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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 J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.7b01946 • Publication Date (Web): 07 Jul 2017 Downloaded from http://pubs.acs.org on July 9, 2017
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Journal of Agricultural and Food Chemistry
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TITLE:
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Cadmium concentration in grains of durum wheat (Triticum turgidum
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L. subsp. durum)
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AUTHORSHIP:
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Marzia Vergine, Department of Biological and Environmental Sciences and Technologies,
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University of Salento, via Prov.le Monteroni 165, 73100 Lecce, Italy
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Alessio Aprile*, corresponding author- Department of Biological and Environmental Sciences
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and Technologies, University of Salento, via Prov.le Monteroni 165, 73100 Lecce, Italy.
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Telephone number: +39 0832298609 e-mail address:
[email protected] 11
Erika Sabella, Department of Biological and Environmental Sciences and Technologies,
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University of Salento, via Prov.le Monteroni 165, 73100 Lecce, Italy.
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Alessandra Genga, Department of Biological and Environmental Sciences and Technologies,
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University of Salento, via Prov.le Monteroni 165, 73100 Lecce, Italy.
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Maria Siciliano, Department of Biological and Environmental Sciences and Technologies,
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University of Salento, via Prov.le Monteroni 165, 73100 Lecce, Italy.
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Patrizia Rampino, Department of Biological and Environmental Sciences and Technologies,
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University of Salento, via Prov.le Monteroni 165, 73100 Lecce, Italy.
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Marcello Salvatore Lenucci, Department of Biological and Environmental Sciences and
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Technologies, University of Salento, via Prov.le Monteroni 165, 73100 Lecce, Italy.
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Andrea Luvisi, Department of Biological and Environmental Sciences and Technologies,
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University of Salento, via Prov.le Monteroni 165, 73100 Lecce, Italy.
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Luigi De Bellis, Department of Biological and Environmental Sciences and Technologies,
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University of Salento, via Prov.le Monteroni 165, 73100 Lecce, Italy.
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Abstract
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Heavy metal excess in soil represents a critical problem for crop productivity. Among these
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pollutants, cadmium (Cd) is one of the most dangerous in terms of food-chain contamination.
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Two durum wheat near-isogenic lines (NILs) and twelve commercial varieties (cultivars Arcangelo,
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Aureo, Aziziah, Cappelli, Cirillo, Creso, Iride, Maestrale, Parsifal, Russello, Strongfield, Svevo) of
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durum wheat were exposed to a non-toxic level of Cd to evaluate its concentration in grains, roots
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and shoots, as well as effects on biomass production.
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Cultivar Iride showed the most interesting behavior because it stored large amounts of Cd in the
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roots preventing its translocation to grains. On the contrary, Cirillo and Svevo genotypes were
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characterized by a high Cd concentration in the grains.
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Furthermore, a molecular characterization employing the ScOPC20 marker associated with the Cd
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uptake locus has shown the absence of the expected fragment in the Iride variety and in other
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varieties characterized by low Cd concentration, and the presence of it in high Cd-accumulating
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cultivars.
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Keywords
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Cadmium (Cd), food safety, heavy metals, genotypic variation, Triticum turgidum L. subsp. durum, cereals,
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soil pollution.
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Introduction
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Heavy metals are major environmental pollutants. Their toxicity is an ecological, evolutionary,
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nutritional and environmental problem of increasing significance that depends on several factors
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including the chemical species, their dose, and status of exposed individuals1,2. Soil contamination
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by heavy metals constitutes an environmental damage both on soil quality and for plant health and
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productivity; in fact, especially for crops of agricultural interest, plant diseases and decreased
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production might occur even below the toxicity threshold values. Furthermore, heavy metals are
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particularly dangerous for humans, since they could easily enter the food chain through plants and
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animals. Among all non-essential heavy metals, cadmium (Cd) is one of the most important in
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terms of food-chain contamination, because it is readily taken up by the cells of different plant
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species3,4. Cd is a water soluble chemical element. It enters the plasma membrane of root cells
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mostly through active transport systems5 following a mechanism similar to zinc transport6.
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Cd
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mineral nutrients uptake, stomatal functioning7, disturbs at the Calvin cycle enzymes and to the
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photosynthetic pigment and carbohydrate metabolism8,9. Cd accumulation can also cause growth
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inhibition, low seed germination1,10 and significant alterations at histo-anatomical and
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ultrastructural level11.
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Various plant species bioaccumulate heavy metals when grown on polluted soils12; in particular,
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durum wheat (Triticum turgidum L. subsp. durum) accumulates more Cd than other cereals13.
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Since Cd accumulation in durum wheat represents a risk for human health, the Codex Alimentarius
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Commission (CODEX STAN 193-1995 2009)14 has set a maximum level of 0.2 mg Cd kg-1 of
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grain, but higher Cd concentrations were found in grains of wheat crops grown worldwide15,16,17.
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Cd is highly persistent and, once absorbed by the organism, it remains for many years18. In the
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human body, kidney represents the critical target organ19, while the exposure to Cd can cause
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several diseases like osteoporosis, non-hypertrophic emphysema, irreversible renal tubular injury,
has
been
shown
to
cause
different
biochemical
changes
in
plants,
such
as
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anemia, eosinophilia, anosmia and chronic rhinitis20. Moreover, Cd can bind to DNA causing strand
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breaks and chromosome aberrations, which might lead to cancer-related mutations21. In particular,
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results of the case study reported by Julin et al.22 support the hypothesis that cadmium exposure has
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a potentially harmful role in the development of prostate cancer. Specifically, a cohort of 41089
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Swedish men aged 45-79 years was followed from 1998 to 2009 to assess the association between
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cadmium exposure, (at baseline, 1998), the incidence of prostate cancer (3085 cases of which 894
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were localized and 794 advanced) and prostate cancer mortality (2008, 326 fatal cases).
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Therefore, it is necessary to decrease Cd presence in cereals employed for flour and food production23,
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particularly in wheat, that is one of the most frequently consumed cereals. This goal could be reached by
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understanding the mechanisms that regulate Cd uptake in plants, its translocation to the leaves and its
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accumulation in wheat grains.
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Large genetic variation for grain Cd concentration exists in durum wheat, but most of the commercial
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varieties have not been selected for a low-Cd trait. Research on genotypic variation and heritability of this
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character represents the main target of worldwide breeding programs of cultivated plants, with the aim to
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reduce the risk related to Cd in the human diet.
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Considering these premises, the objective of this study was to compare the effect of a non-lethal, but
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agronomically relevant24, Cd concentrations in hydroponic solution on the biomass production and Cd
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concentration in grains of several wheat genotypes. The primary aim of this work was the identification
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of genotypes suitable for cultivation in Cd-rich soils and those whose cultivation should be avoided being
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capable of high-Cd concentration in the grains. A multivariate analysis was carried out to identify clusters
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of cultivars sharing similar Cd concentration behaviors in roots, shoots, and grains. Results related to Cd
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bioaccumulation were then integrated with data achieved by ScOPC20 marker analysis25, a dominant
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molecular marker that cosegregates with Cdu1 (Cadmium Uptake 1) locus.
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Materials and Methods
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Genetic materials 4 ACS Paragon Plus Environment
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A set of two near-isogenic lines (NILs) of durum wheat (Triticum turgidum L. subsp. durum) that
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differs in grain Cd accumulation TL 8982-H (High-Cd) and TL-8982 L (Low-Cd)26 were chosen to make
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a comparison with twelve commercial varieties.
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Cultivars selection was based both on the year of release and on the pedigree relationship. Creso and
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Svevo were included in the study because they were selected from the field as the lowest and highest
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grain-Cd accumulating varieties, and finally classified as moderate accumulating and high
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accumulating grain-Cd, respectively, by Arduini et al.27.
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Based on their parental relationships, two Creso breeding lines (Arcangelo and Cirillo, Table 1) and two
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Svevo breeding lines (Aureo and Maestrale, Table 1) were also selected for analysis.
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Varieties and landraces have also been selected and then grouped according to their period of release:
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Aziziah, Cappelli and Russello (ANC: ancient cultivars and populations); Arcangelo and Creso
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(INC: intermediate cultivars); Cirillo, Iride, Parsifal and Svevo (MOC: modern cultivars); Aureo,
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Maestrale and Strongfield (RRC: recently released cultivars) (Table 1). The majority of pedigree
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information were provided from Genetic Resources Information System for Wheat and Triticale (GRIS)
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(http://wheatpedigree.net, last update: 2017-02-24)28.
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Experimental design
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Seeds were surface sterilized in 1.2% NaClO for 20 min, rinsed and imbibed for 24 h in an aerated
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solution of 1mM CaCl2.
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Grains were germinated in plastic Petri dishes with moist filter paper, in the dark at 23°C. After 3-4 days
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three germinated seed were placed in plastic pots (7x7x45 cm) filled with perlite, moistened with
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deionized water and transferred to the hydroponic system as described by Harris and Taylor24.
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The nutrient solution was prepared in reverse osmosis (RO) water (
