Cadmium (Cd) is a toxic metal to living organisms when certain limits are exceeded in their cells and tissues. Once this metal exceeds these tolerance limits, disorders of physiological, biochemical and molecular nature can occur, including imbalances in the uptake and in the transport of nutrients, which may ultimately inhibit plant growth, development and reproduction. Since this metal shows high mobility and low affinity for soil colloids (Akoumianakis et al. 2008, Erdem et al. 2012), it easily enters the trophic chain and has been implicated in various diseases including anemia, pulmonary edema, liver, nerve and brain damage, cancer and even death (ATSDR 2012). In fact, Cd is the most dangerous of all metals since it is the only element that can damage human and animal cells at concentrations that are not toxic in plants (Peijnenburg et al. 2000, Peralta-Videa et al. 2009).

Despite the danger that cadmium poses to human health, Mexico does not have a plan or strategy for either managing it or reducing its use in the manufacture of toys and industrial products such as batteries and fertilizers (Godoy 2011). In addition, the country produces more than 1600 t of cadmium annually and exports fertilizers as well as chemical, plastic and non-corrosive products containing this metal. Mexico also imports considerable quantities of nickel-cadmium batteries that when discarded, exacerbate environmental pollution. Hence, recent studies have found the presence of this metal in some foods at concentrations far exceeding the levels allowed by international standards for human consumption, which represents a huge public health risk (Gama-Flores et al. 2007, Peralta-Videa et al. 2009, Lango-Reynoso et al. 2010, Godoy 2011). As a result, some research groups in the country have focused their attention on studying this matter in greater detail.

In plants, the toxic effects of Cd include oxidative stress, genotoxicity, oxidation of the photosynthetic apparatus, and inhibition of root metabolism (Andresen and Küpper 2013), through its interaction with soil minerals and microbial populations, which in turn alters the uptake of nutrients. Stomatal opening, transpiration and photosynthesis are other processes also affected by Cd. Chlorosis, leaf curls and stunting are the most visible symptoms of Cd toxicity. Chlorosis can be caused by deficiencies in Fe and P or by reduced transport of Mn, and in general, toxic Cd levels interfere with the uptake, transport, mobility and use of nutrients and water in the plant. Cd also affects membrane permeability because it causes lipid peroxidation, which reduces the water content in the cell and alters the organism's water balance. Cd also reduces ATPase activity and causes changes in chloroplast metabolism by inhibiting chlorophyll biosynthesis and reducing the activity of enzymes involved in CO₂ fixation. Oxidative stress caused by toxic Cd levels is determined by inducing the production of free radicals derived from the transport of membrane electrons, chloroplasts and mitochondria, and the decrease in antioxidant system activity, which leads to senescence and cell death in extreme conditions (Benavides et al. 2005, Erdem et al. 2012, Nazar et al. 2012), and which depends on the homeostatic mechanisms that the plant has developed through evolution, making it possible to observe different responses between genotypes. As pepper is one of the most cultivated vegetable and spice crops worldwide, and Mexican sweet pepper production is facing serious environmental problems including heavy metal pollution, this research aimed to analyze the effect of Cd on growth, chlorophyll concentration and the accumulation of some nutrients and Cd in different parts of Yolo Wonder variety sweet pepper (Capsicum annuum L.) seedlings.

In general, the growth of sweet pepper plants decreased with the increased Cd levels in the nutrient solution. These results coincide with those that have been reported by Chen et al. (2011), who observed gradual reductions in growth and development in mustard (Sinapis alba) and Chinese cabbage (Brassica rapa L. var. rosularis) treated with Cd added to the soil at concentrations of 0-24 mg/kg. These authors reported that the application of 24 mg/kg Cd to the soil, significantly reduced chlorophyll a and b contents compared to the control treatment: chlorophyll a fell by 32.29 and 20.56 % in cabbage and mustard, respectively, while the reductions in chlorophyll b were 21.54 y 21.55 %, respectively.

In sorghum, Liu et al. (2011) observed decreased root activity when Cd was added to the soil at concentrations of 50 and 100 mg/kg, and concluded that Cd decreases primary root elongation and lateral root growth. Meanwhile, Dong et al. (2005) reported that the addition of 1 and 10 mmol/L Cd in the nutrient solution of tomato decreased plant height by 18.9 and 46.4 %, respectively, root length by 25.8 and 41.1 %, respectively, and root volume by 45.2 and 63.7 %, respectively, compared to the control.

Blum (1997) noted that the reduction in foliar area is an evasion mechanism that minimizes water loss under stress conditions due to toxic metals. Likewise, in the case of this study, foliar area decreased with increased Cd levels in the nutrient solution.

Astolfi et al. (2005) observed that Cd treatment produces an inhibition in plasma membrane H⁺ATPase activity. Also, Ali et al. (2000) and Maksymiec et al. (2007) pointed out that as a result of the presence of Cd in the plant, there are imbalances in chloroplast metabolism, which inhibits chlorophyll synthesis and reduces the activity of enzymes involved in CO₂ fixing. These findings are also consistent with the results in this study, since the presence of Cd in the growth medium significantly decreased the chlorophyll content in pepper leaves.

Nazar et al. (2012) reported that high Cd levels in the soil alter the uptake and translocation of nutrients, which leads to nutrient deficiencies, oxidative stress, and decreased plant growth and development. In the case of the present study, the accumulation of all the nutrients assessed (N, P and K) decreased in the presence of Cd.

Cadmium accumulates preferentially in the root, and is sequestered in the vacuole of the cells, while only a small fraction is transported to the plant shoot, concentrating in descending order in the stems, leaves, fruits and seeds (Chan and Hale 2004). Likewise, Jidesh and Kurumthottical (2000) found that the highest Cd accumulation occurred in roots compared to other plant organs of the sweet pepper. In our study, the order of Cd accumulation in planta was as follows: roots > leaves > stems (Fig. 3).

Comparatively, the Yolo Wonder variety evaluated is a genotype very sensitive to Cd toxicity, since in preliminary studies (data not shown), seedlings subjected to more than 50 μM Cd in solution did not tolerate more than a day without presenting severe defoliation and visible morphological damage. Similarly, Abdel-Latef (2013) showed that the application of 100 μM Cd severely affected physiological and biochemical variables in pepper plants variety Zhongjiao. Conversely, Ramachandran and Vincent (2013) demonstrated that five different pepper genotypes could tolerate concentrations ranging between 125 and 500 μM Cd in solution, although differential responses were also observed among genetic materials. Moreover, in comparison to other plant species, Sereno et al. (2007) reported that sugarcane can tolerate up to 500 μM of Cd without showing any signs of toxicity. This behavior has also been recently confirmed by Trejo-Téllez et al. (2014), as sugarcane cultivar CP 72-2086 showed no effects of 1 mM Cd on K, Ca, Fe and Mn concentrations in leaves. Therefore, screening for more pepper genotypes would increase our understanding of how this genetic diversity possesses different reservoirs of physiological, biochemical and molecular mechanisms to tolerate Cd.

This research demonstrated that the addition of 15 and 30 μM Cd to the nutrient solution significantly decreases plant height, foliar area, chlorophyll content in leaves and the accumulation of N, P and K in different plant tissues. Additionally, the Cd showed the highest accumulation in roots, followed by leaves and stems.