Silicon alleviates cadmium toxicity by enhanced photosynthetic rate and modified bundle sheath's cell chloroplasts ultrastructure in maize Marek Vaculík a,n , Andrej Pavlovič a,b , Alexander Lux a a Department of Plant Physiology, Faculty of Natural Sciences, Comenius University in Bratislava, Mlynská dolina B2, SK-84215 Bratislava, Slovakia b Department of Biophysics, Centre of the Region Haná for Biotechnological and Agricultural Research, Palacký University in Olomouc, Šlechtitelů 11, CZ-783 71 Olomouc, Czech Republic article info Article history: Received 27 February 2015 Received in revised form 15 May 2015 Accepted 16 May 2015 Keywords: C4 plant anatomy and physiology Cadmium (Cd) Chloroplast ultrastructure Chlorophyll a fluorescence Photosynthesis Silicon (Si) abstract Silicon was shown to alleviate the negative effects of various biotic and abiotic stresses on plant growth. Although the positive role of Si on toxic and heavy metal Cd has been already described, the mechanisms have been explained only partially and still remain unclear. In the present study we investigated the effect of Si on photosynthetic-related processes in maize exposed to two different levels of Cd via measurements of net photosynthetic rate (A N ), chlorophyll a fluorescence and pigment analysis, as well as studies of leaf tissue anatomy and cell ultrastructure using bright-field and transmission electron microscopy. We found that Si actively alleviated the toxic syndromes of Cd by increasing A N , effective photochemical quantum yield of photosystem II (ϕ PSII ) and content of assimilation pigments, although did not decrease the concentration of Cd in leaf tissues. Cadmium did not affect the leaf anatomy and ultrastructure of leaf mesophyll’s cell chloroplasts; however, Cd negatively affected thylakoid formation in chloroplasts of bundle sheath cells, and this was alleviated by Si. Improved thylakoid formation in bundle sheath’s cell chloroplasts may contribute to Si-induced enhancement of photosynthesis and re- lated increase in biomass production in C4 plant maize. & 2015 Elsevier Inc. All rights reserved. 1. Introduction Silicon (Si) and its importance for plant growth and develop- ment is documented by several research papers published during the last years. Although this second most abundant element in the earth crust is not easily accessible for plants, some of them, mostly from the family Poaceae, take up this element in relatively high amount (Wiese et al., 2007). In addition to the importance of Si in plant nutrition, optimal growth and development (Guntzer et al., 2012), it plays a significant role in the alleviation of various symptoms of biotic as well as abiotic stresses (Ma, 2004). It was also shown that Si can alleviate iron deficiency (Pavlovic et al., 2013). On the other hand, it is known that Si can decrease the negative effects of elements, including some heavy metals, when present in excess (Liang et al., 2007; Balakhina and Borkowska, 2013; Wu et al., 2013). Formation of aluminosilicates in the pre- sence of Si was suggested as mechanism of detoxification of alu- minum (Al) excess in some plants (e.g. Pragabar et al., 2011). Si- milarly, the mitigation role of Si has been recently described for several other metals or dangerous toxic elements, including chromium (Ali et al., 2013), lead (Li et al., 2012), antimony (Huang et al., 2012; Vaculíková et al., 2014) or arsenic (Fleck et al., 2013; Tripathi et al., 2013). Previously, it has been reported that Si can mitigate negative influence of dangerous heavy metal cadmium (Cd) on growth of various plants. In maize, the alleviation of Cd toxicity was partially attributed to Si-enhanced cell wall elasticity and plasticity (Vaculík et al., 2009) as well as increased deposition of Cd in the cell walls (Vaculík et al., 2012; Lukačová et al., 2013). Decrease in plant Cd uptake and translocation from root to shoot was suggested as other beneficial role of Si in many species, including maize (Liang et al., 2005, Da Cunha et al., 2008), Solanum nigrum (Liu et al., 2013b) or mangrove seedlings (Zhang et al., 2013), although this feature seems to be species and/or cultivar specific and also de- pends on the concentration of used chemicals (Liang et al., 2005; Vaculík et al., 2009; Lukačová et al., 2013). Additionally, the alle- viative effect of Si on Cd toxicity was partially attributed to the changes in the activity of important antioxidative enzymes in- volved in scavenging of free radicals formed by presence of Cd in pakchoi (Song et al., 2009); maize (Lukačová et al., 2013), S. nigrum (Liu et al., 2013b) and other species. There are also some reports that Si influences the development of apoplasmic barriers, root suberization and lignification, as well as modifies leaf and root anatomy in plants exposed to Cd (Da Cunha and do Nascimento Contents lists available at ScienceDirect journal homepage: www.elsevier.com/locate/ecoenv Ecotoxicology and Environmental Safety http://dx.doi.org/10.1016/j.ecoenv.2015.05.026 0147-6513/& 2015 Elsevier Inc. All rights reserved. n Corresponding author. Fax: þ421 265429064. E-mail address: vaculik@fns.uniba.sk (M. Vaculík). Ecotoxicology and Environmental Safety 120 (2015) 66–73