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      Editorial for Special Issue “Heavy Metals Accumulation, Toxicity, and Detoxification in Plants” †

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      International Journal of Molecular Sciences
      MDPI

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          Abstract

          “Heavy metals” is a collective term widely applied for the group of metals and metalloids with an atomic density above 4 g/cm3 [1]. Non-essential toxic plant heavy metals include arsenic (As), cadmium (Cd), chromium (Cr), cobalt (Co), lead (Pb), mercury (Hg), nickel (Ni), and vanadium (V); whereas others are essential, such as copper (Cu), iron (Fe), manganese (Mn), and zinc (Zn). Heavy metals cause harmful effects in plants, animals, and humans as a result of long-term or acute exposure. Toxicity from heavy metals is increasing due to the extensive release from industrial, agricultural, chemical, domestic, and technological sources, which in turn contaminate the water, soil, and air. Natural phenomena, such as volcanic eruptions and sea movements, also contribute to the natural cyclization of metals on the earth, and human activities often alter the rate of release and transport by increasing emissions by a few orders of magnitude. Heavy metals penetrate the human body through water, food, and air. Inside an organism, they bind to cellular structures, thereby damaging the performance of essential biological functions. Metals, for example, easily bind to the sulfhydryl groups of several enzymes that control the speed of metabolic reactions: the “new” metal-enzyme complex leads to the loss of the catalytic activity of the enzyme. The level of toxicity from heavy metals depends on several factors, including time of exposure, dose, and the health status of the people exposed. The European Environment Agency (EEA) reported that of the 1000 industrial plants that released heavy metals into the air in 2016, eighteen accounted for more than half of the total pollution, suggesting a great responsibility on the part of a few large companies (Figure 1) [2]. An additional issue is the biomagnification (or bioaccumulation) caused by the very slow rate of elimination of heavy metals from an organism. Bioaccumulation, in ecology and biology, is the process whereby the accumulation of toxic substances in living beings increases in concentration following a rise in the trophic level: the higher the trophic level, the stronger the concentration of heavy metals. Biomagnification is also expressed as the concentration increase of a pollutant in a biological organism over time. To limit the risks for humans and the environment, many countries have legislated limits for each heavy metal. Specific limits have been defined in drinking, waste, and surface waters (lakes, rivers, seas). There are also limits in foods and animal feed, because heavy metals can easily enter the food chain through plants (or algae) and are subsequently bioaccumulated into the higher trophic levels. The risk for human health is due to directly eating edible plant tissues, or indirectly through eating animals that have in turn fed on herbivores or directly on edible plant tissues. Understanding the mechanisms for regulating the storage and distribution of heavy metals in plants is the basis for improving the safety of the food chain. This special issue, entitled “Heavy Metals Accumulation, Toxicity, and Detoxification in Plants”, explores three main issues concerning heavy metals: (a) the accumulation and partitioning of heavy metals in crops and wild plants; (b) the toxicity and molecular behaviors of cells, tissues, and their effects on physiology and plant growth; and (c) detoxification strategies, plant tolerance, and phytoremediation. The issue contains a total of 19 articles (Table 1). There are four reviews covering the following topics: phytoremediation [3], manganese phytotoxicity in plants [4], cadmium effect on plant development [5], the genetic characteristics of Cd accumulation and the research status of genes and quantitative trait loci (QTLs) in rice [6], and fifteen original research articles, mainly regarding the impact of cadmium on plants [7,8,9,10,11,12,13,14,15,16,17,18,19,20,21]. Cadmium is therefore the predominant topic of this special issue, thus confirming the focus of the research community on the negative impacts determined by cadmium or cadmium associated with other heavy metals. Interestingly, we did not receive any manuscripts on other heavy metals such as arsenic, chromium and mercury despite their danger for human health. The cadmium research articles come from China, Poland, Italy, Canada, Pakistan, and the United States. These studies investigate different molecular mechanisms or approaches, using model plants such as Arabidopsis and tobacco [17,18,20] or hyperaccumulator plant species [9,16,19,21] to unravel their molecular strategies in heavy metal accumulation. Other articles focus on how to prevent cadmium from entering the food chain by investigating edible plants such as Zea mays [7], durum and bread wheat [12,13], or animal feeding plants such as Lolium multiflorum. The studies reveal some common strategies in terms of the molecular mechanisms involved. Some plants activate the production of small proteins such as glutathione S-transferase (GST) and small heat shock protein (sHSP) [9,11,21] or antioxidants [16]. In order to alleviate heavy metal toxicity, other plants respond by activating a complex metabolism-like auxin pathway [7,8,17]. Plants also produce specific metallothionines and phytosiderophores [10,12] to chelate heavy metals or to activate heavy metals transporters such as heavy metal ATPase (e.g., HMA2 and HMA4) and ATP-binding cassette (ABC) transporters [12,13,18,19,21]. The studies in this special issue highlight considerable genetic variability, suggesting different possibilities for accumulation, translocation, and reducing or controlling heavy metals toxicity in plants. Heavy metal pollution is still one of the world’s great challenges. In the future, the main research objective should be to identify and characterize the genes controlling the uptake and translocation of heavy metals in a plant’s above-ground organs in order to produce (i) phytoremediation plants that efficiently move heavy metals in the stem and leaves or (ii) plants dedicated to human nutrition that transport heavy metals only in trace amounts to seeds or fruits.

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          Heavy Metal Pollutions: State of the Art and Innovation in Phytoremediation

          Mineral nutrition of plants greatly depends on both environmental conditions, particularly of soils, and the genetic background of the plant itself. Being sessile, plants adopted a range of strategies for sensing and responding to nutrient availability to optimize development and growth, as well as to protect their metabolisms from heavy metal toxicity. Such mechanisms, together with the soil environment, meaning the soil microorganisms and their interaction with plant roots, have been extensively studied with the goal of exploiting them to reclaim polluted lands; this approach, defined phytoremediation, will be the subject of this review. The main aspects and innovations in this field are considered, in particular with respect to the selection of efficient plant genotypes, the application of improved cultural strategies, and the symbiotic interaction with soil microorganisms, to manage heavy metal polluted soils.
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            Advances in the Mechanisms of Plant Tolerance to Manganese Toxicity

            Manganese (Mn) is an essential element for plant growth due to its participation in a series of physiological and metabolic processes. Mn is also considered a heavy metal that causes phytotoxicity when present in excess, disrupting photosynthesis and enzyme activity in plants. Thus, Mn toxicity is a major constraint limiting plant growth and production, especially in acid soils. To cope with Mn toxicity, plants have evolved a wide range of adaptive strategies to improve their growth under this stress. Mn tolerance mechanisms include activation of the antioxidant system, regulation of Mn uptake and homeostasis, and compartmentalization of Mn into subcellular compartments (e.g., vacuoles, endoplasmic reticulum, Golgi apparatus, and cell walls). In this regard, numerous genes are involved in specific pathways controlling Mn detoxification. Here, we summarize the recent advances in the mechanisms of Mn toxicity tolerance in plants and highlight the roles of genes responsible for Mn uptake, translocation, and distribution, contributing to Mn detoxification. We hope this review will provide a comprehensive understanding of the adaptive strategies of plants to Mn toxicity through gene regulation, which will aid in breeding crop varieties with Mn tolerance via genetic improvement approaches, enhancing the yield and quality of crops.
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              Hormesis in Plants: The Role of Oxidative Stress, Auxins and Photosynthesis in Corn Treated with Cd or Pb

              Hormesis, which describes the stimulatory effect of low doses of toxic substances on growth, is a well-known phenomenon in the plant and animal kingdoms. However, the mechanisms that are involved in this phenomenon are still poorly understood. We performed preliminary studies on corn coleoptile sections, which showed a positive correlation between the stimulation of growth by Cd or Pb and an increase in the auxin and H2O2 content in the coleoptile sections. Subsequently, we grew corn seedlings in hydroponic culture and tested a wide range of Cd or Pb concentrations in order to determine hormetic growth stimulation. In these seedlings the gas exchange and the chlorophyll a fluorescence, as well as the content of chlorophyll, flavonol, auxin and hydrogen peroxide, were measured. We found that during the hormetic stimulation of growth, the response of the photosynthetic apparatus to Cd and Pb differed significantly. While the application of Cd mostly caused a decrease in various photosynthetic parameters, the application of Pb stimulated some of them. Nevertheless, we discovered that the common features of the hormetic stimulation of shoot growth by heavy metals are an increase in the auxin and flavonol content and the maintenance of hydrogen peroxide at the same level as the control plants.
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                Author and article information

                Journal
                Int J Mol Sci
                Int J Mol Sci
                ijms
                International Journal of Molecular Sciences
                MDPI
                1422-0067
                09 June 2020
                June 2020
                : 21
                : 11
                : 4103
                Affiliations
                Department of Biological and Environmental Sciences and Technologies, University of Salento, I-73100 Lecce, Italy; alessio.aprile@ 123456unisalento.it
                Author notes
                [†]

                This article is dedicated to Antonio Michele Stanca, eminent plant geneticist, friend, and mentor.

                Author information
                https://orcid.org/0000-0002-3124-9146
                https://orcid.org/0000-0002-6047-3526
                Article
                ijms-21-04103
                10.3390/ijms21114103
                7312012
                32526826
                649c88e1-e73b-4327-8164-4b1fac551bbf
                © 2020 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 01 June 2020
                : 05 June 2020
                Categories
                Editorial

                Molecular biology
                Molecular biology

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