A bisphosphonate increasing the shoot biomass of the metal hyperaccumulator Noccaea caerulescens Aino-Liisa Alanne a,⇑ , Sirpa Peräniemi a , Petri Turhanen a , Marjo Tuomainen b , Jouko Vepsäläinen a , Arja Tervahauta b a School of Pharmacy, Biocenter Kuopio, University of Eastern Finland, P.O. Box 1627, FIN-70211 Kuopio, Finland b Department of Biology, Kuopio Campus, University of Eastern Finland, P.O. Box 1627, FIN-70211 Kuopio, Finland highlights The effects of 7 bisphosphonates on the growth by N. caerulescens were studied. Also the shoot metal removal was investigated. The plants were grown in soils spiked with Cd, Ni, Zn and Pb. An insoluble aminobisphosphonate was found to enhance the plant growth in Ni-spiked soil. Therefore, also the shoot Ni removal was increased by the bisphosphonate. article info Article history: Received 28 June 2013 Received in revised form 16 September 2013 Accepted 25 September 2013 Available online 29 October 2013 Keywords: Bisphosphonates Noccaea caerulescens Metal uptake Phytoremediation Nickel abstract The feasibility of using the hyperaccumulator plant, Noccaea caerulescens, to remove trace elements from contaminated soils has been studied extensively. However, this plant creates too low biomass and an inappropriately slow growth rate for actual use in the field. Soluble bisphosphonates (BPs) are well- known pharmaceutical compounds e.g. affecting the osteoclast function in body through metabolic path- ways. We devised an insoluble aminoBP, hydroxyundecylidene-1,1,-bisphosphonic acid with a long alkyl chain to be extremely effective metal chelator, and its possible use in phytoremediation deserves more attention. This article examines the effects of seven BPs on the shoot biomass, shoot metal concentrations and removal (Cd, Ni, Zn and Pb) by N. caerulescens in a pot experiment. The soluble BPs were incorporated into the soil in the irrigation water and the insoluble BP as solid after which the soil was spiked with met- als. The insoluble aminoBP was found to considerably increase the shoot yield of N. caerulescens, espe- cially in Ni-spiked soil, thus showing enhanced shoot Ni removal. Ó 2013 Elsevier Ltd. All rights reserved. 1. Introduction Phytoremediation, the use of plants and associated microorgan- isms to remove pollutants or make them harmless in soil, is a puta- tive solution for the ever increasing problems originating from water and soil contamination (Salt et al., 1998; Vangronsveld et al., 2009; Vamerali et al., 2010; Ali et al., 2013; van der Ent et al., 2013). Trace elements, which originate from the anthropo- genic activity such as main tailings, use of fertilizers and pesticides, industrial discharge etc., are one of the main pollutants in soil and currently a cause of public concern. Phytoextraction refers to the use of plants to remove metal(loid)s from soil by concentrating them in the harvestable parts of the plants. It is both an ecological and economical way to remove harmful contaminants but it poses certain requirements for the characteristics of the plant: the ideal plant should be able to take up metal ions effectively from soil into the root cells, load them in xylem and transport the metals from roots to shoots. In the leaves, metal ions are stored within the cells and detoxified effectively (Meyer and Verbruggen, 2012). Noccaea caerulescens (previously named Thlaspi caerulescens) is a well-studied plant, hyperaccumulating zinc (Zn), cadmium (Cd) and nickel (Ni) (McGrath et al., 2006; Vangronsveld et al., 2009; Bhargava et al., 2012). Unfortunately, the plant has a low biomass and a slow growth rate, these characteristics virtually exclude the possibility of using the plant in the field for phytoextraction. Gen- erally, the increase of the biomass of plants can be accomplished by using fertilizers. However, N, P and S fertilization has been shown not to affect strongly the shoot biomass of N. caerulescens (Sirguey et al., 2006). Another way to increase the biomass could be by genetic engineering (Martínez et al., 2006). The possibility of adding chelating agents into the soil for increasing metal 0045-6535/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.chemosphere.2013.09.116 ⇑ Corresponding author. Tel.: +358 403553826. E-mail address: aino.alanne@uef.fi (A.-L. Alanne). Chemosphere 95 (2014) 566–571 Contents lists available at ScienceDirect Chemosphere journal homepage: www.elsevier.com/locate/chemosphere