Abstract
Mechanisms of Pteris vittata L. to hyperaccumulate arsenic (As), especially the efficient translocation of As from rhizoids to fronds, are not clear yet. The present study aims to investigate the role of transpiration in the accumulation of As from the aspects of transpiration regulation and ecotypic difference. Results showed that As accumulation of P. vittata increased proportionally with an increase in the As exposure concentration. Lowering the transpiration rate by 28∼67 % decreased the shoot As concentration by 19∼56 %. Comparison of As distribution under normal treatment and shade treatment indicated that transpiration determines the distribution pattern of As in pinnae. In terms of the ecotypic difference, the P. vittata ecotype from moister and warmer habitat had 40 % higher transpiration and correspondingly 40 % higher shoot As concentration than the ecotype from drier and cooler habitat. Results disclosed that transpiration is the main driver for P. vittata to accumulate and re-distribute As in pinnae.
Similar content being viewed by others
References
Abd El Rahman HF, Krzywinski K (2008) Environmental effects on morphology of Acacia tortilis group in the Red Sea Hills, North-Eastern Sudan and South-Eastern Egypt. For Ecol Manag 255:254–263
Bartoli F, Coinchelin D, Robin C, Echevarria G (2012) Impact of active transport and transpiration on nickel and cadmium accumulation in the leaves of the Ni-hyperaccumulator Leptoplax emarginata: a biophysical approach. Plant Soil 350:99–115
Basta NT, Ryan JA, Chaney RL (2005) Trace element chemistry in residual-treated soil: key concepts and metal bioavailability. J Environ Qual 34:49–63
Bhatia NP, Baker AJM, Walsh KB, Midmore DJ (2005) A role for nickel in osmotic adjustment in drought-stressed plants of the nickel hyperaccumulator Stackhousia tryonii Bailey. Planta 223:134–139
Cappa JJ, Pilon-Smits EAH (2014) Evolutionary aspects of elemental hyperaccumulation. Planta 239:267–275
Chen TB, Wei CY, Huang ZC, Huang QF, Lu QG, Fan ZL (2002) Arsenic hyperaccumulator Pteris vittata L. and its arsenic accumulation. Chin Sci Bull 47:902–905
Chen TB, Yan XL, Liao XY, Xiao XY, Huang ZC, Xie H, Zhai LM (2005) Subcellular distribution and compartmentalization of arsenic in Pteris vittata L. Chin Sci Bull 50:2843–2849
Dinis LT, Peixoto F, Pinto T, Costa R, Bennett RN, Gomes-Laranjo J (2011) Study of morphological and phenological diversity in chestnut trees (‘Judia’ variety) as a function of temperature sum. Environ Exp Bot 70:110–120
Dodd I, Davies W, Egea G (2007) Transport of growth regulators from roots in drying soil during partial rootzone drying: the mechanics of a new deficit irrigation technique. Comp Biochem Phys A 146:S239–S239
Guo HM, Zhong ZN, Lei M, Xue XL, Wan XM, Zhao JY, Chen TB (2012) Arsenic uptake from arsenic-contaminated water using hyperaccumulator Pteris vittata L.: effect of chloride, bicarbonate, and arsenic species. Water Air Soil Pollut 223:4209–4220
Hinsinger, P., 1998. How do plant roots acquire mineral nutrients? Chemical processes involved in the rhizosphere. In: Donald, LS (ed) Advances in agronomy. Academic Press, USA, pp. 225–265.
Hu T, Kang S, Zhang F, Zhang J (2006) Alternate application of osmotic and nitrogen stresses to partial root system: effects on root growth and nitrogen use efficiency. J Plant Nutr 29:2079–2092
Kholodova V, Volkov K, Abdeyeva A, Kuznetsov V (2011) Water status in Mesembryanthemum crystallinum under heavy metal stress. Environ Exp Bot 71:382–389
Lee SJ, Lee JP (2011) Effect of arsenic absorption on the water-refilling speed of Pteris cretica. Microsc Res Tech 74:517–522
Lei M, Wan X-M, Huang Z-C, Chen T-B, Li X-W, Liu Y-R (2012) First evidence on different transportation modes of arsenic and phosphorus in arsenic hyperaccumulator Pteris vittata. Environ Pollut 161:1–7
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
Liu XQ, Peng KJ, Wang AG, Lian CL, Shen ZG (2010) Cadmium accumulation and distribution in populations of Phytolacca americana L. and the role of transpiration. Chemosphere 78:1136–1141
Lombi E, Zhao FJ, Dunham SJ, McGrath SP (2000) Cadmium accumulation in populations of Thlaspi caerulescens and Thlaspi goesingense. New Phytol 145:11–20
Lu L-L, Tian S-K, Yang X-E, Li T-Q, He Z-L (2009) Cadmium uptake and xylem loading are active processes in the hyperaccumulator Sedum alfredii. J Plant Physiol 166:579–587
Luu DT, Maurel C (2005) Aquaporins in a challenging environment: molecular gears for adjusting plant water status. Plant Cell Environ 28:85–96
Ma CC, Gao YB, Guo HY, Wang JL, Wu JB, Xu JS (2008) Physiological adaptations of four dominant Caragana species in the desert region of the Inner Mongolia Plateau. J Arid Environ 72:247–254
Ma LQ, Komar KM, Tu C, Zhang W, Cai Y, Kennelley ED (2001) A fern that hyperaccumulates arsenic. Nature 409:579
Mathews S, Rathinasabapathi B, Ma LQ (2011) Uptake and translocation of arsenite by Pteris vittata L.: effects of glycerol, antimonite and silver. Environ Pollut 159:3490–3495
Michel BE, Kaufmann MR (1973) The osmotic potential of polyethylene glycol 6000. Plant Physiol 51:914–916
Money NP (1989) Osmotic pressure of aqueous polyethylene glycols. Plant Physiol 91:766–769
Mukhopadhyay R, Bhattacharjee H, Rosen BP (2014) Aquaglyceroporins: generalized metalloid channels. Biochim Biophys Acta Gen Subj 1840:1583–1591
Pollard AJ, Reeves RD, Baker AJM (2014) Facultative hyperaccumulation of heavy metals and metalloids. Plant Sci 217–218:8–17
Poynton CY, Huang JWW, Blaylock MJ, Kochian LV, Elless MP (2004) Mechanisms of arsenic hyperaccumulation in Pteris species: root As influx and translocation. Planta 219:1080–1088
Preston GM, Carroll TP, Guggino WB, Agre P (1992) Appearance of water channels in Xenopus oocytes expressing red-cells CHIP28 protein. Science 256:385–387
Russell RS, Shorrocks VM (1959) The relationship between transpiration and the absorption of inorganic ions by intact plants. J Exp Bot 10:301–316
Salt DE, Prince RC, Pickering IJ, Raskin I (1995) Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol 109:1427–1433
Shen RF, Ma JF (2001) Distribution and mobility of aluminium in an Al-accumulating plant, Fagopyrum esculentum Moench. J Exp Bot 52:1683–1687
Souto CP, Premoli AC, Reich PB (2009) Complex bioclimatic and soil gradients shape leaf trait variation in Embothrium coccineum (Proteaceae) among austral forests in Patagonia. Revista Chilena De Historia Nat 82:209–222
Su YH, McGrath SP, Zhu YG, Zhao FJ (2008) Highly efficient xylem transport of arsenite in the arsenic hyperaccumulator Pteris vittata. New Phytol 180:434–441
Thomas D, Bron P, Ranchy G, Duchesne L, Cavalier A, Rolland J-P, Raguénès-Nicol C, Hubert J-F, Haase W, Delamarche C (2002) Aquaglyceroporins, one channel for two molecules. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1555:181–186
Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181:759–776
Vernay P, Gauthier-Moussard C, Hitmi A (2007) Interaction of bioaccumulation of heavy metal chromium with water relation, mineral nutrition and photosynthesis in developed leaves of Lolium perenne L. Chemosphere 68:1563–1575
Wan XM, Lei M, Liu YR, Huang ZC, Chen TB, Gao D (2013) A comparison of arsenic accumulation and tolerance among four populations of Pteris vittata from habitats with a gradient of arsenic concentration. Sci Total Environ 442:143–151
Wierzbicka M, Pielichowska M (2004) Adaptation of Biscutella laevigata L, a metal hyperaccumulator, to growth on a zinc-lead waste heap in southern Poland - I: differences between waste-heap and mountain populations. Chemosphere 54:1663–1674
Yang XE, Chao YE, Ye HB, He ZL, Stoffella PJ (2010) Zinc and lead accumulation by two contrasting ecotypes of Sedum alfredii Hance at different zinc/lead complex levels. Commun Soil Sci Plant Anal 41:516–525
Zhang X, Wu N, Li C (2005) Physiological and growth responses of Populus davidiana ecotypes to different soil water contents. J Arid Environ 60:567–579
Zhao JY, Guo HM (2013) Arsenic uptake from arsenic-contaminated water using Pteris vittata L. and Polystichum craspedosorum. In: Tang X, Zhong W, Zhuang D, Li C, Liu Y (eds) Progress in environmental protection and processing of resource, vol 1–4, Pts., pp 1139–1143
Acknowledgments
We thank Dr. Augustine Doronila from the University of Melbourne for improving the manuscript. Financial support was provided by the National Natural Science Foundation of China (Grant Nos. 41301547), the Program for “Bingwei” Excellent Talents in the Institute of Geographic Sciences and Natural Resources Research, CAS, and the special fund for environment protection research in the public interest (No. 201409044).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Elena Maestri
Rights and permissions
About this article
Cite this article
Wan, Xm., Lei, M., Chen, Tb. et al. Role of transpiration in arsenic accumulation of hyperaccumulator Pteris vittata L.. Environ Sci Pollut Res 22, 16631–16639 (2015). https://doi.org/10.1007/s11356-015-4746-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-015-4746-6