Cadmium Concentration in Grains of Durum Wheat (Triticum

Two durum wheat near-isogenic lines (NILs) and 12 commercial varieties (cultivars Arcangelo, Aureo, Aziziah, Cappelli, Cirillo, Creso, Iride, Maestral...
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Cadmium Concentration in Grains of Durum Wheat (Triticum turgidum L. subsp. durum) Marzia Vergine, Alessio Aprile,* Erika Sabella, Alessandra Genga, Maria Siciliano, Patrizia Rampino, Marcello Salvatore Lenucci, Andrea Luvisi, and Luigi De Bellis Department of Biological and Environmental Sciences and Technologies, University of Salento, via Prov.le Monteroni 165, 73100 Lecce, Italy

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ABSTRACT: Heavy metal excess in soil represents a critical problem for crop productivity. Among these pollutants, cadmium (Cd) is one of the most dangerous in terms of food-chain contamination. Two durum wheat near-isogenic lines (NILs) and 12 commercial varieties (cultivars Arcangelo, Aureo, Aziziah, Cappelli, Cirillo, Creso, Iride, Maestrale, Parsifal, Russello, Strongfield, and Svevo) of durum wheat were exposed to a nontoxic level of Cd to evaluate its concentration in grains, roots, and shoots, as well as effects on biomass production. Cultivar Iride showed the most interesting behavior because it stored large amounts of Cd in the roots, preventing its translocation to grains. On the contrary, Cirillo and Svevo genotypes were characterized by a high Cd concentration in the grains. Furthermore, a molecular characterization employing the ScOPC20 marker associated with the Cd uptake locus has shown the absence of the expected fragment in the Iride variety and in other varieties characterized by low Cd concentration, as well as the presence of it in high Cd-accumulating cultivars. KEYWORDS: cadmium (Cd), food safety, heavy metals, genotypic variation, Triticum turgidum L. subsp. durum, cereals, soil pollution



0.2 mg of Cd kg−1 of grain, but higher Cd concentrations were found in grains of wheat crops grown worldwide.15−17 Cd is highly persistent, and, once absorbed by the organism, it remains for many years.18 In the human body, kidney represents the critical target organ,19 while the exposure to Cd can cause several diseases like osteoporosis, nonhypertrophic emphysema, irreversible renal tubular injury, anemia, eosinophilia, anosmia, and chronic rhinitis.20 Moreover, Cd can bind to DNA, causing strand breaks and chromosome aberrations, which might lead to cancer-related mutations.21 In particular, results of the case study reported by Julin et al.22 support the hypothesis that cadmium exposure has a potentially harmful role in the development of prostate cancer. Specifically, a cohort of 41 089 Swedish men aged 45−79 years was followed from 1998 to 2009 to assess the association between cadmium exposure (at baseline, 1998), the incidence of prostate cancer (3 085 cases, of which 894 were localized and 794 were advanced), and prostate cancer mortality (2008, 326 fatal cases). Therefore, it is necessary to decrease Cd presence in cereals employed for flour and food production,23 particularly in wheat, which is one of the most frequently consumed cereals. This goal could be reached by understanding the mechanisms that regulate Cd uptake in plants, its translocation to the leaves, and its accumulation in wheat grains. Large genetic variation for grain Cd concentration exists in durum wheat, but most of the commercial varieties have not been selected for a low-Cd trait. Research on genotypic

INTRODUCTION Heavy metals are major environmental pollutants. Their toxicity is an ecological, evolutionary, nutritional, and environmental problem of increasing significance that depends on several factors including the chemical species, their dose, and the status of exposed individuals.1,2 Soil contamination by heavy metals constitutes an environmental damage both on soil quality and for plant health and productivity; in fact, especially for crops of agricultural interest, plant diseases and decreased production might occur even below the toxicity threshold values. Furthermore, heavy metals are particularly dangerous for humans, because they could easily enter the food chain through plants and animals. Among all nonessential heavy metals, cadmium (Cd) is one of the most important in terms of food-chain contamination, because it is readily taken up by the cells of different plant species.3,4 Cd is a water-soluble chemical element. It enters the plasma membrane of root cells mostly through active transport systems5 following a mechanism similar to zinc transport.6 Cd has been shown to cause different biochemical changes in plants, such as mineral nutrients uptake, stomatal functioning,7 disturbances at the Calvin cycle enzymes and to the photosynthetic pigment, and carbohydrate metabolism.8,9 Cd accumulation can also cause growth inhibition, low seed germination,1,10 and significant alterations at histo-anatomical and ultrastructural level.11 Various plant species bioaccumulate heavy metals when grown on polluted soils;12 in particular, durum wheat (Triticum turgidum L. subsp. durum) accumulates more Cd than other cereals.13 Because Cd accumulation in durum wheat represents a risk for human health, the Codex Alimentarius Commission (CODEX STAN 193-1995 2009)14 has set a maximum level of © 2017 American Chemical Society

Received: Revised: Accepted: Published: 6240

April 27, 2017 June 28, 2017 July 7, 2017 July 7, 2017 DOI: 10.1021/acs.jafc.7b01946 J. Agric. Food Chem. 2017, 65, 6240−6246

Article

Journal of Agricultural and Food Chemistry

(ANC, ancient cultivars and populations); Arcangelo and Creso (INC, intermediate cultivars); Cirillo, Iride, Parsifal, and Svevo (MOC, modern cultivars); and Aureo, Maestrale, and Strongfield (RRC, recently released cultivars) (Table 1). The majority of the pedigree information was provided from Genetic Resources Information System for Wheat and Triticale (GRIS) (http://wheatpedigree.net; last update, Feb 24, 2017).28 Experimental Design. Seeds were surface-sterilized in 1.2% NaClO for 20 min, rinsed, and soaked for 24 h in an aerated solution of 1 mM CaCl2. Grains were germinated in plastic Petri dishes with moist filter paper, in the dark at 23 °C. After 3−4 days three germinated seeds were placed in plastic pots (7 × 7 × 45 cm) filled with perlite, moistened with deionized water, and transferred to the hydroponic system as described by Harris and Taylor.24 The nutrient solution was prepared in reverse osmosis (RO) water (