ORIGINAL ARTICLE PHYSIOLOGICAL AND AGROECOLOGICAL ASPECTS OF CADMIUM INTERACTIONS WITH BARLEY PLANTS: AN OVERVIEW ФИЗИОЛОГИЧНИ И АГРОЕКОЛОГИЧНИ АСПЕКТИ НА ВЗАИМОДЕЙСТВИЕТО НА КАДМИЯ С ЕЧЕМИЧНИТЕ РАСТЕНИЯ: ОБЗОР VASSILEV A. РЕЗЮМЕ Тази работа е обзор върху публикации и непубликувани резултати на автора, както и данни от достъпната литература върху реакцията на ечемика към замърсяване с Cd. Кратко са описани физиологичните основи на острата (акутна) Cd токсичност при ечемични растения. Приведени са и данни характеризиращи хроничната Cd токсичност при ечемика във връзка с възможното му използването за семепроизводство и Cd фитоекстракция на замърсени с тежкия метал почви. Представена е информация за основните физиологични фактори, лимитиращи растежа на третирани с Cd ечемични растения, както и за добива на зърно, качествата на семената и капацитета на ечемика за екстракция Cd при отглеждане върху замърсени с Cd почви. КЛЮЧОВИ ДУМИ: кадмий, ечемик, фитотоксичност, семепроизводство, фитоекстракция ABSTRACT This work is a review of author’s previous publications, unpublished results as well as available literature on barley responses to Cd contamination. The physiological backgrounds of the acute Cd toxicity in barley plants are briefly described. Some data characterizing the chronic Cd toxicity in barley have been also provided in relation to its possible use for seed production and Cd phytoextraction on Cd-contaminated agricultural soils. Information about the main physiological factors limiting growth of Cd-exposed barley plants and grain yield, seedling quality as well as Cd phytoextraction capacity of barley grown in Cd-contaminated soils is presented. KEY WORDS: cadmium, barley, phytotoxicity, seed production, phytoextraction Manuscript received: 16. December, 2002. Accepted for publication: 16. February, 2003. VASSILEV A. DETAILED ABSTRACT A part of agricultural soils all over the world is slightly to moderately contaminated by cadmium (Cd) creating risk for human and environmental health. Consequently, several strategies have been proposed for the management of Cd-contaminated agricultural soils. Some of them recommend cereals for seed production as a profitable option for heavy metal-contaminated soils as well as Cd phytoextraction as an environmentally friendly approach for soil remediation. Barley is a cereal crop attracting attention in both mentioned directions. Nevertheless, its successful use for those purposes needs better understanding of many questions related to its behavior under Cd contamination. To obtain this information complex research experiments have been conducted during the last decade at the Agricultural University of Plovdiv, Bulgaria. One part of experiments was focused on the main physiological disorders of Cd-exposed barley plants grown in hydroponics, sand and soil conditions. Another part of experiments aimed to study barley productivity and seedling characteristics has been conducted with plants grown in soils differing in Cd contamination and soil properties. The generalised information from these research efforts as well as available literature sources that could be of help to a wide spectrum of agricultural specialists is presented in this review. The main conclusions drawn from the conducted studies are the following: • The reductive analysis of factors limiting growth of Cd-exposed barley plants revealed photosynthesis retardation as one of the most important factors. Cd negatively affects barley photosynthesis directly at different structural-functional levels and indirectly by the metal induced disturbances in the other physiological processes. • The use of barley for seed production on Cd-contaminated agricultural soils seems a rationale option, as (1) barley seedling qualities are high; (2) its productivity is not significantly affected (except at some very high soil Cd contamination levels); (3) barley plants in the next generation, grown on non- contaminated soils have grain Cd levels within the norm and normal development and productivity. • Shoot Cd accumulation of barley plants is not high enough to meet the requirements for short-term phytoextraction perspective. If higher shoot Cd accumulation is achieved by means of the induced phytoextraction approach, barley Cd phytoextraction will be limited by phytotoxicity problems. 66 Journal of Central European Agriculture, Volume 4 (2002) No. 1 PHYSIOLOGICAL AND AGROECOLOGICAL ASPECTS OF CADMIUM INTERACTIONS WITH BARLEY PLANTS: AN OVERVIEW INTRODUCTION at Cd contamination. From the plant physiological point of view there are many questions that are still A part of agricultural soils all over the world are not fully understood. For example, how this element, slightly to moderately contaminated by cadmium that is non-essential for the plant metabolism and (Cd) due to extended use of superphosphate has a low redox potential, is able to participate in fertilisers, sewage sludge application as well as biological redox reactions is attracting now a smelters dust spreading [2, 8]. Due to high Cd significant research attention [11]. In more applied mobility in the soil-plant system it can easily enter aspects it is very important to describe the capacity into food chain and can create risk for human and of barely to resist and accumulate Cd in the grain, environmental health [15, 25]. Increasing effects of Cd on seed quality, etc. To obtain this international concern about the risks associated with information complex research experiments have long-term consumption of crops with Cd been conducted during the last decade at the concentrations has led the international food Agricultural University of Plovdiv, Bulgaria. One standards organisation, Codex Alimentarius part of experiments was focused on the main Commission, to propose a 0.1 mg Cd kg-1 limit for physiological disorders of Cd-exposed barley plants cereals, pulses and legumes [16]. Consequently, grown in hydroponics, sand and soil conditions. several strategies have been proposed for the Another part of experiments aimed to study barley successful management of the Cd-contaminated productivity and seedling characteristics has been agricultural soils. One approach, applicable on conducted with plants grown in soils differing in Cd slightly contaminated soils, is aiming to screen and contamination and soil properties. The generalised use low Cd-accumulating genotypes of crops, known information from these research efforts as well as to accumulate unacceptable high Cd levels in grain available literature sources that could be of help to a [3]. The second approach recommends profitable use wide spectrum of agricultural specialists is presented of non-food crops [49]. The third option is directed in this review. towards phytoextraction, representing use of plants for metal (including Cd) removal from contaminated soils [9, 23]. PHYSIOLOGICAL RESPONSES OF BARLEY PLANTS TO CD CONTAMINATION Besides non-food crops, there are some expectations that seed production of cereals could be another The studies on Cd interactions with plants have been possibility for rationale use of Cd-contaminated conducted during the last three decades but there soils. This idea is motivated by several facts and still remain some aspects unclear enough. Partly, it presumptions: (1) it is known that cereals are semi- is due to differences in the experimental designs resistant to Cd [19]; (2) it is well documented that used concerning the applied metal concentrations, Cd accumulation in above-ground organs of many kind of medium, age of plant exposure to metal crops decreases towards generative organs [1]; (3) a treatment, etc. Generally, each plant is able to presumption exists that when Cd-enriched seeds are withstand Cd loading into the plant tissue until the sown in non-contaminated soil, grain Cd content of metal reaches the toxic threshold level, suffering plants from the next generation will be bellow toxicity at higher levels. If it takes long enough to guideline values for combustion [17]. achieve this "critical" Cd concentration plant can respond to the treatment by different Cd detoxifying Cd phytoextraction from contaminated agricultural mechanisms. In this situation plants are able to resist soils has been proposed by Robinson et al. [23, 24] Cd to some extend and grow continuously at the pointing at the high mobility of this metal in soil- presence of Cd but with lower growth rate (chronic plant system and its relatively low contamination Cd phytotoxicity). In a case of exposure of plants to levels as compared, for example, with Pb and Zn. very strong Cd concentrations, they are not able to According to Ebbs and Kochian [13] barley is a express their protective mechanisms and as a result promising crop for Zn and Cd phytoextraction as it of this suffer Cd toxicity and generally die within could resist (to some extend) these metals as well as couple of weeks (acute Cd phytotoxicity). In our accumulate elevated concentrations in shoots. experimentation we studied the physiological The use of barley for both above-mentioned backgrounds of both chronic and acute Cd toxicity directions needs better understanding of its behavior in barley plants. Journal of Central European Agriculture, Volume 4 (2002) No. 1 67 VASSILEV A. ACUTE CD PHYTOTOXICITY that might have impact on barley physiology. For example, the levels of K, Cu and Zn in barley plants The studies on the acute Cd toxicity in barley were significantly diminished [33]. A tendency seedlings and young plants have been realized in towards acceleration of R of roots and leaves was both hydroponics and sand culture experiments. In D observed [34], which according to Ernst [14] could the hydroponics experiments the Bulgarian cultivars be explained as a compensatory mechanism Obzor and Hemus were used. The applied Cd supplying ATP through oxidative phosphorylation. concentrations varied between 9 and 54 µmol/L, given at 3-day-old seedlings and maintained for 12 The negative effects of Cd on photosynthesis were days [32]. The Portuguese cultivars Ribeka and CE also studied. Generally, Cd inhibited P ; in the N 9704 were used in the sand experiments, where Cd highest treatments P averaged 80-85% of control N concentrations varied from 14 to 56 mg kg-1 sand, values [36]. The established negative Cd effect was given at 20-day-old plants for 10 days [46, 47]. At mainly due to mesophyll constrains. In barley plants the highest Cd treatments in both experimental at 54 µmol Cd/L destructive changes were observed designs the acute Cd phytotoxicity was well in chloroplast ultrastructure, namely reduction in the expressed. The visual phytotoxicity symptoms number of grana and their disorganisation, swelling observed were chlorosis and necrosis of leaf tips as of thylakoids, thinning and partial tearing of the well as necrosis and reduction of site root formation chloroplast envelope, etc. [36]. Cd decreased in the root system, all having nonspecific nature. photosynthetic pigments content too, on average by The basic physiological disorders connected with the 20% at 54 µmol/L. All mentioned disturbances acute Cd toxicity in barley plants are described leaded to decreased photosynthetic functioning, below and listed in Table 1. shown also by weaker incorporation of 14C in the early photoproducts [40]. Furthermore, Cd changed the pattern of 14C partitioning towards that Hydroponics studies characteristic for aging leaves. The fluorescence It was established that Cd concentrations above 4.5 analysis showed down regulation of PSII as the light µM Cd/L inhibited dry mass accumulation in barley dependence of the maximum apparent electron plants [35]. In general, Cd accumulation and transport rate of these plants were reached under distribution in barley plants followed a similar lower light intensities and earlier than in control pattern to that reported for other gramineae species plants [44]. Additionally, we established that [20, 21]. The observed root Cd accumulations were susceptibility of the photosynthetic apparatus of Cd- several fold higher than in the leaves. For example, exposed plants to other stresses (low and high Cd concentrations in the roots and the leaves of temperature stresses) was higher than that of plants from cv. Obzor reached at 54 µmol Cd/L 289 controls [35, 39]. and 94 mg kg-1, respectively [32]. Although to a lesser extend, the RGR inhibition of DM The relative growth rate (RGR ) of Cd-exposed Cd-exposed barley plants was also related to DM barley plants (cv. Obzor) was retarded due mainly to changes of LAR, mainly due to decreased in specific net assimilation rate (NAR) inhibition, while leaf leaf area (SLA), indicating that Cd induced water area ratio (LAR) was less influenced [43]. Plants relation problems. In fact, we established lower from cv. Hemus grown at 54 µmol/L Cd treatment values of leaf water potential (Ψ ) and transpiration w showed 85% inhibition of RGRDM and accumulated rate (E) as well as an increase in leaf proline content about 188 mg Cd kg-1 DW in their leaves [41]. of Cd-exposed plants [43]. NAR depends on photosynthetic rate (PN), cell respiration (RD) and the relative ratio of non- Sand culture studies photosynthesising plant organs, mainly root mass The exposure of barley plants to Cd in the sand ratio (RMR) in young plants. RMR in Cd-exposed experiments has been done on 20-day-old plants barley plants decreased due to greater Cd having well developed root system and accumulation and subsequently stronger toxicity as photosynthetic apparatus and thus, being able to compared with leaves [32]. The inhibition of root withstand better the influence of the metal. growth and functioning provoked changes in plant Consequently, all observed physiological disorders cytokinins levels that could further affect the growth rate (4). It also induced some mineral imbalances 68 Journal of Central European Agriculture, Volume 4 (2002) No. 1 PHYSIOLOGICAL AND AGROECOLOGICAL ASPECTS OF CADMIUM INTERACTIONS WITH BARLEY PLANTS: AN OVERVIEW were similar, but weaker expressed as compared fatty acids content in the thylakoids of Cd-exposed with the plants grown at hydroponics conditions. plants [Vassilev and Lidon, unpublished data]. RGRDM of plants from cv. CE 9704 was significantly lower as compared to control plants, CHRONIC CD PHYTOTOXICITY being retarded at 42 mg Cd kg-1 sand by 41% and The data on barley responses to Cd is mainly based having leaf Cd concentration of 128 mg kg-1 DW on hydroponics experiments and more often [47]. However, well-expressed cultivar differences represents an acute phytotoxicity [10, 7, 29]. in growth responses and Cd accumulation have been Behaviour of barley on Cd-contaminated soils is also detected. For example, plants from cv. Ribeka rarely investigated. There is some information about grown at the same treatments as cv. CE 9704 metal uptake and productivity of barley grown on accumulated less Cd and their growth rate was less industrially polluted soil, but it is relevant just to affected [48]. mixed metal contamination [12]. In our As in the hydroponics experiments it was observed experimentation the study on the chronic Cd toxicity that Cd treatment induced plant mineral imbalances. in barley plants has been realized in pot-soil The concentrations of K, Zn, Ca and Fe in both roots experiments where plants were grown continuously and leaves of plants from cv. Ribeka and cv. CE on Cd-contaminated soil. The Cd contamination was 9704 decreased at high Cd treatments probably due set up from 0.6 mg kg-1 soil (noncontaminated to break down of mineral regulatory functions [46, control soil) to 45 mg kg-1 soil (artificially spiked by 47]. The most pronounced effect of Cd was cadmium sulphate), being up to 23-fold the limit established on PN and photosynthetic capacity value of Cd in Bulgarian soils - 2 mg kg-1 soil [17]. (photosynthetic rate at non-limiting conditions), The experiments have been done with two soils, which were significantly retarded. In the highest differing mainly in soil texture (clay loam and sandy treatments - 42 mg Cd kg-1 - PN averaged 50% of loam) and two cultivars - Obzor and Hemus [31, 38]. control values in both cultivars CE 9704 and Ribeka The observed physiological disorders of barley [47, 48]. There was some evidence for stomatal plants related to the chronic Cd phytotoxicity are limitation in Cd-exposed plants because PN was shortly described below and shown in Table 1. stronger inhibited as compared to photosynthetic Plants grown at up to 45 mg kg-1 clay loam soil did capacity, and stomatal conductance (gs) and not exhibit any visual symptoms of toxicity in intercellular CO2 concentration (ci) were strongly above-ground parts, but some browning of roots was reduced. Besides the already mentioned observed [42] whereas plants grown in sandy loam disturbances, Cd-exposed plants showed mesophyll soil at 25 mg Cd kg-1 suffered toxicity showing limitations as was shown by the lower efficiency of necrosis of leaf tips [31]. light utilisation (φe) and electron transport rates involving PSII and PSI (Vassilev and Lidon, The most obvious effect of Cd at 45 mg kg-1 clay unpublished data). After 10 days exposure of the soil was found on the development of barley plants. plants from cv. Ribeka to 28 mg Cd kg-1, the It was retarded at tillering up to 10 days, but this decrease in PSII activity with OEC represented effect became weaker during ontogenesis and at full about 40% and without OEC 19%, whereas in PSI maturity the development was partly compensated activity decreased ca. 30%. The similar inhibition of by shortening the duration of the following phases. PSII activities with or without OEC at 42 mg Cd kg- The slower development could be partly attributed to 1 treatment showed that Cd could interact with both later emergence of these plants, probably due to the the donor and the acceptor side of this photosystem. negative effects of Cd on mobilisation of food The lower photosynthetic electron transport in Cd- reserves in the seeds as reported by Bishnoi et al. [5] exposed plants from this cultivar was probably not for pea seeds. Dry mass accumulation of plants was due to Cd-induced lipid peroxidation at thylakoid diminished by 32-35% at tillering to 10-13% at full level as the ethylene production associated with maturity compared to the values of control plants thylakoids was close to that in the control plants. On [42]. The relatively weaker effect of Cd at latter the contrary, the stronger inhibition of the phases probably was due to an expression of photosynthetic electron transport in the more efficient adaptation mechanisms leading to Cd sensitive to Cd cultivar CE9704 was linked with binding in cell walls, complexation with increased ethylene production and diminished total Journal of Central European Agriculture, Volume 4 (2002) No. 1 69 VASSILEV A. phytochelatins, compartmentalisation in vacuoles, et al. [28] stated Cd as strong inhibitor of etc. [27]. chlorophyll biosynthesis in incubated barley leaf segments, obviously, when barley is grown from Plants grown at 45 mg Cd kg-1 clay loam soil at seed to seed on Cd-contaminated soil the situation is early stages of the development had decreased different. Probably, the observed slight negative photosynthetic rate (P ) by 10 - 25% [42]. This N effect on P at the early developmental stages was negative effect varied in different leaves, being the N due to Cd-induced disorders at other sites of the strongest in the upper leaves, which have higher process – enzymes activities, electron transport, etc. functional activity [45]. The retarded P could be N as well as other physiological processes having related to disorders in many sites of this integral impact on the functioning of photosynthesis. On the process. It clearly was not due to stomatal limitation, other hand, the results obtained showed that whole since transpiration rate was not significantly barley plants were able to acclimatise to high Cd changed. Malik et al. [22] concluded the same for concentrations in the soil. This in turn has lead to a Cd-exposed wheat seedlings grown on sand culture. good performance of barley photosynthetic Cd-induced diminishing in P was neither linked to N machinery on soils with increased Cd content. decreased chlorophyll content. Despite that Stobart Table 1: Physiological disorders of Cd-exposed barley plants Parameter Physiological disorders in barley plants Disorders observed at Cd-exposed plants having 40 - 80% inhibition of RGR DW Leaf water potential ↓ A depression due to a complex of negative effects of Cd on water relations Changes in the free cytokinins levels that might reflect on the export of the Root cytokinins hormone to the shoots ↓ An inhibition due to both indirect effects on leaf water content and direct effect Transpiration rate on stomata functioning Mineral status Imbalances in some essential nutrients (K, Zn, Ca, Fe ) ↑↓ An initial increase (stress response) followed by decrease in a result of enzymes Cell respiration rate inhibition Disturbed envelope, thylakoid swelling, reduction in the number of grana and Chloroplast ultrastructure thylakoids therein, etc. Net photosynthetic rate ↓ An inhibition due to both stomata and mesophyll limitations 14C incorporation pattern Pattern similar to that in aging leaves ↓ A decrease, probably due to biosynthesis inhibition as well as enzymatic Photosynthetic pigments content degradation Potential activity of PSII ↓ A slight inhibition Quantum yield ↓ An inhibition, well expressed at light saturation level Disorders observed at barley plants suffering chronic Cd toxicity Plant development ↓ A retardation at earlier stages, partly due to later emergence Dry mass accumulation ↓ A decrease expressed better at earlier plant stages Net photosynthetic rate ↓ A slight inhibition at earlier plant stages, no effect later Transpiration rate ↓ No significant changes Leaf respiration ↑ An increase, probably due to stress response 70 Journal of Central European Agriculture, Volume 4 (2002) No. 1 PHYSIOLOGICAL AND AGROECOLOGICAL ASPECTS OF CADMIUM INTERACTIONS WITH BARLEY PLANTS: AN OVERVIEW PRODUCTIVITY, SEEDLING 1000-seed weight was slightly higher than in control CHARACTERISTICS AND CD plants due to an expression of compensation PHYTOEXTRACTION CAPACITY OF mechanisms based on sink-source interaction change BARLEY GROWN IN CD-CONTAMINATED [31]. SOILS The background levels of Cd in cereal grains range Seed production of barley on Cd-contaminated soil from 0.013 to 0.22 mg Cd kg-1 (DW). The highest could be successful if this heavy metal does not Cd grain concentration has been reported for wheat remarkably reduce its productivity and seedling (14.2 mg Cd kg-1), but generally even in characteristics. We found that grain productivity of contaminated areas it is much lower [18]. In our barley significantly decreased only at concentrations studies Cd accumulation in grain exceeded the of 25 and 45 mg Cd kg-1 soil, which are far over the international food standard 0.1 mg Cd kg-1 DW [16] typical Cd contamination of agricultural soils [31, if plants were grown at 5 mg Cd kg-1 soil, thus, the 38]. The decrease in grain productivity of cvs. grain produced may not be used as a foodstuff [31]. Hemus and Obzor averaged 12 to 18% in Cd- The observed mean Cd values in the straw varied contaminated clay loam soil, whereas in sandy loam between 2 and 15 mg kg-1 DW when barley was soil it was higher. The regression equations grown at 5 to 45 mg Cd kg-1 soil, respectively [31]. describing dependence of grain yield of barley on The value of Cd in the straw is not standardised and soil Cd concentrations are shown in Table 2. there is no generally shared opinion about its harmless amount in feeds. However, in view of The yield formation in cereals involves processes of variable and secondary effects of Cd in the food reduction and compensation in the major yield chain, it is desirable to minimize its concentrations structural elements during ontogenesis. We found in crops [18]. On the contrary, for phytoextraction that Cd at 25 mg kg-1 and higher significantly purpose Cd concentration in the straw should be decreased all yield structural elements. The maximised, as after the harvest and post harvest inhibiting effect of the metal was first apparent treatments it may be disposed as a hazardous waste through a decreased total tillering. During [6]. The regression equations representing the ontogenesis plants were characterised by weaker dependence of shoot and grain Cd concentrations on growth, the formation of less productive tillers with soil Cd concentrations and soil properties are given lower number of grains per ear and a lower 1000- in Table 2. seed weight [38]. On sandy loam soil, where the negative effect of Cd at tillering was stronger, the Table 2: Dependence of grain yield, leaf and grain Cd concentrations of barley (cv. Obzor) on soil Cd concentrations (X) and soil properties Parameter (Y) Soil properties Regression equation R2 sandy loam soil Y = -0.15X+15.44 0.77 Grain yield (g / pot) clay loam soil Y = -0.06X+12.71 0.84 Leaf Cd sandy loam soil Y = 0.35X+1.19 0.78 concentration(mg / kg clay loam soil Y = 0.22X+1.07 0.69 DW) Grain Cd sandy loam soil Y = 0.04X+0.21 0.77 concentration(mg / kg clay loam soil Y = 0.03X+0.33 0.71 DW) Soil Cd contamination of up to 45 mg kg-1 had no these seeds were within the norm [30, 38]. Barley effect on the seedling characteristics of barley seeds. plants originating from Cd-enriched seeds (up to 2 Germination energy, germination rate and ability of mg Cd kg-1 grain) sown in non-polluted soil grew Journal of Central European Agriculture, Volume 4 (2002) No. 1 71 VASSILEV A. CONCLUSIONS well without any abnormalities. We did not observe Summing up, our studies showed that: any negative effects on growth, development and productivity of barley in the next generation and, on • The reductive analysis of factors limiting the other hand, Cd concentrations in grain were growth of Cd-exposed barley plants revealed below 0.1 mg kg-1 [37]. However, if the photosynthesis retardation as one of the most contaminated soil had sandy loam texture and Cd important factors. Cd negatively affects barley concentration exceeds 20-25 mg kg-1, a significant photosynthesis directly at different structure- decrease (more than 10% of seed productivity) functional levels and indirectly by the metal should be expected. induced disturbances in the other physiological processes. The maximum Cd concentration in the aerial parts of barley was about 22 – 25 mg kg-1 DW, found in the • The use of barley for seed production on Cd- lower leaves of plants grown on soil containing 45 contaminated agricultural soils seems a mg kg-1 soil [42]. We calculated that even in pot rationale option, as (1) barley seedling qualities conditions, which are well known to increase metal are high; (2) its productivity is not significantly transfer from soil to plants, the maximum Cd affected (except at some very high soil Cd phytoextraction with barley would be estimated to contamination levels); (3) barley plants in the not more than 100 g ha-1 yr-1 [45]. This value is 10 to next generation, grown on non-contaminated 20 times lower than values reported for other crops soils have grain Cd levels within the norm and proposed for Cd removal, for example willow and normal development and productivity. pannycress [24, 26]. It will take more than 100 • Shoot Cd accumulation of barley plants is not consecutive croppings to decrease soil Cd high enough to meet the requirements for short- concentration from 5 to 2 mg kg-1 soil by barley term phytoextraction perspective. If higher phytoextraction. Therefore, without additional shoot Cd accumulation is achieved by means of enhancing of Cd uptake this option seems unrealistic the induced phytoextraction approach, barley for practical implementation. Cd phytoextraction will be limited by phytotoxicity problems. REFERENCES [5] BISHNOI, N. R., I. S. SHEORAN, R. SINGH, 1993. Effect of cadmium and nickel on [1] ADRIANO, D., 2001. Cadmium. In: Trace mobilisation of food reserves and activities of elements in terrestrial environments: hydrolytic enzymes in germinating pigeon pea biogeochemistry, bioavailability, and risks of seeds. J. Environ. Qual., 5 (1), 57-59. metals. 2nd edition. Springer-Verlag New York Berlin Heidelberg, 264-314. [6] BLAYLOCK, M., J. HUANG, 2000. Phytoextraction of metals. In: I. Raskin, B. [2] ANGELOVA, I., I. ATANASSOV, 1993. Ensley (Editors), Phytoremediation of toxic Deposition of Pb, Zn, Cd and Cu in the soil of metals: Using plants to clean up the the smelter’s area near Plovdiv. Sci. Works environment. John Wiley &Sons, Inc., 53-69. Higher Inst. Agri., 38 (2), 99-102 (BG). [7] BOUSSAMA, N., O. OUARITI, M. H. [3] ARCHAMBAULT, D., E. MARENTES, W. GHORBAL, 1999. Changes in growth and BUCKLEY, J. CLARKE, G. TAYLOR, 2001. nitrogen assimilation in barley seedlings under A rapid, seedling–based bioassay for cadmium stress. J. Plant Nutr., 22, 731-752. identifying low cadmium-accumulating individuals of durum wheat (Triticum turgidum [8] CHANEY, R. L., 1980. Health risks associated L.), Euphytica, 117, 175-182. with toxic metals in municipal sludge. In: G. Bitton, B. Damron, G. Edds, M. Davidson [4] ATANASOVA, L., A. VASSILEV, M. (Editors), Sludge – Health Risks of Land PISARSKA, I. YORDANOV, 1999. Cd- Application. 59-83. induced changes of root cytokinins from two barley cultivars. Compt. Rend. Acad. Bulg. Sci., [9] CHANEY, R. L., 1983. Plant uptake of 53 (6), 91-94. inorganic waste. In: J. E. Parr, P. B. Marsh, J. 72 Journal of Central European Agriculture, Volume 4 (2002) No. 1 PHYSIOLOGICAL AND AGROECOLOGICAL ASPECTS OF CADMIUM INTERACTIONS WITH BARLEY PLANTS: AN OVERVIEW M. Kla (Editors), Land Treatment of Hazardous related enzymes in young maize plants (Zea Waste. 50-76. Noyes Data Corp. Park Ridge, mays L.). Plant Soil, 200, 241-250. IL. [21] LANDBERG, T., M. GREGER, 1994. [10] CHEN, Y, A. HUERTA, 1997. Effects of sulfur Influence of selenium on uptake and toxicity of nutrition on photosynthesis in Cd-treated barley copper and cadmium in pea (Pisum sativum) seedlings. J. Plant Nutr., 20, 845-855. and wheat (Triticum aestivum). Physiol. Plant. 90, 637-644. [11] CLIJSTERS, H., A. CUYPERS, J. VANGRONSVELD, 1999. Physiological [22] MALIK, D., I. SHEORAN, R. SINGH, 1992. responses to heavy metals in higher plants; Carbon metabolism in leaves of cadmium defence against oxidative stress. Z. treated wheat seedlings. Plant Physiol. Naturforsch., 54c, 730-734. Biochem. 30, 223-229. [12] DUDKA, S., M. PIOTROWSKA, H. [23] ROBINSON, B. H., M. LEBLANC, D. PETIT, TERELAK, 1996. Transfer of cadmium, lead, R. R. BROOKS, J. H. KIRKMAN, P. E. H. and zinc from industrially contaminated soil to GREGG, 1998. The potential of Thlaspi crop plants: a field study. Environ. Pollut., 94 carelessness for phytoremediation of (2), 181-188. contaminated soils. Plant Soils, 203, 47-56. [13] EBBS, S. D., L. V. KOCHIAN, 1998. [24] ROBINSON, B., T. MILLS, D. PETIT, L. Phytoextraction of zinc by oat (Avena sativa), FUNG, S. GREEN, B. CLOTHIER, 2000. barley (Hordeum vulgare), and Indian mustard Natural and induced cadmium-accumulation in (Brassica juncea). Environ. Sci. Technol. 32, poplar and willow: Implications for 802-806. phytoremediation. Plant Soil, 227, 301-306. [14] ERNST, W., 1980. Biochemical aspects of [25] RYAN, J., H. PAHREN, J. LUCAS, 1982. cadmium in plants. In: Cadmium in the Controlling cadmium in the human food chain. Environment. Ed. J. Nriagu, Wiley and Sons, A review and rationale based on health effects. New York, 639-653. Environmental Research, 27, 251-302. [15] GRANT, C., W. BUCKLEY, L. BAILEY, F. [26] SAXENA, P., S. KRISHNARAJ, T. DAN, M. SELLES, 1998. Cadmium accumulation in PERRAS, N. VETTAKKORUMAKANKAV, crops. Can. J. Plant Science, 78, 1-17. 1999. Phytoremediation of heavy metals contaminated and polluted soils. In: M. N. V. [16] HARRIS, N., G. J. TAYLOR, 2001. Prasad, J. Hagemaer (Editors), Heavy metal Remobilization of cadmium in maturing shoots stress in plants: from molecules to ecosystems. of near isogenic lines of durum wheat that 305-329. Springer-Verlag: Berlin Heidelberg. differ in grain cadmium accumulation. J. Exp. Bot., 52 (360), 1473-1481. [27] SEREGIN, I. V., V. B. IVANOV, 2001. Physiological aspects of cadmium and lead [17] INSTRUCTION RD-00-11/13.07.1994 of toxic effects on higher plants. Russ. J. Plant Bulgarian Ministry of Agriculture Physiol., 48, 523-544. [18] KABATA-PENDIAS, A., H. PENDIAS, 2000. [28] STOBART, A., W. GRIFFITHS, I. AMEEN- Trace Elements in Soils and Plants. In: BUKHARI, R. SHERWOOD, 1985. The effect Elements of Group II. CRC Press: London, of Cd2+ on the biosynthesis of chlorophyll in 131-141 leaves of barley. Physiol. Plant., 63, 293-298. [19] KUBOI, T., A. NOGUCHI, A. J. YAZAKI, [29] TALANOVA, V.V., A. F. TITOV, N. P. 1986. Family-dependent cadmium BOEVA 2001. Effect of increasing accumulation characteristics in higher plants. concentrations of heavy metals on the growth Plant Soil 92, 405-415. of barley and wheat seedlings. Russ. J. Plant [20] LAGRIFFOUL, A., B. MOCQUOT, M. Physiol. 48, 100-103. MENCH, J. VANGRONSVELD, 1998. [30] VASSILEV, A., 1993. Influence of Cd on Cadmium toxicity effects on growth, mineral productivity and seedling qualities of barley and chlorophyll contents, and activities of stress Journal of Central European Agriculture, Volume 4 (2002) No. 1 73 VASSILEV A. grown in two different soils. II. Sci. Works [40] VASSILEV, A., I. YORDANOV, T. TSONEV, Higher Inst. Agri., 38, 145-148 (BG). 1997a. Effect of Cd2+ on the physiological state and photosynthetic activity of young barley [31] VASSILEV, A., V. KERIN, G. BEKYAROV, plants. Photosynthetica 34, 293-302. 1993a. Influence of Cd on productivity and seedling qualities of barley grown in two [41] VASSILEV, A., I. YORDANOV, 1997b. different soils. I. Sci. Works Higher Inst. Agri., Reductive analysis of factors limiting growth of 38, 149-152 (BG). Cd-exposed plants: a review. Bulg. J. Plant Physiol. 23, 114-133. [32] VASSILEV, A., V. KERIN, I. YORDANOV, 1993b. The effect of Cd2+ stress on the growth [42] VASSILEV, A., T. TSONEV, I. YORDANOV, and photosynthesis of young barley plants (H. 1998a. Physiological response of barley plants vulgare L.). I. Growth. Bulg. J. Plant Physiol. (Hordeum vulgare) to cadmium contamination 19, 22-29. in soil during ontogenesis. Environ. Pollut. 103, 287-293. [33] VASSILEV, A., M. BEROVA, Z. ZLATEV, V. KERIN, 1994b. Influence of Cd stress on [43] VASSILEV, A., M. BEROVA, Z. ZLATEV, uptake and content of some mineral elements in 1998b. Influence of Cd2+ on growth, barley plants. Sci. Works Higher Inst. Agri., 34, chlorophyll content, and water relations in 285-293 (BG). young barley plants. Biologia Plantarum, 41 (4), 601-606. [34] VASSILEV, A., Z. ZLATEV, V. KERIN, 1994a. Physiological responses of two barley [44] VASSILEV, A., P. MANOLOV, 1999. cultivars to toxic Cd treatments. Sci. Works Chlorophyll fluorescence of barley (H. vulgare Higher Inst. Agri., 34, 295-301 (BG). L.) seedlings grown in excess of Cd. Bulg. J. Plant Physiol. 25, 67-76. [35] VASSILEV, A., V. KERIN, K. GEORGIEVA, 1995a. Cultivar sensitivity and cold resistance [45] VASSILEV, A., P. ZAPRYANOVA, 1999. of Cd-treated barley plants. Proceedings of Removal of Cd by winter barley (H. vulgare L.) Jubilee conference on an occasion of 60 years grown in soils with Cd pollution. Bulg. J. Agri. of the establishment of the Institute of seeds Science, 5: 131-136. and breeding “Obraztsov chiflik” – Russe, Vol. [46] VASSILEV, A., 2001. A comparative study on 2, 163-167 (BG). growth and mineral status of barley plants [36] VASSILEV, A., I. YORDANOV, E. grown at presence of Cd and Cu. Changes in CHAKALOVA, V. KERIN, 1995b. Effect of the mineral status. Achievements and prospects cadmium stress on growth and photosynthesis of plant physiology and biochemistry of of young barley (H. vulgare L.) plants. II. mineral nutrition and water relations in Structural and functional changes in Bulgaria, Ed. G. Ignatov, Vol. 2, 165-167. photosynthetic apparatus. Bulg. J. Plant [47] VASSILEV, A., F. C., LIDON, M. DO CÉU Physiol. 21, 21-21. MATOS, J. C. RAMALHO, I. YORDANOV, [37] VASSILEV, A., Z. ZLATEV, V. KERIN, 2002. Photosynthetic performance and some 1995c. Effect of Cd-enriched barley seeds on nutrients content in cadmium and copper- yield and quality of barley. Sci. Works Higher treated barley plants. J. Plant Nutrition 25 (11), Inst. Agri., XL (2), 241-244 (BG). 2343-2360. [38] VASSILEV, A., V. KERIN, P. ATANASSOV, [48] VASSILEV, A., F. C., LIDON, J. C. 1996a. Effect of cadmium pollution of soil RAMALHO, M. DO CÉU MATOS, M. DA upon productivity and seedling qualities of two GRACA, 2002. Shoot cadmium accumulation barley (H. vulgare L.) cultivars. Bulg. J. Agri. and photosynthesis performance of barley Science, 2: 333-340. plants at high cadmium treatments. J. Plant Nutrition (submitted) [39] VASSILEV, A., K. GEORGIEVA, I. YORDANOV, 1996b. Influence of Cd-stress [49] ZHELJAZKOV, V. N. NIELSEN, 1996. Effect on the thermosensitivity of chlorophyll of heavy metals on peppermint and cornmint. fluorescence parameters in two barley cultivars. Plant Soil, 178, 59-66. Compt. Rend. Acad. Bulg. Sci., 49, 2, 85-88. 74 Journal of Central European Agriculture, Volume 4 (2002) No. 1