measured by high-performance liquid chromatography. Based on the Nemerow pollution index, the six sites were classified into four levels of pollution (i.e., low, medium, high, and severely high). The degree of soil metal pollution was cadmium (Cd) > arsenic (As) > lead (Pb) > zinc (Zn) > copper (Cu). The leaf trans-zeatin content in Pteris vittata (an arsenic hyperaccumulator) increased significantly by 98.6 % in soil with a severely high level of pollution compared with soil at a low level of pollution. However, in non-hyperaccumulators Bidens pilosa var. radiata and Ageratina adenophora, a significant decrease in leaf trans-zeatin content of 35.6 and 87.6 %, respectively, was observed. The leaf trans-zeatin content in Artemisia argyi also decreased significantly by 73.6 % in high metal-polluted soil compared with that in medium metal-polluted soil. Furthermore, significant correlations were observed between leaf trans-zeatin content in Pteris vittata and As, Pb, and Cd concentrations in the soil; however, either no correlation or a negative one was observed in the other plant species. Therefore, a high content of trans-zeatin in the leaves of Pteris vittata may play an important role in its normal growth and tolerance to metals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

ANOVA:

Analysis of variance

CTK:

Cytokinin

DTPA :

Diethylenetriamine pentaacetic acid

GA :

Gibberellin

HPLC :

High-performance liquid chromatography

PGR :

Plant growth regulator

PVPP :

Polyvinylpolypyrrolidone

ROS :

Reactive oxygen species

TEA :

Triethanolamine

Z :

Trans-zeatin

References

  • Asgher M, Khan MIR, Anjum NA, Khan NA (2015) Minimizing toxicity of cadmium in plants - role of plant growth regulators. Protoplasma 252:399–413. doi:10.1007/s00709-014-0710-4

    Article  CAS  Google Scholar 

  • Atanasova LY, Pissarska MG, Popov GS, Georgiev GI (2004) Growth and endogenous cytokinins of juniper shoots as affected by high metal concentrations. Biol Plantarum 48(1):157–159. doi:10.1023/B:BIOP.0000024296.01389.f2

    Article  CAS  Google Scholar 

  • Bajguz A, Piotrowska A (2009) Conjugates of auxin and cytokinin. Phytochemistry 70(8):957–969. doi:10.1016/j.phytochem.200905.006

    Article  CAS  Google Scholar 

  • Baker AJM, Walker PL (1990) Ecophysiology of metal uptake by tolerant plants. In: Shaw AJ (ed) Heavy metal tolerance in plants: evolutionary aspects. CRC Press, Boca Raton, Florida, pp. 155–177

    Google Scholar 

  • Balestri M, Bottega S, Spanò C (2014a) Response of Pteris vittata to different cadmium treatments. Acta Physiol Plant 36(3):767–775. doi:10.1007/s11738-013-1454-z

    Article  CAS  Google Scholar 

  • Balestri M, Ceccarini A, Forino LMC, Zelko I, Martinka M, Lux A, Castiglione MR (2014b) Cadmium uptake, localization and stress-induced morphogenic response in the fern Pteris vittata. Planta 239(5):1055–1064. doi:10.1007/s00425-014-2036-z

    Article  CAS  Google Scholar 

  • Blagoeva E, Dobrev PI, Malbeck J, Motyka V, Gaudinova A, Vankova R (2004) Effect of exogenous cytokinins, auxins and adenine on cytokinin N-glucosylation and cytokinin oxidase/dehydrogenase activity in de-rooted radish seedlings. Plant Growth Regul 44(1):15–23. doi:10.1007/s10725-004-1934-7

    Article  CAS  Google Scholar 

  • Brady JP, Ayoko GA, Martens WN, Goonetilleke A (2015) Development of a hybrid pollution index for heavy metals in marine and estuarine sediments. Environ Monit Assess 187:1–14. doi:10.1007/s10661-015-4563-x

    Article  Google Scholar 

  • Brugière N, Jiao S, Hantke S, Zinselmeier C, Roessler JA, Niu X, Jones RJ, Habben JE (2003) Cytokinin oxidase gene expression in maize is localized to the vasculature, and is induced by cytokinins, abscisic acid, and abiotic stress. Plant Physiol 132(3):1228–1240. doi:10.1104/pp.102.017707

    Article  Google Scholar 

  • Bulak P, Walkiewicz A, Brzezińska M (2014) Plant growth regulators-assisted phytoextraction. Biol Plantarum 58(1):1–8. doi:10.1007/s10535-013-0382-5

    Article  CAS  Google Scholar 

  • Cabello-Conejo MI, Centofanti T, Kidd PS, Prieto-Fernández Á, Chaney RL (2013) Evaluation of plant growth regulators to increase nickel phytoextraction by Alyssum species. Int J Phytoremediat 15(4):365–375. doi:10.1080/15226514.2012.702806

  • Cabello-Conejo MI, Prieto-Fernández Á, Kidd PS (2014) Exogenous treatments with phytohormones can improve growth and nickel yield of hyperaccumulating plants. Sci Total Environ 494:1–8. doi:10.1016/j.scitotenv.2014.06.102

    Article  Google Scholar 

  • Cai L, Xu Z, Ren M, Guo Q, Hu X, Hu G, Wan H, Peng P (2012) Source identification of eight hazardous heavy metals in agricultural soils of Huizhou, Guangdong Province, China. Ecotox Environ Safe 78(3):2–8. doi:10.1016/j.ecoenv.2011.07.004

    Article  CAS  Google Scholar 

  • Caille N, Zhao FJ, Mcgrath SP (2005) Comparison of root absorption, translocation and tolerance of arsenic in the hyperaccumulator Pteris vittata and the nonhyperaccumulator Pteris tremula. New Phytol 165(3):755–761. doi:10.1111/j.1469-8137.2004.01239.x

    Article  CAS  Google Scholar 

  • Cao A, Cappai G, Carucci A, Lai T (2008) Heavy metal bioavailability and chelate mobilization efficiency in an assisted phytoextraction process. Environ Geochem Hlth 30(2):115–119. doi:10.1007/s10653-008-9136-2

    Article  CAS  Google Scholar 

  • Cassina L, Tassi E, Morelli E, Giorgetti L, Remorini D, Chaney RL, Barbafieri M (2011) Exogenous cytokinin treatments of an Ni hyper-accumulator, Alyssum murale, grown in a serpentine soil: implications for phytoextraction. Int J Phytoremediat 13(s1):90–101. doi:10.1080/15226514.2011.568538

    Article  Google Scholar 

  • Cassina L, Tassi E, Pedron F, Petruzzelli G, Ambrosini P, Barbafieri M (2012) Using a plant hormone and a thioligand to improve phytoremediation of Hg-contaminated soil from a petrochemical plant. J Hazard Mater 231:36–42. doi:10.1016/j.jhazmat.2012.06.031

    Article  Google Scholar 

  • Chen TB, Wei CY, Huang ZC, Huang QF, Lu QG, Fan ZL (2002) Arsenic hyperaccumulator Pteris vittata L. and its arsenic accumulation. Chinese Sci Bull 47(11):902–905. doi:10.3321/j.issn:0023-074X.2002.03.011

    Article  CAS  Google Scholar 

  • Cortleven A, Valcke R (2012) Evaluation of the photosynthetic activity in transgenic tobacco plants with altered endogenous cytokinin content: lessons from cytokinin. Physiol Plantarum 144(4):394–408. doi:10.1111/j.1399-3054.2011.01558.x

    Article  CAS  Google Scholar 

  • Dobrev PI, Kamı́nek M (2002) Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction. J Chromatogr A 950(1):21–29. doi:10.1016/S0021-9673(02)00024-9

    Article  Google Scholar 

  • Foo E, Morris SE, Parmenter K, Young N, Wang H, Jones A, Rameau C, Turnbull CG, Beveridge CA (2007) Feedback regulation of xylem cytokinin content is conserved in pea and Arabidopsis. Plant Physiol 143(3):1418–1428. doi:10.1104/pp.106.093708

    Article  CAS  Google Scholar 

  • Gajdosova S, Spichal L, Kaminek M, Hoyerova K, Novak O, Dobrev PI, Galuszka P, Klima P, Gaudinova A, Zizkova E, Hanus J, Dancak M, Travnicek B, Pesek B, Krupicka M, Vankova R, Strnad M, Motyka V (2011) Distribution, biological activities, metabolism, and the conceivable function of cis-zeatin-type cytokinins in plants. J Exp Bot 62(62):2827–2840. doi:10.1093/jxb/erq457

  • Gangwar S, Singh VP, Tripathi DK, Chauhan DK, Prasad SM, Maurya JN (2014) Plant responses to metal stress: the emerging role of plant growth hormones in toxicity alleviation. In: Ahmad P, Rasool S (eds) Emerging technologies and management of crop stress tolerance, volume 2: a sustainable approach. Academic Press, London, pp. 215–248. doi:10.1016/B978-0-12-800875-1.00010-7

    Chapter  Google Scholar 

  • Ghanem ME, Albacete A, Smigocki AC, Frebort I, Posopisilova H, Martinez-Andujar C, Acosta M, Sanchez-Bravo J, Lutts S, Dodd IC, Perez-Alfocea F (2011) Root-synthesized cytokinins improve shoot growth and fruit yield in salinized tomato (Solanum lycopersicum L.) plants. J Exp Bot 62(1):125–140. doi:10.1093/jxb/erq266

    Article  CAS  Google Scholar 

  • Gu X, Le C, Wang Y, Li Z, Jiang D, Wang Y, He Y (2013) Arabidopsis FLC clade members form flowering-repressor complexes coordinating responses to endogenous and environmental cues. Nat Commun 4(3):1947. doi:10.1038/ncomms2947

    Google Scholar 

  • Gupta V, Kumar M, Brahmbhatt H, Reddy CRK, Seth A, Jha B (2011) Simultaneous determination of different endogenetic plant growth regulators in common green seaweeds using dispersive liquid–liquid microextraction method. Plant Physiol Bioch 49(11):1259–1263. doi:10.1016/j.plaphy.2011.08.004

    Article  CAS  Google Scholar 

  • Ha S, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Tran LSP (2012) Cytokinins: metabolism and function in plant adaptation to environmental stresses. Trends Plant Sci 17(3):172–179. doi:10.1016/j.tplants.2011.12.005

    Article  CAS  Google Scholar 

  • Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53(366):1–11. doi:10.1093/jexbot/53.366.1

    Article  CAS  Google Scholar 

  • Hashem HA (2014) Cadmium toxicity induces lipid peroxidation and alters cytokinin content and antioxidant enzyme activities in soybean. Botany 92(1):1–7. doi:10.1139/cjb-2013-0164

    Article  CAS  Google Scholar 

  • Hegedüs A, Erdei S, Horváth G (2001) Comparative studies of H2O2 detoxifying enzymes in green and greening barley seedlings under cadmium stress. Plant Sci 160(6):1085–1093. doi:10.1016/S0168-9452(01)00330-2

    Article  Google Scholar 

  • Huang RQ, Gao SF, Wang WL, Staunton S, Wang G (2006) Soil arsenic availability and the transfer of soil arsenic to crops in suburban areas in Fujian Province, southeast China. Sci Total Environ 368(2):531–541. doi:10.1016/j.scitotenv.2006.03.013

    Article  CAS  Google Scholar 

  • Israr M, Sahi SV (2008) Promising role of plant hormones in translocation of lead in Sesbania drummondii shoots. Environ Pollut 153(1):29–36. doi:10.1016/j.envpol.2007.12.029

    Article  CAS  Google Scholar 

  • Li J, Xiao LT, Zeng GM, Huang GH, Shen GL, Yu RQ (2003) Amperometric immunosensor based on polypyrrole/poly (m-pheylenediamine) multilayer on glassy carbon electrode for cytokinin N 6-(Δ2-isopentenyl) adenosine assay. Anal Biochem 321(1):89–95. doi:10.1016/s0003-2697(03)00427-5

    Article  CAS  Google Scholar 

  • Li YY, Wang HB, Wang HJ, Yin F, Yang XY, Hu YJ (2014) Heavy metal pollution in vegetables grown in the vicinity of a multi-metal mining area in Gejiu, China: total concentrations, speciation analysis, and health risk. Environ Sci Pollut R 21(21):12569–12582. doi:10.1007/s11356-014-3188-x

    Article  CAS  Google Scholar 

  • McGrath SP, Zhao FJ (2003) Phytoextraction of metals and metalloids from contaminated soils. Curr Opin Biotech 14(3):277–282. doi:10.1016/s0958-1669(03)0060-0

    Article  CAS  Google Scholar 

  • Miyawaki K, Matsumoto-Kitano M, Kakimoto T (2004) Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. Plant J 37(1):128–138. doi:10.1046/j.1365-313X.2003.01945.x

    Article  CAS  Google Scholar 

  • Motte H, Galuszka P, Spichal L, Tarkowski P, Plihal O, Smehilova M, Jaworek P, Vereecke D, Werbrouck S, Geelen D (2013) Phenyl-adenine, identified in a light-dependent short hypocotyls4-assisted chemical screen, is a potent compound for shoot regeneration through the inhibition of cytokinin oxidase/dehydrogenase activity. Plant Physiol 161(3):1229–1241. doi:10.1104/pp.112.210716

    Article  CAS  Google Scholar 

  • Nouri J, Khorasani N, Lorestani B, Karami M, Hassani AH, Yousefi N (2009) Accumulation of heavy metals in soil and uptake by plant species with phytoremediation potential. Environ Earth Sci 59(2):315–323. doi:10.1007/s12665-009-0028-2

    Article  CAS  Google Scholar 

  • O’Brian JA, Benková E (2013) Cytokinin cross-talking during biotic and abiotic stress responses. Front Plant Sci 4(1):451. doi:10.3389/fpls.2013.00451

    Google Scholar 

  • Ouni Y, Albacete A, Cantero E, Lakhdar A, Abdelly C, Perez-Alfocea F, Barhoumi Z (2014) Influence of municipal solid waste (MSW) compost on hormonal status and biomass partitioning in two forage species growing under saline soil conditions. Ecol Eng 64(3):142–150. doi:10.1016/j.ecoleng.2013.12.053

    Article  Google Scholar 

  • Peijnenburg WJGM, Jager T (2003) Monitoring approaches to assess bioaccessibility and bioavailability of metals: matrix issues. Ecotox Environ Safe 56(56):63–77. doi:10.1016/S0147-6513(03)00051-4

    Article  CAS  Google Scholar 

  • Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14(3):290–295. doi:10.1016/j.pbi.2011.02.001

    Article  CAS  Google Scholar 

  • Peralta-Videa JR, Lopez ML, Narayan M, Saupe G, Gardea-Torresdey J (2009) The biochemistry of environmental heavy metal uptake by plants: implications for the food chain. Int J Biochem Cell B 41(8):1665–1677. doi:10.1016/j.biocel.2009.03.005

    Article  CAS  Google Scholar 

  • Piotrowska-Niczyporuk A, Bajguz A, Zambrzycka E, Godlewska-Żyłkiewicz B (2012) Phytohormones as regulators of heavy metal biosorption and toxicity in green alga Chlorella vulgaris (Chlorophyceae). Plant Physiol Bioch 52:52–65. doi:10.1016/j.plaphy.2011.11.009

  • Qin WS, Zou XJ, Qiu RL (2008) Health risk of heavy metals to the general public in Guangzhou, China via consumption of vegetables. Journal of Agro-Environment Science 27(4):1638–1642. doi:10.3321/j.issn:1672-2043.2008.04.063 in Chinese

    CAS  Google Scholar 

  • Reeves RD, Baker AJM (2000) Metal-accumulating plants. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plant to clean up the environment. Wiley, New York, pp. 193–229

    Google Scholar 

  • Reeves RD (1992) Hyperaccumulation of nickel by serpentine plants. In: Proctor J, Baker AJM, Reeves RD (eds) The vegetation of ultramafic (serpentine) soils. Intercept Ltd., Andover, UK, pp. 253–277

    Google Scholar 

  • Reguera M, Peleg Z, Abdeltawab YM, Tumimbang EB, Delatorre CA, Blumwald E (2013) Stress-induced cytokinin synthesis increases drought tolerance through the coordinated regulation of carbon and nitrogen assimilation in rice. Plant Physiol 163(4):1609–1622. doi:10.1104/pp.113.227702

    Article  CAS  Google Scholar 

  • Robert-Seilaniantz A, Navarro L, Bari R, Jones J (2007) Pathological hormone imbalances. Curr Opin Plant Biol 10(4):372–379. doi:10.1016/j.pbi.2007.06.003

    Article  CAS  Google Scholar 

  • Soongsombat P, Kruatrachue M, Chaiyarat R, Pokethitiyook P, Ngemsansaruay C (2009) Lead tolerance and accumulation in Pteris vittata and Pityrogramma calomelanos, and their potential for phytoremediation of lead-contaminated soil. Int J Phytorem 11(4):396–412. doi:10.1080/15226510802565634

    Article  CAS  Google Scholar 

  • Sun YB, Zhou QX, Liu WT, An J, Xu ZQ, Wang L (2009) Joint effects of arsenic and cadmium on plant growth and metal bioaccumulation: a potential Cd-hyperaccumulator and As-excluder Bidens pilosa L. J Hazard Mater 165(1–3):1023–1028. doi:10.1016/j.jhazmat.2008.10.097

    Article  CAS  Google Scholar 

  • Tamás L, Dudíková J, Ďurčeková K, Huttová J, Mistrík I, Zelinová V (2008) The impacts of heavy metals on the activity of some enzymes along the barley root. Environ Exp Bot 62(1):86–91. doi:10.1016/j.envexpbot.2007.07.009

    Article  Google Scholar 

  • Vangronsveld J, Herzig R, Weyens N, Boulet J, Adriaensen K, Ruttens A, Thewys T, Vassilev A, Meers E, Nehnevajova E (2009) Phytoremediation of contaminated soils and groundwater: lessons from the field. Environ Sci Pollut R 16(7):765–794. doi:10.1007/s11356-009-0213-6

    Article  CAS  Google Scholar 

  • Wei SH, Yang CJ, Zhou QX (2008) Hyperaccumulative characteristics of 7 widely distributing weed species in composite family especially Bidens pilosa to heavy metals. Chinese. Journal of Environmental Science 29(10):2912–2918. doi:10.3321/j.issn:0250-3301.2008.10.039 in Chinese

    Google Scholar 

  • Xiao XY, Chen TB, An ZZ, Lei M, Huang ZC, Liao XY, Liu YR (2008) Potential of Pteris vittata L. for phytoremediation of sites co-contaminated with cadmium and arsenic: the tolerance and accumulation. J Environ Sci-China 20:62–67. doi:10.1016/S1001-0742(08)60009-1

    Article  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (Grant No. 31360132) and Candidates of the Young and Middle Aged Academic Leaders of Yunnan Province (2012HB007).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hongbin Wang.

Additional information

Responsible Editor: Elena Maestri

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, Q., Yang, X., Wang, H. et al. Endogenous trans-zeatin content in plants with different metal-accumulating ability: a field survey. Environ Sci Pollut Res 23, 23422–23435 (2016). https://doi.org/10.1007/s11356-016-7544-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-016-7544-x

Keywords

Navigation