Abstract
Cadmium uptake, tissue localization and structural changes induced at cellular level are essential to understand Cd tolerance in plants. In this study we have exposed plants of Pteris vittata to different concentrations of CdCl2 (0, 30, 60, 100 μM) to evaluate the tolerance of the fern to cadmium. Cadmium content determination and its histochemical localization showed that P. vittata not only takes up, but also transports and accumulates cadmium in the aboveground tissues, delocalizing it mainly in the less bioactive tissues of the frond, the trichomes and the scales. Cadmium tolerance in P. vittata was strictly related to morphogenic response induced by the metal itself in the root system. Adaptive response regarded changes of the root apex size, the developmental pattern of root hairs, the differentiation of xylem elements and endodermal suberin lamellae. All the considered parameters suggest that, in our experimental conditions, 60 μM of Cd may represent the highest concentration that P. vittata can tolerate; indeed this Cd level even improves the absorbance features of the root and allows good transport and accumulation of the metal in the fronds. The results of this study can provide useful information for phytoremediation strategies of soils contaminated by Cd, exploiting the established ability of P. vittata to transport, delocalize in the aboveground biomass and accumulate polluting metals.
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Benavides M, Gallego SM, Tomaro ML (2005) Cadmium toxicity in plants. Braz J Plant Physiol 17:49–55. doi:10.1590/S1677-04202005000100003
Brundrett MC, Enstone DE, Peterson CA (1988) A berberine–aniline blue fluorescent staining procedure for suberin, lignin, and callose in plant tissue. Protoplasma 146:133–142. doi:10.1007/BF01405922
Brundrett MC, Kendrick B, Peterson CA (1991) Efficient lipid staining in plant material with Sudan red 7B or fluoral yellow 088 in polyethylene glycol-glycerol. Biotech Histochem 66:111–116. doi:10.3109/10520299109110562
Chen T, Wei C, Huang Z, Huang Q, Lu Q, Fan Z (2002) Arsenic hyperaccumulator Pteris vittata L. and its arsenic accumulation. Chinese Sci Bull 47:902–905. doi:10.1360/02tb9202
Curie C, Cassin G, Couch D, Divol F, Higuchi K, Le Jean M, Misson J, Schikora A, Czernic P, Mari S (2009) Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters. Ann Bot 103:1–11. doi:10.1093/aob/mcn207
Degraeve N (1981) Carcinogenic, teratogenic and mutagenic effects of cadmium. Mutat Res 86:115–135. doi:10.1016/0165-1110(81)90035-X
Drava G, Roccotiello E, Minganti V, Manfredi A, Cornara L (2012) Effects of cadmium and arsenic on Pteris vittata under hydroponic conditions. Environ Tox Chem 31:1375–1380. doi:10.1002/etc.1835
Driouich A, Durand C, Vicré M (2007) Formation and separation of root border cells. Trends Plant Sci 12:14–19. doi:10.1016/j.tplants.2006.11.003
Ďurčeková K, Huttová J, Mistrík I, Ollé M, Tamás L (2007) Cadmium induces premature xylogenesis in barley roots. Plant Soil 290:61–68. doi:10.1007/s11104-006-9111-6
Fayiga AO, Ma LQ, Cao X, Rathinasabapathi B (2004) Effect of heavy metals on growth of Pteris vittata. Environ Pollut 132:289–296. doi:10.1016/j.envpol.2004.04.020
Feder N, O’Brien TP (1968) Plant microtechnique: some principles and new methods. Am J Bot 55:123–142. doi:10.2307/2440500
Fischer RA (1968) Stomatal opening in isolated epidermal strips of Vicia faba. I. Response to light and to CO2-free air. Plant Physiol 43:1947–1952. doi:10.1104/pp.43.12.1947
Forino LMC, Ruffini Castiglione M, Bartoli G, Balestri M, Andreucci A, Tagliasacchi AM (2012) Arsenic-induced morphogenic response in roots of arsenic hyperaccumulator fern Pteris vittata. J Hazard Mater 235–236:271–278. doi:10.1016/j.jhazmat.2012.07.051
Groudev SN, Spasova II, Georgiev PS (2001) In situ bioremediation of soils contaminated with radioactive elements and toxic heavy metals. Int J Miner Process 62:301–308. doi:10.1016/S0301-7516(00)00061-2
Gupta M, Devi S (1994) Chronic toxicity of cadmium in Pteris vittata, a roadside fern. Ecotoxicology 3:235–247. doi:10.1007/BF00117990
Kim MJ, Ahn KH, Jung Y, Lee S, Lim BR (2003) Arsenic, cadmium, chromium, copper, lead, and zinc contamination in mine tailings and nearby streams of three abandoned mines from Korea. Bull Environ Contam Toxicol 70:942–947. doi:10.1007/s00128-003-0073-6
Küpper H, Lombi E, Zhao FJ, McGrath SP (2000) Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 212:75–84. doi:10.1007/s004250000366
Li WX, Chen TB, Chen Y, Lei M (2005) Role of trichome of Pteris vittata L. in arsenic hyperaccumulation. Sci China Ser C 48:148–154. doi:10.1007/BF02879667
Li T, Yang X, Lu L, Islam E, He Z (2009) Effects of zinc and cadmium interactions on root morphology and metal translocation in a hyperaccumulating species under hydroponic conditions. J Hazard Mater 169:734–741. doi:10.1016/j.jhazmat.2009.04.004
Lillie RD (1965) Histopathology Technique and Practical Histochemistry. McGrawn-Hill Book Company, London
Lombi E, Zhao FJ, Fuhrmann M, Ma LQ, McGrath SP (2002) Arsenic distribution and speciation in the fronds of the hyperaccumulator Pteris vittata. New Phytol 156:195–203. doi:10.1046/j.1469-8137.2002.00512.x
Lux A, Martinka M, Vaculík M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37. doi:10.1093/jxb/erq281
Martinka M, Lux A (2004) Response of roots of three populations of Silene dioica to cadmium treatment. Biologia 59:185–189
Michalak A (2006) Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Polish J Environ Stud 15:523–530
Miyasaka SC, Hawes MC (2001) Possible role of root border cells in detection and avoidance of aluminum toxicity. Plant Physiol 125:1978–1987. doi:10.1104/pp.125.4.1978
Pielichowska M, Wierzbicka M (2004) Uptake and localization of cadmium by Biscutella leavigata, a cadmium hyperaccumulator. Acta Biol Cracov Bot 46:57–63
Pineros MA, Shaff JE, Kochian LV (1998) Development, characterization, and application of a cadmium-selective microelectrode for the measurement of cadmium fluxes in roots of Thlaspi species and wheat. Plant Physiol 116:1393–1401. doi:10.1104/pp.116.4.1393
Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MAK (2007) Stress-induced morphogenic responses: growing out of trouble? Trends Plant Sci 12:98–105. doi:10.1016/j.tplants.2007.01.004
Redjala T, Zelko I, Sterckeman T, Legué V, Lux A (2011) Relationship between root structure and root cadmium uptake in maize. Environ Exp Bot 71:241–248. doi:10.1016/j.envexpbot.2010.12.010
Sass JE (1958) Botanical microtechnique, 3rd edn. Iowa State College Press, Ames
Seregin IV, Ivanov VB (1997) Histochemical investigation of cadmium and lead distribution in plants. Russ J Plant Physiol 44:791–796
Tu C, Ma L (2002) Effects of arsenic concentrations and forms on arsenic uptake by the hyperaccumulator ladder brake. J Environ Qual 31:641–647. doi:10.2134/jeq2002.0641
Vaculík M, Lux A, Luxová M, Tanimoto E, Lichtscheidl I (2009) Silicon mitigates cadmium inhibitory effects in young maize plants. Environ Exp Bot 67:52–58. doi:10.1016/j.envexpbot.2009.06.012
Verbruggen N, Hermans C, Schat H (2009) Mechanisms to cope with arsenic or cadmium excess in plants. Curr Opin Plant Biol 12:364–372. doi:10.1016/j.pbi.2009.05.001
Vieira da Cunha KP, Araújo do Nascimento CW, de Magalhães Mendonça Pimentel R, Pereira Ferreira C (2008) Cellular localization of cadmium and structural changes in maize plants grown on a cadmium contaminated soil with and without liming. J Hazard Mater 160:228–234. doi:10.1016/j.jhazmat.2008.02.118
Wang J, Zhao FJ, Meharg AA, Raab A, Feldmann J, McGrath SP (2002) Mechanisms of arsenic hyperaccumulation in Pteris vittata. Uptake kinetics, interactions with phosphate, and arsenic speciation. Plant Physiol 130:1552–1561. doi:10.1104/pp.008185
Xiao X, Chen T, An Z, Lei M, Huang Z, Liao X, Liu Y (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
Zelko I, Lux A (2004) Effect of cadmium on Karwinskia humboldtiana roots. Biologia 59:205–209
Zelko I, Lux A, Sterckeman T, Martinka M, Kollárová K, Lišková D (2012) An easy method for cutting and fluorescent staining of thin roots. Ann Bot 110:475–478. doi:10.1093/aob/mcs046
Zheng R, Li H, Jiang R, Römheld V, Zhang F, Zhao FJ (2011) The role of root hairs in cadmium acquisition by barley. Environ Pollut 159:408–415. doi:10.1016/j.envpol.2010.10.034
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This work was supported by local funding of the University of Pisa (ex 60 %) and by the grants of Slovak Research and Development Agency (contract APVV-0140-10) and the COST Action FA-0905.
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Balestri, M., Ceccarini, A., Forino, L.M.C. et al. Cadmium uptake, localization and stress-induced morphogenic response in the fern Pteris vittata . Planta 239, 1055–1064 (2014). https://doi.org/10.1007/s00425-014-2036-z
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DOI: https://doi.org/10.1007/s00425-014-2036-z