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The genus Brassica Brassicaceae includes more than 30 species plus several varieties and hybrids [ 1 ]. Among these are several important species in agriculture, used for human consumption, animal fodder, condiments, oil production, biofuel, among others [ 2 ]. Common vegetables used for human consumption are included in this genus, including several Brassica oleracea varieties like cabbages, broccoli, cauliflower and Brussel sprouts.

They are considered a source of many nutrients such as carotenoids, tocopherols, different essential elements, carbohydrates and amino acids [ 3 , 4 ]. Several Brassica species are known metal accumulators and have been evaluated as potential phytoextraction plants [ 5 , 6 ]. The fact that some of these plants can accumulate relatively high amounts of toxic metals, without visible symptoms, and are also food crops, leads to potential contamination of the food chain [ 7 ] and this has to be taken into account in any phytoremediation process. The potential use of Brassica species in phytoremediation mainly phytoextraction stems from its intrinsic tolerance to heavy metals and considerable above-ground biomass production [ 8 ].

This review will focus mainly on six economically important species: Brassica juncea , B. Brassica juncea Indian mustard is important in oil production, has medicinal properties and is used as a condiment. It is a tolerant plant to heavy metals, grows fast and produces large amount of above-ground biomass. Due to these characteristics, this species has been the target of several studies to evaluate its phytoremediation potential [ 10 ]. However, the presence of heavy metals, like cadmium, has been reported to reduce the amount of oil produced by these plants [ 11 ].

Brassica napus rapeseed is consumed as a vegetable but its main use is as a source of oil, being one of the largest sources of edible oil in the world [ 12 ].

The by-products from oil production are used in animal feed. Brassica oleracea varieties include very common vegetables used for human consumption, like cabbages, broccoli, cauliflower and Brussel sprouts among others. They are an important source of many nutrients, of compounds with antioxidative activity and of other bioactive compounds such as some glucosinolates that are recognized as beneficial for human health [ 13 , 14 ].

the mustard family

Brassica carinata is mainly cultivated in Ethiopia as an oil crop, although it has also received some attention as a source for biofuel production [ 15 ]. Both B. There is an increasingly large body of literature describing the effects of heavy metals in different Brassica species, confirming the relatively high tolerance that they have towards this abiotic stress, however the exact mechanism for this tolerance remains to be fully clarified [ 6 , 16 ]. In this review, we will evaluate the most recent discoveries in the accumulation and tolerance mechanisms of plants in the Brassica genus against heavy metal stress.

Today, large areas all over the world containing arable land are contaminated with heavy metals [ 17 , 18 ]. The pressure to increase crop production can lead to the use of marginal or contaminated soils with a potential danger of food contamination [ 19 ].

Some edible plants, include several from the Brassica genus under analysis in this review, are known to accumulate relatively large amounts of toxic metals. This has led to the search for plants that can adequately be used for phytoremediation, with the main following characteristics [ 20 ]: i ability to accumulate the heavy metals in the aboveground parts; ii tolerance to the high metal concentrations in soils; iii fast growth and high accumulating biomass; iv easy to grow as an agricultural crop and easily harvestable.

Phytoremediation: Halophytes as Promising Heavy Metal Hyperaccumulators

Most studies regarding the effect of heavy metals on Brassica species have focused on a few non-essentials elements mainly Cd and Pb and also on some essential elements like Cu and Zn. One of the problems regarding the applicability of plants for phytoremediation purposes is the difficulty in establishing representative experimental setups. Some studies are performed in hydroponic solution, others in soils spiked with heavy metals and other in naturally contaminated soils.

Most of the studies reported have been performed under controlled conditions usually in pots, and few in field conditions. The results obtained between all these different experimental conditions are very diverse and it is sometimes difficult to extrapolate the results from one experimental condition to another [ 21 , 22 ]. In Table S1 we present some representative results of heavy metal accumulation in different species under different experimental conditions, but only including contamination by single metals.

It is clear the range in concentration of metals in plants of the same species, but of different varieties or cultivars and grown in different experimental conditions. Some studies are performed in hydroponic solution, others in soil spiked with a fixed amount of metals while in others watering is performed with heavy metal contaminated solution. In soil experiments the amount of time between heavy metal spiking and seeding ranges between one week and several months, obviously causing differences in the metal uptake, besides all the large differences in soil characteristics.

Several works have been published comparing the performance of several Brassica species to toxic concentrations of heavy metals. Hernandez-Allica et al. Purakayastha et al. They concluded that B. In relation to Cu, B. Ebbs and Kochian [ 25 ] had previously in published a study comparing the toxicity and accumulation of Zn and Cu in three species from the genus Brassica B.

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The apparently different results obtained could be explained by differences in experimental conditions and also of different cultivars used. On the other hand, Gisbert et al.

They also observed that these Brassica species behaved as Zn and Pb excluders, able to maintain an almost constant level of these metals in the shoots, up to a certain level of toxicity. In yet another study comparing the phytoextraction behavior of B. In their study with B. Curiously Feigle et al. These results emphasize that the results observed are highly dependent on the experimental conditions used some of which are indicated in Table S1 , making harder to extrapolate any general conclusions.

Naturally the concentrations of the heavy metal under study and the duration of the effect are very important experimental parameters. Some authors perform the experiments in hydroponics because it is easier to control all other conditions, besides the variable under study.

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Even so, different hydroponic techniques, nutrient concentrations and pH can also affect plant development. The experiments in soil are usually more complex as the number of variables affecting heavy metal uptake also increase like soil type, pH, organic matter etc. Some authors use soil contaminated over years of anthropogenic activity while others spike the soil and perform the experiment after a few days or weeks of stabilization and this can have a large impact on the results obtained. Other parameters like the age of the plant at contamination are also critical to the effects usually measured.

Within the same species there is variability in the uptake capacity of different varieties, and even of different accessions [ 21 ]. Qadir et al.

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Although the general response to the evaluated parameters was similar, some cultivars presented higher Cd tolerance than others. Gill et al. Nouairi et al. Seth et al. Most of the studies about multielement toxicity, like the ones described above, assume a homogeneous distribution of the metals in soil. Podar et al.

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The results presented suggest that phytoremediation experiments in homogeneous conditions may underestimate the quantity of contaminants that can be taken up by plants. As some Brassica species are important in oil production, both for human consumption and for the production of biodiesel, the possible contamination of seed and oil from these plants has also been the objective of some studies, as it could lead to contamination of the food chain and of the environment. Park et al. They reported that the plants could grow and tolerate relatively high levels of a combination of different heavy metals and at the same time produce oil that was safe to be used as an energy source as the content in heavy metals was relatively low they reported that most of the remaining heavy metals were retained in the residues from the oil extraction process.

This could potentially make phytoremediation a more profitable process by linking it to economic valorization. Sankaran and Ebbs [ 36 ] devised an interesting experiment, evaluating the toxicity of Cd in B.

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They concluded that although the levels of Cd in seeds were dependent on the stage of plant development, they could easily accumulate in concentrations above acceptable limits for food crops, limiting its safe consumption. The increasing demand for water in agriculture has led to the study of alternatives including the use of treated waste waters TWW that can be rich in plant nutrients but have also the potential to contain different contaminants including heavy metals.

Some recent studies have been made regarding the use of TWW in crop species including some from the genus Brassica , showing the dangers of using contaminated waters in the irrigation of plants that can be used for human consumption [ 37 , 38 ]. Other heavy metals have received less attention as they are also of less concern regarding its presence in toxic concentration. For example, Hale et al. In order to enhance the availability of heavy metals to allow the effective use of phytoextraction processes, several chemical chelating agents have been proposed to increase the uptake of metals by plants and the translocation from roots to shoots but without affecting plant growth [ 40 ].

Several studies have been performed in Brassica species, with different chelating agents [ 18 ]. The addition of citric acid to the contaminated medium led to increased uptake and amelioration of B. This was attributed by the authors of the first study to the improvement of several metabolic processes through the mobilization of essential nutrients, although the exact mechanism for this is still unknown. In two publications Quartacci et al. According to their results, the plants were able to accumulate more Cd with the addition of NTA while for citric acid the differences in relation to the control were very small.

This EDTA-isomer had the added advantage of a rapid degradation in the soil, reducing the potential leaching into ground waters. While EDTA itself has also been reported to increase the uptake of heavy metals from contaminated soils by Brassica species [ 46 , 47 , 48 ], there are concerns regarding the environmental persistence of this chelating agent and its strong chelating capacity [ 49 ].

Clemente et al. They concluded that plant growth and metal uptake was highly dependent on soil pH, although the added amendments improved plant growth. They also calculated that between a minimum of years for Cu and a maximum of , years for Pb would be necessary for the effective clean-up using B. Similar results were obtained in the study of Brunetti et al. Other studies confirm that it would take hundreds or thousands of years for the complete clean-up of heavily contaminated sites [ 51 ].