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The Role of Heavy Metals in Plant Response to Biotic Stress

Iwona Morkunas, Agnieszka Woźniak, Van Chung Mai and 2 more

Molecules · 2018 · Review · CC BY

doi:10.3390/molecules23092320

Abstract

The present review discusses the impact of heavy metals on the growth of plants at different concentrations, paying particular attention to the hormesis effect. Within the past decade, study of the hormesis phenomenon has generated considerable interest because it was considered not only in the framework of plant growth stimulation but also as an adaptive response of plants to a low level of stress which in turn can play an important role in their responses to other stress factors. In this review, we focused on the defence mechanisms of plants as a response to different metal ion doses and during the crosstalk between metal ions and biotic stressors such as insects and pathogenic fungi. Issues relating to metal ion acquisition and ion homeostasis that may be essential for the survival of plants, pathogens and herbivores competing in the same environment were highlighted. Besides, the influence of heavy metals on insects, especially aphids and pathogenic fungi, was shown. Our intention was also to shed light on the relationship between heavy metals deposition in the environment and ecological communities formed under a strong selective pressure.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 27, 2026. Paragraph numbers are ours, so an answer can point at one.

1. Introduction

Heavy metals belong to the group of the most dangerous pollutants in ecotoxicology regarding their high toxicity and their significant amounts released into the environment as a result of natural and anthropogenic processes. This situation creates a need for research focusing on the assessment of the impact of heavy metals on living organisms and other elements of the natural environment. Heavy metals might be poisonous depending on the metal type, its oxidation state, pH, concentration, duration and so forth, leading to the death of organisms. The toxicity of a specific substance depends on a variety of factors, including how much of the substance organisms are exposed to, how they are exposed and for how long. It is documented that chemicals at a low dose may have beneficial effects that is termed hormesis and at a high dose, harmful effects. In this review, we focus on the impact of heavy metals at hormetic and toxic doses on plant responses and how their presence in the surrounding environment affects the response of plants to biotic stressors such as insects, especially aphids and pathogenic fungi playing a definite role in the trophic chain (Table S1 and Table 1). Additionally, the effect of heavy metals on insects, especially aphids and fungi were demonstrated (Table 2 and Table 3). It has been documented that air and soil pollution, including heavy metals can affect the plants-insects/plants-pathogens relationships directly or indirectly, can be toxic or cause hormesis effect and change their behaviour and metabolism.

Understanding the mechanisms underlying plant resistance or tolerance of plants to abiotic and biotic stress factors is extremely important in the era of global warming, where the mobility of pollutants in the environment increases. Because plants are prone to various abiotic and biotic stresses, exposure of plants to one stress affects their response during the next stress leading to enhanced defence mechanisms to a later stress. This phenomenon called as “priming” results in a faster and stronger induction of basal defence mechanisms upon subsequent biotic stress factors. This is an example of the occurrence of “metabolic memory” in higher plants, some stress “memory” or “stress imprinting” defined as genetic or biochemical modifications. Moreover, it requires less energy expenditure than defence directly induced by insect feeding or infection caused by pathogens. Ahmad et al. reported that priming-inducing stimuli can provide more effective basal resistance, especially when an earlier defence response precedes immune suppression by the invading pathogen. Convergence points in abiotic and biotic stress signalling networks were also shown. On the other hand, the extremely interesting hypotheses of Poschenrieder and co-workers such as elemental defence hypothesis, trade-off hypothesis, metal therapy and metal-induced fortification showed that metal ions may be factors that induce chemical defences against herbivores and infective microorganisms. Suitable intracellular concentrations of essential metal ions are not only required for the optimal growth and development of plants and their enemies but also for pathogen virulence and plant defence. In the presence of different toxic levels of metal ions, the degree of metal avoidance and/or tolerance of the interacting organisms will determine the response of plant host-insect/plant host-pathogen.

Of all the known elements, more than 75% exhibit the properties of metals. The metals were divided into two groups due to their density (specific atomic mass). Thus, light metals present a density of less than 5 g/cm3 and heavy metals are defined as elements having specific weights higher than 5 g/cm3. A number of them (e.g., cobalt-Co, iron-Fe, manganese-Mn, molybdenum-Mo, nickel-Ni, zinc-Zn, copper-Cu) are essential micronutrients required for normal growth and take part in redox reactions, electron transfers and other important metabolic processes in plants, whereas, others such as lead-Pb, cadmium-Cd, chromium-Cr, mercury-Hg, arsenic-As and so forth are potentially highly toxic for plants. Heavy metals in the environment have various origins: they arise from natural processes such as rock weathering, volcanic eruptions, forest fires, soil-forming processes. However, the most important sources are anthropogenic processes. Large areas of land are contaminated with heavy metals resulting from mines, industries, urban activities and agricultural practices. In terrestrial ecosystems, heavy metals mainly enter into the plants from soil but they may also originate from the external atmosphere surrounding plants. One of the most serious problems related to metal toxicology is the contamination of soils with heavy metals, because they exhibit very high stability in soils and lack of biodegradability. Therefore, metals present in soils can easily enter into the food chain. According to the United States Environmental Protection Agency (UEPA), heavy metals are listed as priority pollutants. In terms of environmental risks, Pb, Hg, As and Cd are ranked as the first, second, third and sixth, respectively, in the list of US Agency for Toxic Substances and Disease Registry (ATSDR).

The effects of metals in soils are very complex and these effects are dependent on chemical processes such as adsorption–desorption, complexation–dissociation, oxidation–reduction, ion exchange and transporters. Adsorption–desorption and complexation–dissociation reactions mainly affect metal activity in soil, while oxidation–reduction can also change metal valence. The bioavailability and toxicity of metals in soils are significantly influenced by pH conditions. Excessive concentrations of heavy metals inhibit physiological processes such as photosynthesis, respiration, transpiration rates, N-metabolism and mineral nutrition, cell elongation, decrease in biomass and consequently can cause plant death. Plant responses to heavy metals are observed as changes in redox status, the level of signal molecules, the activity of antioxidant system enzymes, membrane permeability, cysteine content, glutathione (GSH) and phytochelatin (PCs) contents, protein content, expression of genes encoding pathogenesis-related (PR) proteins and genes encoding enzymes of the flavonoid biosynthesis pathway, level of phenolics and so forth (see references in Table S1). The impact of heavy metals is strongly related to their doses, the plant species and the plant developmental phase as well as environmental factors characteristic for a given climate zone. Toxic effects of metals on plants are generally well documented in the literature but research on the responses of organisms, including plants, insects and fungal pathogens to heavy metals at the hormetic doses are less known and at the same time extremely interesting.

2. Hormesis as A Biological Phenomenon in the Context of Organisms’ Defence against Heavy Metals

In the published literature, the impact of heavy metals on the reduction of plant growth and modification of root morphology was widely presented. Inhibition of the growth of plants under the effect of heavy metals leads to a decrease in yield, which is associated with the inhibition of most of the basic life processes of plants. However, at a low metal dose in the substrate, the opposite reaction can be observed. In the present review, we focus on the progress of research into hormetic responses in terms of growth of plants, insects and fungi. The hormesis phenomenon has been observed in many organisms in response to different stress factors, that is, chemical, physical and biological. As mentioned above, already in the 16th century, Paracelsus wrote that various toxic substances may be beneficial in small quantities. Calabrese and Baldwin reported that the concept of chemical hormesis originate over a century ago from the research of Schulz, who observed a stimulation of both the growth and the respiration of yeast at low metal doses. Later, this concept was supported by other studies known as the Arndt-Schulz law. Moreover, in the opinion of some authors, hormetic effects are observed not only for growth but also during development, reproduction, survival and longevity. These authors reported that hormetic effects may also be closely related to numerous metabolic and physiological responses such as metallothionein synthesis, DNA and RNA syntheses, mitosis, oxygen consumption, photosynthesis rate, tissue regeneration, immune response, stress protein synthesis, seed germination and so forth. According to Damelin et al., hormetic activity is a specific cellular response and most likely, a stress response to low but harmful levels of toxic agents. In another definition, hormesis refers to a process whereby a sublethal stressor renders an organism resistant to a subsequent stress. Additionally, an assessment of the toxicological basis of the hormetic dose-response relationship including implications for risk assessment, was provided by Calabrese. In turn, a detailed assessment of the occurrence of hormesis within plants was also reported by Calabrese and Blain. These authors presented the most prevalent chemical classes, including heavy metals and physical agents in the general hormesis database useful for plant studies. We summarized in Table S1, a list of various plant species, where the hormesis effect caused by various heavy metals has been observed. Additionally, information concerning the changes observed in various physiological and biochemical indicators of plants were also presented in Table S1.

For example, the hormesis effect of aluminium (Al) on the growth, development and biomass production of plants such as rice, tea, coffee, Melastoma malabathricum, soybean and maize was also recorded. Moreover, numerous studies have reported the hormesis effect caused by Cd for plant species such as Gypsophila fastigiata, Sedum alfredii, Viola baoshanensis, Lonicera japonica, Dianthus carhusianorum, Solanum melongena, Arabis paniculata, Brassica juncea, Salsola kali, Spirodela polyrrhiza, Arabis paniculata. This effect was also caused by As in the case of Spirodela polyrrhiza L.. Besides, numerous experiments with chromium (Cr) revealed hormetic growth in the cases of Eichhornia crassipes, Salsola kali L., Lemna minuta, Allium cepa L. and Capsicium annum L.. An hormetic response was observed as well, in the case of elements such as lanthanum (La) for Lonicera japonica, Oryza sativa L. and Arabis paniculata, Pb for Pisum sativum, Brassica pekinensis and Dianthus carthusianorum, Hg for Anthyllis vulneraria and Helianthus tuberosus, palladium (Pd) for P. sativum L., platinum (Pt) for Arabidopsis thaliana, uranium (U) for Schizachyrium scoparium, Zn for Thlaspi caerulescens, Sedum alfredii and Arabis paniculata.

Additionally, an hormesis effect was also demonstrated in the case of insects. For example, hormesis as induced by Cd was reported in an insect model, such as the queen blowfly, Phormia regina, where low levels of dietary Cd caused a significant increase of the pupation rate of larvae. Results of the above-mentioned research indicate the need to evaluate the impact of environmental stressors at different concentration ranges and during the entire life cycle. In turn, an hormetic effect was observed for insect survival of Folsomia candida under the influence of copper (Cu). Uranium (U) as well, caused hormetic responses in the case of earthworms (Eisenia fetida), which are the most abundant terrestrial species, playing an important role in maintaining the ecological function of soil. Eisenia andrei (Oligochaeta: Lumbricidae), the potworm Enchytraeus crypticus (Oligochaeta: Enchytraeidae) and the springtail Folsomia candida (Collembola: Isotomidae) were also used as invertebrate test organisms in studying the hormesis effect in insects. In turn, the glutathione S-transferase was involved in the induction of methylmercury (MeHg)-hormesis in the case of Caenorhabditis elegans, a free-living (non-parasitic) nematode. These studies were performed to search whether MeHg induces hormesis, that is, whereby a sub lethal exposure to MeHg rendered C. elegans resistant to a subsequent exposure to this organometal. Previous studies of the same authors reported neurotoxic resistance of C. elegans to MeHg.

Nickel (Ni)-contamination of soils containing earthworms caused a hormesis response of the soil microorganisms that displayed a stimulation of microbial biomass C and soil basal respiration (SBR). Moreover, the hormesis effect has also been shown to accelerate pest population growth, insecticide resistance development, pesticide-induced arthropod pest resurgences, leading to interesting applications for the management of beneficial insects. Environmental factors and other factors affect the amplitude of a wide range of hormetic responses. For example, availability of nutrients, temperature, light and factors such as symbiosis, density-dependent factors, time, have an influence on hormetic responses.

In turn, a few studies reported hormetic responses to fungi. As shown by Calabrese and Baldwin, the assessment of the toxic effect of substances on fungi has a long history referring to the physiology, the growth and the reproduction of fungi. Already, Raulin revealed that the sulphates of Zn and Fe markedly stimulated the growth of the fungus Aspergillus. Raulin′s studies were aimed at showing quantitative relationships between disinfection agents and fungi. Establishment of fungal dose-response data near the turn of the 19th/20th centuries was carried out by investigators such as Stevens, Clark and Duggar, who worked on the effect of numerous agents on fungal germination and/or mycelium growth and fruiting using wide metal dosage ranges. Later research, for example, Collin-Hansen et al. demonstrated the toxic and the hormetic effects of the potential emissions from a Zn smelter to induce oxidative damages to DNA and lipids in Boletus edulis. These authors observed negative trends between the concentration of some metals (Cd, Zn, Cu and Hg) and apurinic/apyrimidinic sites or lipid hydroperoxides in the reference king bolete group. It has been indicated that in B. edulis, low concentrations of Hg, caused relationships of an hormetic nature such as an increase in metabolism, immunity and growth. Lefcort et al. revealed that low levels of heavy metal pollution can have positive effects for populations of one snail species and one periphyton species. It should also be mentioned that a highly significant contribution to the history of hormesis was afforded by the research on yeast performed by Schulz.

3. Influence of Heavy Metals in the Response of Plants to Biotic Stressors and Cross-Talk between Heavy Metals and Biotic Stressors

Plants in the course of evolution demonstrate adaptation or tolerance to various abiotic and biotic stress factors. Responses of plants to environmental stresses involve constitutive defences as well as stress-inducible reactions. Stimulation of important tolerance pathways, such as enhancement of antioxidant enzymes activity, osmolyte accumulation, induction of membrane-localized transporters for efficient compartmentation of deleterious ions and accumulation of essential elements against pests or pathogens is also an area that has been intensively studied. Plants have developed mechanisms for ion homeostasis that enable them to cope with a certain limited excess of heavy metals. Potentially toxic but essential metals required for normal growth have to be absorbed and distributed to different parts of the plant. Hall and Williams reported that chaperons, chelators and specific transmembrane transporters have evolved. In plants non-adapted to given environmental conditions, that are challenged with ion excess, an enhanced biosynthesis of complexing substances such as phytochelatins, metallothioneins and/or organic acids can occur. It has been proven that in the case of arsenic (As) tolerance, normal constitutive tolerance as well as adaptive hypertolerance are based on phytochelatin-mediated sequestration. In turn, in the case of copper (Cu) tolerance, it has been found that high Cu tolerance in a metallicolous population of Silene vulgaris was associated with high transcript levels of the metallothionein-like gene SvMT2b. Abundance and tissue distribution of efficient, specific, efflux and transport systems for metal ions and chelators seem fundamental traits for high-level tolerance in plants.

Some metal cations are also important for plant nutrition. Metals such as Cu, Fe, Zn and Mn act as important cofactors for many enzymes and are essential for both mitochondrial and chloroplast functions. However, when supplied in excess, these essential cations can become toxic like other heavy metals. To maintain micronutrient metal homeostasis and to cope with the deleterious effects of nonessential heavy metals, plants have developed a complex network of metal uptake, chelation, trafficking and storage processes. Metal transporters are required to maintain metal homeostasis in plant cells. As reported by Ahanger et al., plants sensitive to high levels of metals cannot survive in unfavourable environmental conditions, despite the induction of tolerance mechanisms. It has been documented that the plant responses to stress are dependent on the tissue or the organ affected by a given stress factor. For example, transcriptional responses to stress are tissue or cell specific in roots and are quite different depending on the stress factor. In addition, the level and the duration of the stress (acute vs. chronic) can have a significant effect on the complexity of the response. However, it should be noted that, in the environment, metals do not act as a single factor but simultaneous or subsequent effects of several other stress factors are observed. Here, our goal is to provide literature data evidencing phenomena such as cross-tolerance and cross-resistance in the case of heavy metal and biotic stress factor interactions. Plant resistance mechanisms to heavy metals and biotic stress factors such as pathogenic fungi, bacteria and invertebrates, including insects are well known. However, progress in the field of abiotic and biotic stress signal transduction pathways and research results concerning metal hyperaccumulating plants make this topic still very interesting.

Responses to heavy metal excess in sensitive plants can resemble elicitor-induced defence reactions. As an example of the negative cross-talk existing between abiotic stress (heavy metal) and biotic stress responses, the study by Llugany et al. has indicated that Cd accumulation induces salicylic acid (SA) production in Thymus praecox but diminishes the plants′ ability to induce SA as a defence signal in response to attack by Erysiphe cruciferarum. Another study by Fones et al. has shown that some pathogen-induced defences such as callose deposition and pathogenesis-related (PR) protein gene induction appears to be absent in Noccaea caerulescens, although the tested plants retained the ability to produce SA as a response to infection. This study also showed that the ability of Pseudomonas syringae to infect N. caerulescens plants grown on low concentrations of Zn was dependent on a functional type III secretion system (T3SS), a pathogenicity mechanism used by P. syringae to disable plant defences. This suggests that certain defence mechanisms that are suppressed by T3SS-secreted effector proteins remain functional in this plant. On the contrary, cross talk in down-stream signalling events has been well documented. As one of few candidates for such an early interaction, the cell wall associated kinase 1 (WAK1) is required for Arabidopsis resistance to P. syringae; plants over-expressing WAK1 exhibit enhanced Al tolerance. Signal transduction pathways of biotic stresses offer multiple points of interaction with heavy metal stress signalling. Stress-activated increases in mitogen-activated protein kinases (MAPKs), phytohormones such as jasmonic acid (JA), salicylic acid (SA) and ethylene (ET) are in fact major cross points of interactions between pathogen-elicited responses and specific toxic effects of heavy metals. For example, exposure of Medicago sativa seedlings to excessive concentrations of Cu or Cd activates different MAPKs such as SIMK, MMK2, MMK3 and SAMK, thus suggesting that plants respond to heavy metal stress through the induction of several distinct MAPK pathways and that excess amounts of Cu and Cd induce different cellular signalling mechanisms. Another screen for Cd-responsive genes identified the Arabidopsis MAPKKK MEKK1 to be transcriptionally induced by high concentrations of Cd. JA is one of the typically phytohormones involved in signalling and induced as a result of cell damage by herbivores and necrotrophic pathogens but Cu and Cd were also found to induce JA in both A. thaliana and Phaseolus coccineus plants. JA is connected to the toxic action of these two heavy metals in plants, differentially reacting to exogenous JA and possessing variable dynamics depending on the studied plants as well as their growth stage. The Ni tolerant capability mediating SA signalling pathway in Thlaspi plants was constitutively elevated and the ability to maintain high levels of reduced glutathione seems to be a key factor for both metal tolerance and pathogen resistance. The mentioned above examples prove that plant hormones may play central roles in the tolerance of plants to changing environmental conditions. Moreover, the synergistic or antagonistic hormone actions and the coordinated regulation of hormone biosynthetic pathways in association with the induction of other defence responses, play crucial roles in the adaptation of plants to stresses.

Contamination of the environment with heavy metals causes their significant accumulation in organisms at various levels of the food chain. The presence of heavy metals in plants can affect other organisms such as bacteria, fungi and herbivores. As reported by Poschenrieder et al., antagonistic, synergistic or no-effect interactions between metal accumulation and infestation of herbivores or infection caused by pathogenic fungi/pathogenic bacteria may occur. In some cases, heavy metal accumulation in plants may function as a self-defence strategy evolved in hyperaccumulator plants against natural enemies. Metal-hyperaccumulating plants are able to accumulate exceptionally high concentrations of metals in their tissues. A new insight was provided that some metal hyperaccumulating plants can use high concentrations of accumulated metals to defend themselves against attacks by pathogenic microorganisms and herbivores. Already, in the introduction of this review work, we mentioned hypotheses concerning heavy metal-plant-pathogen and heavy metal-plant-insect relationships. The first “Elemental defence” hypothesis presented by Poschenrieder et al. assumes that high metal concentrations in plant tissues are deterrent for herbivores or fungi or can kill these organisms. This hypothesis is based on two modes of action by which the plant may exhibit the “elemental defence” against attacking herbivores: (1) the direct toxicity of the consumed plant material on the attacking herbivore and (2) the deterrence of herbivores, whereby plant tissues containing elevated concentrations of elements are less preferred by herbivores than plant material not having such high metal concentrations. Testing this hypothesis, some studies confirmed the role of the accumulation of Ni, Cd, Zn, As and Se and so forth in plant defence mechanisms. Heavy metals can act against herbivores through their toxic action but this does not safeguard the plant from undergoing damages before poisoning the enemy.

The initial mechanisms enabling insects to avoid heavy metal effects might be “avoidance”, which leads them to selectively eat only low-metal tissues of the plant and “dietary dilution,” consisting in lowering overall metal ingestion by eating both high-metal and low-metal containing tissues. On the other hand, experimental evidence does exist that some herbivores prefer to eat low-Zn containing Thlaspi caerulescens and low-Ni Senecio coronatus when offered a choice between plants containing either low or high-metal concentrations. Deterrent effects have also been observed for Cd, As and Se. This ability to avoid feeding on plants with high levels of heavy metals might support that herbivores have a “taste for metals.” Another mechanism deserving a particular interest is “tolerance,” in which physiological adaptations allow specialist herbivores to withstand a high-metal diet, thus disarming the elemental defences of the plant. The bug Melanotrichus boydi, for instance, prefers to feed on the Ni hyperaccumulator Streptanthus polygaloides and a strain of the moth Plutella xylostella (Lepidoptera: Plutellidae) feeds on the Se hyperaccumulator S. pinnata without suffering from the high-Se diet. However, since the metal treatment will strongly affect the plants′ metabolome, it might be that herbivores do not directly perceive metals in their food but rather metal-induced metabolites.

The next hypothesis known as “the joint effects,” assumes that many chemicals in plant cell compartments can act separately and/or in combination. If two or more defensive chemicals are enhanced and present combined effects, they display “joint effects” in a defensive model of plant. In general, there are several types of joint effects: additive, synergism and antagonism. The joint effect is considered as additive when two chemicals have a joint effect equal to that of their single effects when combined. The two chemicals display a positive interaction when they have an effect greater than the expected additive effect; the joint effect is thus synergistic. On the contrary, the joint effect is antagonistic if the two chemicals together have an effect lesser than the expected additive effect. “The joint effects” hypothesis has been tested using Spodoptera exigua neonates fed with artificial diets. Metal+metal experiments utilized diets amended with metal pairs, using four metals (Co, Cu, Ni and Zn) commonly hyperaccumulated by plants. Metals combined with other metals or organic compounds may be more effective against herbivores than individual metals. The latter authors evaluated the type of joint effects between Co, Cu, Ni and Zn when fed in combinations of two metals to larvae of a model herbivore, S. exigua (Lepidoptera: Noctuidae). Boyd and Moar reported that tissues of the Ni hyperaccumulator S. polygaloides was toxic to S. exigua when plants hyperaccumulated Ni. Cheruiyot et al. used artificial diets to determine lethal and sub lethal concentrations of four metals (Co, Cu, Ni and Zn) to S. exigua. Another experiment explored the toxicity of four metals hyperaccumulated by plants (Cd, Ni, Pb and Zn) and searched if metal combinations might broaden the defensive effectiveness of metals in S. polygaloides. Metals were used alone and in various combinations such as metal + metal (Zn plus Ni, Pb, or Cd). Artificial diet amended with these treatments was fed to larvae of the crucifer specialist herbivore Plutella xylostella. Combinations of metals significantly decreased survival and pupation rates. Effects of combinations were additive rather than synergistic or antagonistic. Because Zn enhanced the toxicity of other metals and Ni enhanced the toxicity of organic defensive chemicals, the defensive effects of metals are more widespread among plants than previously believed.

“The joint effects” hypothesis may justify the simultaneous presence of elemental and organic defences, which may act in concert with each other and enhance the overall plant defences. The results of studies from experiments on inorganic defences and organic defence chemicals in the Ni hyperaccumulator S. polygaloides and fed to larvae of P. xylostella revealed additive joint effects between Ni and some organic defence chemicals such as atropine, nicotine and tannic acid (Table 1). Combinations of metals plus organic chemicals significantly decreased survival and pupation rates. In turn, the research results of Noret et al. demonstrated that Zn hyperaccumulation in Thlaspi caerulescens did not protect plants against snails, Helix aspersa (Eupulmonata: Helicidae) and raised the important role of secondary metabolites such as glucosinolates in these plants. Therefore, the above results did not support the defence hypothesis of plants by heavy metals and have shown that nonmetallicolous plants afforded a better protection than metallicolous plants, as glucosinolates increased in plants without Zn after herbivore infestation. Winter et al. discovered that copper (Cu) enhanced the capacity of Zea mays to synthesize volatile organic compounds under insect attack. The higher Cu dose was found to be primed for enhanced volatile production that can be triggered by caterpillar feeding. Cu stress correlated with increased levels of ROS in roots and priming of herbivore-induced JA in leaves. In turn, Tolrà et al. demonstrated opposing response of T. caerulescens organs after exposure to increasing concentrations of Zn. In leaves of shoots that had accumulated extremely high Zn concentrations, total glucosinolate levels decreased, while in roots the level of glucosinolates increased with increasing Zn in tissues. This mechanism may contribute to increased defence of roots against biotic stressors. In the case of T. caerulescens shoot response, the above-mentioned research results support the hypothesis of a trade-off between Zn and glucosinolates.

In turn, “the defensive enhancement” hypothesis suggested that, in some plant species, heavy metals can protect the plants against herbivores and pathogens. Following this hypothesis, the threshold protective benefit concentration is crucial, as each concentration can cause death and/or reduced herbivore growth rate, smaller herbivore size at maturity and reduced fecundity. The increased concentrations of inorganic compounds in herbivore bodies may negatively impact their natural enemies, providing a beneficial component to the herbivore. It has been shown that hyperaccumulation and accumulation of certain elements may affect the defence of plants against herbivores. In the context of this hypothesis, it has been demonstrated that As, Cd, Ni, Se and Zn repelled the herbivores. The research dedicated to providing evidence of the “joint effects hypothesis” has demonstrated defence at relatively low element concentrations and tests of metal/metal and metal/organic compound combinations have revealed joint effects. On the other hand, sub lethal effects of elements may result in more damage to a plant under some scenarios. Heavy metals absorbed by insects have a clear effect on their growth, mortality and physiology. Zn and Cu connect to the cytosol metallothionein in the midgut of many organisms and, as such, are essential elements but at high concentrations they can be toxic. Cd is highly toxic, even at a low concentration and can create mutations in the organism. The effect of heavy metals on an index such as relative growth rate (RGR) is quite various. For example, the effect of a high concentration of Ni in Spodoptera litura reduced relative consumption rate (RCR) but a low concentration of Ni increased RGR. A similar study by Baghban et al. on the effect of Cd, Cu and Zn on feeding indices and energy reserves of the cotton boll worm Helicoverpa armigera showed that high concentrations of Cd significantly increased approximate digestibility. RGR was significantly enhanced with treatments by Cu, Cd and Zn. It is clear from the present results that the presence of heavy metals in the environment has an intense impact on insects as far as food consumption.

4. Effects of Heavy Metals on Insects Including Aphids

Insects play a definite role in the trophic chain and, as food for other organisms, they may constitute an important path for the bioaccumulation of heavy metals. Invertebrates, including insects are good models to study toxicity of heavy metals and, as such, are important bioindicators of environmental contaminations. In the published literature, there were several studies related to the transfer of heavy metals between soil-plant-insect. For example, it has been revealed that the concentration of Cd and Pb declined with increasing trophic levels, while concentrations of Zn and Cu slightly increased from plant to insect. Additionally, numerous literature reports show that the bioamplification (biomagnification) of metals in organisms occurs at higher food chain levels. The presence of heavy metals in insects and its impact on growth rate, mortality and physiology are well-known. Local adaptation of insects to environments contaminated with heavy metals was also reported. For example, van Ooik and Rantala demonstrated that the polluted strain (genotype) of the autumnal moth Epirrita autumnata displayed a better growth on polluted leaves than the non-polluted strain. Besides, it has previously been found that adding heavy metals to food at moderate levels enhanced the immune system of mots, while a high level of heavy metals decreased their immunity. Moreover, herbivore polyphagic species can avoid heavy metals-containing food.

On the other hand, it is known that elements such as Cd are highly toxic, even at a low concentration and have a broad impact on insects causing mutations. Besides, there are some examples of harmful effects of this metal on insects. In fact, Kafel et al. demonstrated that the insect Spodoptera exigua had a significantly lower survival rate and body weight upon Cd exposure. In turn, the development of Lymantria dispar L. larvae in the fourth, fifth and sixth instar was delayed and the larval mass in the third and fourth instar decreased. Additionally, Wu et al. showed that Boettcherisca peregrina larvae had altered total larval duration. Moreover, Cd can also have an impact on antioxidant systems in insects. As reported by Zhang et al., some herbivorous insects are strong accumulators of Cd, for example, Locusta migratoria, Oxya chinensis, Acrida chinensis (Orthoptera), Eligma narcissus or Lymantria dispar (Lepidoptera). As well, Pb ions can affect cells responsible for insect metamorphosis, damage mitochondrial cristae, decrease ATP synthesis and decrease the production of growth hormones. As a result of the influence of Pb, nanism and malformation of the fly imagines Calliphora vicina, reduces motor activity, delays the formation and the emergence of puparia, reduces the fertility and egg hatching in Drosophila melanogaster as well as elongation and finally changes the shape of wings, affect the prolongation and foldation of legs in Musca domestica L.. Moreover, there are some research results showing the deleterious effect of Hg on the number of developed oocytes, spermatogonia and spermatocytes in Culex pipiens and that Hg causes abnormality of mosquito’s fat body. Also, Hg ions induce oxidative stress in insect species housefly (Musca domestica), the cabbage looper moth (Trichoplusia ni), two caddisflies (Chimarra sp. and Hydropsyche betteni) and two mayflies (Maccaffertium modestum and Isonychia sp.). Harmful effects on insects have also been identified for other metals such as Mn, Cr, Cu, Hg, Zn and Ni. Hormesis effects of metals on insects are presented in Table 2. It should also be mentioned that the hormesis effect on insects is mostly observed in response to different insecticides.

Plant contamination with heavy metals may directly affect aphids, due to phloem feeding style and relationships with the plant host. Our latest research has revealed the effect of Pb on demographic parameters of pea aphid population, that is, pre-reproductive, reproductive and post-reproductive periods, fecundity and longevity and the feeding process by electronic recording of feeding by the Electrical Penetration Graph technique (EPG) (unpublished data). Moreover, it was shown that contamination with Cu, Pb, Zn and Cd in host plants like cabbage (Brassica oleracea) and radish (Raphanus sativus) affects the developmental instability of the cabbage aphids Brevicoryne brassicae. The population of cabbage aphids reared on host plants that accumulated heavy metals showed higher fluctuating asymmetry than population reared on non-contaminated ones. Besides, Cd and Pb effects on morphology of cabbage aphids of both host plants, that is, cabbage and radish, were revealed. All the six measured morphological characters were longer among populations reared on non-contaminated hosts than on contaminated populations, that is, length of ultimate rostral segment, second hind tarsal segment, siphunculi, hind tibia segment, total antennal segment, body length. Moreover, the research of Maryański et al. proved that heavy metal accumulation in aphids might cause additional energy expenditure because of metal detoxification and this might be reflected in an alteration of some traits, such as decreased body mass. These authors showed negative effects of both Cd and Zn on sizes of a number of body parts of carabid beetles, Poecillus cupreus L. Moreover, it has been demonstrated that pea aphids are unaffected by Ni accumulation in their host plants such as Streptanthus polygaloides. In turn, the aphid Brachycaudus lychindis L. feeding on Zn accumulating plants Silene vulgaris, can tolerate elevated levels of heavy metals but such an accumulation in turn changes its morphology. The development time of aphids is relatively shorter than for other groups of insects and depends on the host plant.

Contaminated plants with Cd and Pb separately, have important effects on the life history of aphids. The population characteristics of aphids such as fecundity (number of offspring produced per day) and fitness (intrinsic rate of population increase) were lower on contaminated host plants. However, there was no significant effect on development time (from birth to beginning of the first reproduction). Aphid population reared on the contaminated host plants had significantly decreased reproduction potential and their mortality was about 20% higher on contaminated host plants. Culliney and Pimentel revealed that the green peach aphid Myzus persicae fed on collard plants (Brassica oleracea L.) growing in pots with soils treated with chemically contaminated sewage sludge, had decreased survival and fecundity rates. In turn, Jaworska and Gospodarek performed experiments with plants that were cultivated in soils contaminated with heavy metals such as Cd, Ni, Cu, Zn and Pb and in soils with natural contents of these elements. It was demonstrated that in both experimental years, aphids preyed more numerously on plants cultivated in the contaminated soil. Besides, Mg fertilization of heavy metal-contaminated soils caused lower Cd and Ni contents and lower the number of Aphis fabae. Not all experiments about effects of host plant contaminated with heavy metals on the life history traits are clear and it may depend on many factors. Feeding aphids on contaminated host plants can cause accumulation of harmful metals in their body tissues and affect introduction into food chains. In addition, aphid infestation led to enhanced concentrations of heavy metals in the phloem sap. Studies about the effects of heavy metal- contaminated plants on aphids are limited. Earlier studies also revealed that aphids from contaminated host plants with Cu, firstly excreted Cu with honeydew although its concentration in body tissues did not increase. It has been noted that high metal concentrations had small adverse, not repeatable effects on development, reproduction and growth of aphids. Experiments were planned where green peach aphids (Myzus persicae L.) could choose plant Brassica juncea contaminated with or without Se. M. persicae clearly avoids plants containing Se. In another nonchoice experiment, accumulation of Se decreased up to 50% the growth of aphids and was even lethal. Hanson reported that Se-hyperaccumulators can protect plants from aphid feeding two orders of magnitude higher than the non-hyperaccumulators. Moreover, Boyd and Martens noticed that the concentration of Ni in aphids feeding on high-Ni plants (hyperaccumulating plants) was not dramatically increased. It was found that a high level of Ni in Ni-hyperaccumulator plants did not protect plants against aphids. On the basis of the analysed literature, it can thus be concluded that the influence of metals on aphids is diverse and dependent on heavy metals, plant species and predisposition of the plant for metal accumulation. Therefore, there is the need for further research in this area.

5. Effects of Heavy Metals on Fungi

Stimulation of fungal growth by low levels of heavy metals has generally been scarcely reported. In the published literature, there are reports concerning the stimulating effect of heavy metals on the growth of mycelium of pathogenic fungi as well as edible fungi (Table 3). For example, metal ion treatments with 5 mg·L−1 of Zn, Cu2+ and Fe2+ independently had a stimulating effect on the mycelial growth of Aspergillus flavus. In turn, salts of Cu2+, Fe2+ and Fe3+ at concentrations such as 5 × 10−4 M and 5 × 10−3 M enhanced mycelial growth of the fungus Endothia parasitica, while at a concentration of 5 × 10−4 M, Zn only induced a slight stimulation of the growth of the mycelium. Moreover, the stimulating impact of Pb, at a concentration of 3 ppm, on the mycelial growth of Pythium debaryanum (R. Hesse) was observed. Additionally, stimulation of the mycelial growth as a result of the impact of heavy metals such as Zn at concentrations 100–400 mg·kg−1 on Coniothyrum sp., Cr at 20–100 mg·kg−1, Li at 20–100 mg·kg−1 and Mn at 10–400 mg·kg−1 on Agrocybe praecox and Cu at 40 ppm and Pb on Cryptococcus neoformans was observed.

Binsadiq and Al-Rahmah demonstrated tolerance mechanisms of fungi in the presence of heavy metals. There are two suggested mechanisms for heavy metal tolerance in fungi, that is, extracellular sequestration (which includes chelation and cell-wall binding) and intracellular sequestration by binding ligands. The influence of heavy metals can exert against microorganisms themselves and through microbial processes. Whipps provided evidence that the influence of heavy metals on the microbial processes in the soil can occur through effects on the decomposition of litter, enzyme activity and growth of plants. In turn, Rudawska et al. showed that heavy metals influence the fungal population by changing the number, the composition and the diversity of microorganisms. The chemical and physical properties of the soil affect the presence of fungi in the soil and these soil characteristics may change according to increased concentrations of heavy metals which can be present separately or in combination. It should be stressed that the interaction between heavy metals and pathogenic fungi is dependent on many factors, that is, the degree of tolerance of the fungi and their possibility of absorption of the heavy metals. However, Agrios indicated that, as a result of adverse environmental factors, different types of fungi became able to survive in the forms of scleroses, chlamydospores, or others. Van West et al. suggested that some fungal species display tolerance to the presence of heavy metals in the environment. In turn, Khan et al. reported that fungi can be used as bioremediators in the polluted soils or as bioindicators.

On the other hand, the toxic effects of heavy metals on mycelial growth are mostly described in the literature. Stroiński and Floryszak-Wieczorek demonstrated that the cell membrane is the first target of the toxic action of metals which can cause electrolyte leakage and modification of the membrane permeability. Besides, heavy metals induce the generation of ROS upon fungal oxidative stress. It must be emphasized that the toxic effects of heavy metals on fungal growth vary widely, depending on the type of metals, their concentration and the considered fungal species. Hartikainen et al. studied the effects of Zn, Cu, Cd, Co, Cr and Li on many fungal species belonging to taxons such as Ascomycota, Basidiomycota and Zygomycota. These authors demonstrated harmful effects of these heavy metals on mycelium growth. In addition, Ag, Co, Cu, Fe, Hg, Mn, Pb and Zn had a deleterious impact on fungi of Nematophagus including Trichoderma harzianum, Trichoderma virens, Trichoderma hamatum, Pochonia chlamydosporia var. chlamydosporia and Arthrobotrys oligospora. Moreover, Abu-Mejdad demonstrated that the ionic forms of Cu and Zn inhibited the mycelial growth of Aspergilus niger, Candida albicans and Cryptococcus neoformans. In the presence of Cu, Zn, Cd and Pb, the mycelial growth speed of the fungi Fusarium oxysporum Schlecht. and Pythium debaryanum (R. Hesse) was considerably inhibited.

On the other hand, there are also reports in the published literature showing that the edible fungus Imleria badia is capable of accumulating high concentrations of various elements, including toxic metals and metalloids and this fact consequently had a significant effect on the total content of phenolic compounds and the antioxidant potential.

Metals can also enhance the resistance of plants to fungal infection. Triticum aestivum var Sonalika seedlings pre-exposed to 50 μM CdCl2 during 48 h and infected with Fusarium oxysporum did not exhibit Fusarium wilt, while the untreated seedlings displayed disease symptoms characteristics for Fusarium infection within 7 days post inoculation. Moreover, a similar inhibitory effect of heavy metals such as Cd, Al, Mn and Cu on the development of infections caused by fungal pathogens are presented in Table 3.

On the other hand, latest research concerning hormesis has focused on the effects of sub lethal doses of metal–containing fungicides on growth and virulence stimulations of plant-pathogenic fungi and oomycetes. There are a lot of reports of hormetic responses in plant pathogens. One of the earliest observations performed by Southam and Ehrlich demonstrated an hormetic response in plant pathogens, for example, stimulation of the metabolism of a wood-decaying fungus Fomitopsis officinalis by red cedar extracts. In turn, Hessayon demonstrated the hormesis effect of trichothecin on Fusarium oxysporum. Similar examples were also noted in the case of Pythium aphanidermatum, which was stimulated by the fungicide mefenoxam. Moreover, the presence of thiabendazole increased the germination of Penicillium expansum. Also, the mycelial growths of fungi such as Lyophyllum palustre (Peck) Singer and Phythium aphanidermatum, P. irregular and P. ultimatum were increased by propamocarb. Besides, Phytophthora infestans growth increased as a result of the impact of metalaxyl and Sclerotinia sclerotiorum under treatment with dimethachlon conditions.

6. Effects of Heavy Metals Deposition in the Environment on the Formation of Ecological Communities of Aphids under Natural Conditions

In recent years, increased interest has arisen in environmental research, whose results have underlined the relationship between the impact of environmental factors, including heavy metals and invertebrates, including aphids in natural uncontrolled conditions. Aphids react to all environmental changes and are considered to be organisms that have the ability to adapt to specific ecological conditions. Abiotic factors such as temperature, photoperiod, atmosphere quality, heavy metals have a significant impact on the development of these insects. Czylok et al. revealed aphid communities occurring in metalliferous areas. Baker et al. reported that ecological communities (biocoenosis) formed on soils with high levels of heavy metals have unique flora and fauna. Adverse environmental factors exert a strong selection pressure on organisms and the appearance, during coevolution, of new ecotypes or kinds of plants which are more resistant. According to Osiadacz and Hałaj, it would be important to find out whether the pressure exerted on plants could also affect a higher level of the food chain, that is, primary consumers, especially insects. These authors carried out research to clarify which aphid species and how numerous occur in metalliferous areas and whether they can form characteristic aphid communities. The obtained results demonstrated that metalliferous areas have characteristic communities associated with heavy metal grasslands. They concluded that the high content of metals in the soil did not affect the number of aphid species in the aphid communities but help to form species-rich characteristic for these communities. Moreover, Mackoś–Iwaszko performed observations on the species composition and the number of arthropods from various trophic groups settling the hawthorn Crataegus xmedia growing in urban conditions in different degrees of anthropopressure. The formation of proper aphid species in the city plays a crucial role. These works revealed that the sucking-piercing phytophagous aphids were the dominating trophic group settling C. xmedia.

In turn, other studies revealed that in an urban environment with different degrees of pollution (street and a large green complex), aphids were abundant on Acer platanoides. Besides, the number of aphids was significantly higher in the street site than in a large green complex and the highest number of aphids was observed for Periphyllus genus, which are better adapted to urbanized conditions due to high diapausing generations (morphs). The review of Mogren and Trumble evaluated the effects of metal and metalloid pollution on insect behaviors in various environmental conditions. Presented data reveal that a surprising number of insect species cannot detect metal and metalloid contamination, therefore do not always avoid food with significant metal concentrations. The consequence of this was a modification of ingestion, locomotor and reproductive behaviors of insects. Bahadorani and Hilliker and Hanson et al. reported that other species of insects moved to contaminated locations, resulting in general reduced species fitness, decrease of population size, species diversity and numerical superiority. In contrast, some species of aquatic insects showed a tendency to escape from contaminated sites.

7. Conclusions

In the presented review, we have provided data regarding the effect of heavy metals at low doses (the so-called hormetic effect) and toxic doses on the defense responses of plants and the cross-talk of heavy metals and biotic stressors such as insects or pathogenic fungi. Moreover, the hormetic response of insects and pathogens of plants was described. Additionally, we show the relationship between the impact of environmental factors, including heavy metals and invertebrates in natural uncontrolled conditions.

References 253

  1. 1.

    Straalen N., Donker M. Heavy metals adaptation in terrestial arthropods—Physiological and genetic aspects. Proc. Exp. Appl. Entomol. Neth. Entomol. Soc. 1994;5:3-17.

    Not in our library

  2. 2.

    Wang S., Li R., Zhang Z., Feng J., Shen F. Assessment of the heavy metal pollution and potential ecological hazardous in agricultural soils and crops of Tongguan, Shaanxi Province. J. Environ. Sci. China. 2014;34:2313-2320.

    Not in our library

  3. 3.

    Yadav S.K. Heavy metals toxicity in plants: An overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S. Afr. J. Bot. 2010;76:167-179.

    Not in our library10.1016/j.sajb.2009.10.007

  4. 4.

    Wierzbicka A., Bohgard M., Pagels J.H., Dahl A., Löndahl J., Hussein T., Swietlicki E., Gudmundsson A. Quantification of differences between occupancy and total monitoring periods for better assessment of exposure to particles in indoor environments. Atmos. Environ. 2015;106:419-428.

    Not in our library10.1016/j.atmosenv.2014.08.011

  5. 5.

    Bell J.N.B., Treshow M. Air Pollution and Plant Life. 2002.

    Not in our library

  6. 6.

    Mleczek M., Goliński P., Krzesłowska M., Gąsecka M., Magdziak Z., Rutkowski P., Budzyńska S., Waliszewska B., Kozubik T., Karolewski Z., et al. Phytoextraction of potentially toxic elements by six tree species growing on hazardous mining sludge. Environ. Sci. Pollut. Res. 2017;24:22183-22195.

    Not in our library10.1007/s11356-017-9842-3

  7. 7.

    Chmielowska-Bąk J., Izbiańska K., Ekner-Grzyb A., Bayar M., Deckert J. Cadmium stress leads to rapid increase in RNA oxidative modifications in soybean seedlings. Front. Plant Sci. 2018;8.

    Not in our library10.3389/fpls.2017.02219

  8. 8.

    Pastor V., Luna E., Mauch-Mani B., Ton J., Flors V. Primed plants do not forget. Environ. Exp. Bot. 2013;94:46-56.

    Not in our library10.1016/j.envexpbot.2012.02.013

  9. 9.

    Chen K., Arora R. Priming memory invokes seed stress-tolerance. Environ. Exp. Bot. 2013;94:33-45.

    Not in our library10.1016/j.envexpbot.2012.03.005

  10. 10.

    Borges A.A., Jiménez-Arias D., Expósito-Rodríguez M., Sandalio L.M., Pérez J.A. Priming crops against biotic and abiotic stresses: MSB as a tool for studying mechanisms. Front. Plant Sci. 2014;5.

    Not in our library10.3389/fpls.2014.00642

  11. 11.

    Bruce T.J.A., Matthes M.C., Napier J.A., Pickett J.A. Stressful “memories” of plants: Evidence and possible mechanisms. Plant Sci. 2007;173:603-608.

    Not in our library10.1016/j.plantsci.2007.09.002

  12. 12.

    Ahmad S., Gordon-Weeks R., Pickett J., Ton J. Natural variation in priming of basal resistance: From evolutionary origin to agricultural exploitation: Natural variation in priming of basal resistance. Mol. Plant Pathol. 2010;11:817-827.

    Not in our library10.1111/j.1364-3703.2010.00645.x

  13. 13.

    Fujita M., Fujita Y., Noutoshi Y., Takahashi F., Narusaka Y., Yamaguchi-Shinozaki K., Shinozaki K. Crosstalk between abiotic and biotic stress responses: A current view from the points of convergence in the stress signaling networks. Curr. Opin. Plant Biol. 2006;9:436-442.

    Not in our library10.1016/j.pbi.2006.05.014

  14. 14.

    Poschenrieder C., Tolrà R., Barceló J. Can metals defend plants against biotic stress? Trends Plant Sci. 2006;11:288-295.

    Not in our library10.1016/j.tplants.2006.04.007

  15. 15.

    Poschenrieder C., Tolrà R., Barceló J. Interactions between metal ion toxicity and defences against biotic stress: Glucosinolates and benzoxazinoids as case studies. For. Snow Landsc. Res. 2006;80:149-160.

    Not in our library

  16. 16.

    Holleman N., Wiberg E. Lehrbuch der Anorganischen Chemie. 1985.

    Not in our library

  17. 17.

    Sebastiani L., Scebba F., Tognetti R. Heavy metal accumulation and growth responses in poplar clones Eridano (Populus deltoides × maximowiczii) and I-214 (P. × euramericana) exposed to industrial waste. Environ. Exp. Bot. 2004;52:79-88.

    Not in our library10.1016/j.envexpbot.2004.01.003

  18. 18.

    Rai V., Khatoon S., Bisht S.S., Mehrotra S. Effect of cadmium on growth, ultramorphology of leaf and secondary metabolites of Phyllanthus amarus Schum. and Thonn. Chemosphere. 2005;61:1644-1650.

    Not in our library10.1016/j.chemosphere.2005.04.052

  19. 19.

    Khan A., Kuek C., Chaudhry T., Khoo C., Hayes W. Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation. Chemosphere. 2000;41:197-207.

    Not in our library10.1016/s0045-6535(99)00412-9

  20. 20.

    Clemens S. Molecular mechanisms of plant metal tolerance and homeostasis. Planta. 2001;212:475-486.

    Not in our library10.1007/s004250000458

  21. 21.

    Chang C.Y., Yu H.Y., Chen J.J., Li F.B., Zhang H.H., Liu C.P. Accumulation of heavy metals in leaf vegetables from agricultural soils and associated potential health risks in the Pearl River Delta, South China. Environ. Monit. Assess. 2014;186:1547-1560.

    Not in our library10.1007/s10661-013-3472-0

  22. 22.

    Singh A., Prasad S.M. Remediation of heavy metal contaminated ecosystem: An overview on technology advancement. Int. J. Environ. Sci. Technol. 2015;12:353-366.

    Not in our library10.1007/s13762-014-0542-y

  23. 23.

    Farouk S., Mosa A.A., Taha A.A., Ibrahim H.M., El-Gahmery A.M. Protective effect of humic acid and chitosan on radish (Raphanus sativus, L. var. sativus) plants subjected to cadmium stress. J. Stress Physiol. Biochem. 2011;7:99-116.

    Not in our library

  24. 24.

    Swartjes F.A., Breemen E.M.D., Otte P.F., Beelen P.V., Rikken M.G.J., Tuinstra J. Human health risks due to consumption of vegetables from contaminated sites. RIVM Rep. 2007;711701040:2007.

    Not in our library

  25. 25.

    Badawy S.H., Helal M.I., Chaudri A.M., Lawlor K., McGrath S.P. Soli solid-phase controls lead activity in soil solution. J. Environ. Qual. 2002;31:162-167.

    Not in our library10.2134/jeq2002.1620

  26. 26.

    Zornoza P., Vázquez S., Esteban E., Fernández-Pascual M., Carpena R. Cadmium-stress in nodulated white lupin: Strategies to avoid toxicity. Plant Physiol. Biochem. 2002;40:1003-1009.

    Not in our library10.1016/s0981-9428(02)01464-x

  27. 27.

    Tomaszewska B., Tukendorf A., Barałkiewicz D. The synthesis of phytochelatins in lupin roots treated with lead ions. Sci. Legumes. 1996;3:206-217.

    Not in our library

  28. 28.

    Małecka A., Jarmuszkiewicz W., Tomaszewska B. Antioxidative defense to lead stress in sub cellular compartments of pea root cells. Acta Biochim. Pol. 2001;48:687-698.

    Not in our library

  29. 29.

    Małecka A., Piechalak A., Morkunas I., Tomaszewska B. Accumulation of lead in root cells of Pisum sativum. Acta Physiol. Plant. 2008;30:629-637.

    Not in our library10.1007/s11738-008-0159-1

  30. 30.

    Rucinska R., Gwozdz E.A. Influence of lead on membrane permeability and lipoxygenase activity in lupine roots. Biol. Plant. 2005;49:617-619.

    Not in our library10.1007/s10535-005-0059-9

  31. 31.

    Pawlak-Sprada S., Arasimowicz-Jelonek M., Podgórska M., Deckert J. Activation of phenylpropanoid pathway in legume plants exposed to heavy metals. Part I. Effects of cadmium and lead on phenylalanine ammonia-lyase gene expression, enzyme activity and lignin content. Acta Biochim. Pol. 2011;58:6.

    Not in our library

  32. 32.

    Rucińska-Sobkowiak R. Water relations in plants subjected to heavy metal stresses. Acta Physiol. Plant. 2016;38.

    Not in our library10.1007/s11738-016-2277-5

  33. 33.

    Krzesłowska M., Woźny A. Lead uptake, localization and changes in cell ultrastructure of Funaria hygrometrica protonemata. Biol. Plant. 1996;38:253-259.

    Not in our library10.1007/bf02873855

  34. 34.

    Krzesłowska M., Lenartowska M., Samardakiewicz S., Bilski H., Woźny A. Lead deposited in the cell wall of Funaria hygrometrica protonemata is not stable—A remobilization can occur. Environ. Pollut. 2010;158:325-338.

    Not in our library10.1016/j.envpol.2009.06.035

  35. 35.

    Woźniak A., Drzewiecka K., Kęsy J., Marczak Ł., Narożna D., Grobela M., Motała R., Bocianowski J., Morkunas I. The influence of lead on generation of signalling molecules and accumulation of flavonoids in pea seedlings in response to pea aphid infestation. Molecules. 2017;22:1404.

    Not in our library10.3390/molecules22091404

  36. 36.

    Drzewiecka K., Gąsecka M., Rutkowski P., Magdziak Z., Goliński P., Mleczek M. Arsenic forms and their combinations induce differences in phenolic accumulation in Ulmus laevis Pall. J. Plant. Physiol. 2018;220:34-42.

    Not in our library10.1016/j.jplph.2017.09.013

  37. 37.

    Małecka A., Derba-Maceluch M., Kaczorowska K., Piechalak A., Tomaszewska B. Reactive oxygen species production and antioxidative defense system in pea root tissues treated with lead ions: Mitochondrial and peroxisomal level. Acta Physiol. Plant. 2009;31:1065-1075.

    Not in our library10.1007/s11738-009-0327-y

  38. 38.
    Hormesis: a fundamental concept in biology · 2014
    No notice
  39. 39.

    Kaiser J. Sipping from a poisoned chalice. Science. 2003;302:376-379.

    Not in our library10.1126/science.302.5644.376

  40. 40.

    Rucińska R., Waplak S., Gwóźdź E. Free radical formation and activity of antioxidantenzymes in lupin root exposed to lead. Plant Physiol. Biochem. 1999;37:187-194.

    Not in our library10.1016/s0981-9428(99)80033-3

  41. 41.

    Sandalio L.M., Dalurzo H.C., Gómez M., Romero-Puertas M.C., del Río L.A. Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J. Exp. Bot. 2001;52:2115-2126.

    Not in our library10.1093/jexbot/52.364.2115

  42. 42.

    Sobkowiak R., Deckert J. Cadmium-induced changes in growth and cell cycle gene expression in suspension-culture cells of soybean. Plant Physiol. Biochem. 2003;41:767-772.

    Not in our library10.1016/s0981-9428(03)00101-3

  43. 43.

    Chibuike G.U., Obiora S.C. Heavy metal polluted soils: Effect on plants and bioremediation methods. Appl. Environ. Soil Sci. 2014;2014:1-12.

    Not in our library10.1155/2014/752708

  44. 44.

    Moreno-Alvarado M., García-Morales S., Trejo-Téllez L.I., Hidalgo-Contreras J.V., Gómez-Merino F.C. Aluminum enhances growth and sugar concentration, alters macronutrient status and regulates the expression of NAC transcription factors in rice. Front. Plant Sci. 2017;8:73.

    Not in our library10.3389/fpls.2017.00073

  45. 45.

    Stebbing A.R.D. Hormesis—The stimulation of growth by low levels of inhibitors. Sci. Total Environ. 1982;22:213-234.

    Not in our library10.1016/0048-9697(82)90066-3

  46. 46.

    Calabrese E.J., Baldwin L.A. Can the concept of hormesis be generalized to carcinogenesis? Regul. Toxicol. Pharmacol. 1998;28:230-241.

    Not in our library10.1006/rtph.1998.1267

  47. 47.

    Schulz H. Uber Hefegifte. Pflugers Arch. Gesmate Physiol. Menschen Tiere. 1888;42:517-541.

    Not in our library10.1007/bf01669373

  48. 48.

    Damelin L.H., Vokes S., Whitcutt J.M., Damelin S.B., Alexander J.J. Hormesis: A stress response in cells exposed to low levels of heavy metals. Hum. Exp. Toxicol. 2000;19:420-430.

    Not in our library10.1191/096032700678816133

  49. 49.

    Calabrese E., Blain R. The occurrence of hormetic dose responses in the toxicological literature, the hormesis database: An overview. Toxicol. Appl. Pharmacol. 2005;202:289-301.

    Not in our library10.1016/j.taap.2004.06.023

  50. 50.

    Calabrese E.J., Blain R.B. Hormesis and plant biology. Environ. Pollut. 2009;157:42-48.

    Not in our library10.1016/j.envpol.2008.07.028

  51. 51.

    Hajiboland R., Bahrami Rad S., Barceló J., Poschenrieder C. Mechanisms of aluminum-induced growth stimulation in tea (Camellia sinensis). J. Plant Nutr. Soil Sci. 2013;176:616-625.

    Not in our library10.1002/jpln.201200311

  52. 52.

    da Silva de Jesus D., Machado Martins F., Dias de Azevedo Neto A. Structural changes in leaves and roots are anatomical markers of aluminum sensitivity in sunflower. Pesqui. Agropecu. Trop. 2016;46:383-390.

    Not in our library10.1590/1983-40632016v4641426

  53. 53.

    Ghanati F., Morita A., Yokota H. Effects of aluminum on the growth of tea plant and activation of antioxidant system. Plant Soil. 2005;276:133-141.

    Not in our library10.1007/s11104-005-3697-y

  54. 54.

    Watanabe T., Jansen S., Osaki M. The beneficial effect of aluminium and the role of citrate in Al accumulation in Melastoma malabathricum. New Phytol. 2004;165:773-780.

    Not in our library10.1111/j.1469-8137.2004.01261.x

  55. 55.

    Du B., Nian H., Zhang Z., Yang C. Effects of aluminum on superoxide dismutase and peroxidase activities, and lipid peroxidation in the roots and calluses of soybeans differing in aluminum tolerance. Acta Physiol. Plant. 2010;32:883-890.

    Not in our library10.1007/s11738-010-0476-z

  56. 56.

    Wang L., Fan X.-W., Pan J.-L., Huang Z.-B., Li Y.-Z. Physiological characterization of maize tolerance to low dose of aluminum, highlighted by promoted leaf growth. Planta. 2015;242:1391-1403.

    Not in our library10.1007/s00425-015-2376-3

  57. 57.

    Yang X.E., Long X.X., Ye H.B., He Z.L., Calvert D.V., Stoffella P.J. Cadmium tolerance and hyperaccumulation in a new Zn-hyperaccumulating plant species (Sedum alfredii Hance). Plant Soil. 2004;259:181-189.

    Not in our library10.1023/b:plso.0000020956.24027.f2

  58. 58.

    Liu W. Viola baoshanensis, a plant that hyperaccumulates cadmium. Chin. Sci. Bull. 2004;49:29.

    Not in our library10.1007/bf02901739

  59. 59.

    Jia L., Liu Z., Chen W., Ye Y., Yu S., He X. Hormesis effects induced by cadmium on growth and photosynthetic performance in a hyperaccumulator, Lonicera japonica Thunb. J. Plant Growth Regul. 2015;34:13-21.

    Not in our library10.1007/s00344-014-9433-1

  60. 60.

    Muszyńska E., Hanus-Fajerska E., Ciarkowska K. Studies on lead and cadmium toxicity in Dianthus carthusianorum calamine ecotype cultivated in vitro. Plant Biol. 2018;20:474-482.

    Not in our library10.1111/plb.12712

  61. 61.

    Siddhu G., Sirohi D.S., Kashyap K., Khan I.A., Khan M.A.A. Toxicity of cadmium on the growth and yield of Solanum melongena L. J. Environ. Biol. 2008;29:853-857.

    Not in our library

  62. 62.

    Qiu R.-L., Zhao X., Tang Y.-T., Yu F.-M., Hu P.-J. Antioxidative response to Cd in a newly discovered cadmium hyperaccumulator, Arabis paniculata F. Chemosphere. 2008;74:6-12.

    Not in our library10.1016/j.chemosphere.2008.09.069

  63. 63.

    Seth C.S., Kumar Chaturvedi P., Misra V. The role of phytochelatins and antioxidants in tolerance to Cd accumulation in Brassica juncea L. Ecotoxicol. Environ. Saf. 2008;71:76-85.

    Not in our library10.1016/j.ecoenv.2007.10.030

  64. 64.

    de la Rosa G., Peralta-Videa J.R., Montes M., Parsons J.G., Cano-Aguilera I., Gardea-Torresdey J.L. Cadmium uptake and translocation in tumbleweed (Salsola kali), a potential Cd-hyperaccumulator desert plant species: ICP/OES and XAS studies. Chemosphere. 2004;55:1159-1168.

    Not in our library10.1016/j.chemosphere.2004.01.028

  65. 65.

    Seth C.S., Chaturvedi P.K., Misra V. Toxic effect of arsenate and cadmium alone and in combination on giant duckweed (Spirodela polyrrhiza L.) in response to its accumulation. Environ. Toxicol. 2007;22:539-549.

    Not in our library10.1002/tox.20292

  66. 66.

    Tang Y.-T., Qiu R.-L., Zeng X.-W., Ying R.-R., Yu F.-M., Zhou X.-Y. Lead, zinc, cadmium hyperaccumulation and growth stimulation in Arabis paniculata Franch. Environ. Exp. Bot. 2009;66:126-134.

    Not in our library10.1016/j.envexpbot.2008.12.016

  67. 67.

    González C.I., Maine M.A., Cazenave J., Sanchez G.C., Benavides M.P. Physiological and biochemical responses of Eichhornia crassipes exposed to Cr (III). Environ. Sci. Pollut. Res. 2015;22:3739-3747.

    Not in our library10.1007/s11356-014-3558-4

  68. 68.

    Gardea-Torresdey J.L., de la Rosa G., Peralta-Videa J.R., Montes M., Cruz-Jimenez G., Cano-Aguilera I. Differential uptake and transport of trivalent and hexavalent chromium by tumbleweed (Salsola kali). Arch. Environ. Contam. Toxicol. 2005;48:225-232.

    Not in our library10.1007/s00244-003-0162-x

  69. 69.

    Paisio C.E., Fernandez M., González P.S., Talano M.A., Medina M.I., Agostini E. Simultaneous phytoremediation of chromium and phenol by Lemna minuta Kunth: A promising biotechnological tool. Int. J. Environ. Sci. Technol. 2018;15:37-48.

    Not in our library10.1007/s13762-017-1368-1

  70. 70.

    Patnaik A.R., Achary V.M.M., Panda B.B. Chromium (VI)-induced hormesis and genotoxicity are mediated through oxidative stress in root cells of Allium cepa L. Plant Growth Regul. 2013;71:157-170.

    Not in our library10.1007/s10725-013-9816-5

  71. 71.

    García-Jiménez A., Gómez-Merino F.C., Tejeda-Sartorius O., Trejo-Téllez L.I. Lanthanum affects bell pepper seedling quality depending on the genotype and time of exposure by differentially modifying plant height, stem diameter and concentrations of chlorophylls, sugars, amino Acids, and proteins. Front. Plant Sci. 2017;8.

    Not in our library10.3389/fpls.2017.00308

  72. 72.

    Guo S.F., Yu S.F., Huang X.H. Effect of La (III) on some physiological index and ultrastructure of honeysuckle (Lonicera japonica Thunb.). Adv. Mater. Res. 2013;864–867:295-298.

    Not in our library10.4028/www.scientific.net/amr.864-867.295

  73. 73.

    Liu D., Wang X., Zhang X., Gao Z. Effects of lanthanum on growth and accumulation in roots of rice seedlings. Plant Soil Environ. 2013;59:196-200.

    Not in our library10.17221/760/2012-pse

  74. 74.

    Xiong Z.-T. Lead uptake and effects on seed germination and plant growth in a Pb hyperaccumulator Brassica pekinensis Rupr. Bull. Environ. Contam. Toxicol. 1998;60:285-291.

    Not in our library10.1007/s001289900623

  75. 75.

    Piwowarczyk B., Tokarz K., Muszyńska E., Makowski W., Jędrzejczyk R., Gajewski Z., Hanus-Fajerska E. The acclimatization strategies of kidney vetch (Anthyllis vulneraria L.) to Pb toxicity. Environ. Sci. Pollut. Res. 2018;25:19739-19752.

    Not in our library10.1007/s11356-018-2197-6

  76. 76.

    Lv S., Yang B., Kou Y., Zeng J., Wang R., Xiao Y., Li F., Lu Y., Mu Y., Zhao C. Assessing the difference of tolerance and phytoremediation potential in mercury contaminated soil of a non-food energy crop, Helianthus tuberosus L. (Jerusalem artichoke). PeerJ. 2018;6:e4325.

    Not in our library10.7717/peerj.4325

  77. 77.

    Ronchini M., Cherchi L., Cantamessa S., Lanfranchi M., Vianelli A., Gerola P., Berta G., Fumagalli A. Palladium uptake by Pisum sativum: Partitioning and effects on growth and reproduction. Environ. Sci. Pollut. Res. 2015;22:7600-7611.

    Not in our library10.1007/s11356-015-4132-4

  78. 78.

    Gawrońska H., Przybysz A., Szalacha E., Pawlak K., Brama K., Miszczak A., Stankiewicz-Kosyl M., Gawroński S.W. Platinum uptake, distribution and toxicity in Arabidopsis thaliana L. plants. Ecotoxicol. Environ. Saf. 2018;147:982-989.

    Not in our library10.1016/j.ecoenv.2017.09.065

  79. 79.

    Meyer M.C., McLendon T., Price D. Evidence of depleted uranium-induced hormesis and differential plant response in three grasses. J. Plant Nutr. 1998;21:2475-2484.

    Not in our library10.1080/01904169809365579

  80. 80.

    Küpper H., Zhao F.J., McGrath S.P. Cellular compartmentation of Zinc in leaves of the hyperaccumulator Thlaspi caerulescens. Plant Physiol. 1999;119:305-312.

    Not in our library10.1104/pp.119.1.305

  81. 81.

    Nascarella M.A., Stoffolano J.G., Stanek E.J., Kostecki P.T., Calabrese E.J. Hormesis and stage specific toxicity induced by cadmium in an insect model, the queen blowfly, Phormia regina Meig. Environ. Pollut. 2003;124:257-262.

    Not in our library10.1016/s0269-7491(02)00479-7

  82. 82.

    Ardestani M.M., van Gestel C.A.M. Toxicodynamics of copper and cadmium in Folsomia candida exposed to simulated soil solutions: Copper and cadmium toxicodynamics in springtails. Environ. Toxicol. Chem. 2013;32:2746-2754.

    Not in our library10.1002/etc.2353

  83. 83.

    Giovanetti A., Fesenko S., Cozzella M.L., Asencio L.D., Sansone U. Bioaccumulation and biological effects in the earthworm Eisenia fetida exposed to natural and depleted uranium. J. Environ. Radioac. 2010;101:509-516.

    Not in our library10.1016/j.jenvrad.2010.03.003

  84. 84.

    Helmcke K.J., Aschner M. Hormetic effect of methylmercury on Caen orhabditis elegans. Toxicol. Appl. Pharmacol. 2010;248:156-164.

    Not in our library10.1016/j.taap.2010.07.023

  85. 85.

    Helmcke K.J., Syversen T., Miller D.M., Aschner M. Characterization of the effects of methylmercury on Caenorhabditis elegans. Toxicol. Appl. Pharmacol. 2009;240:265-272.

    Not in our library10.1016/j.taap.2009.03.013

  86. 86.

    Xia X., Lin S., Zhao J., Zhang W., Lin K., Lu Q., Zhou B. Toxic responses of microorganisms to nickel exposure in farmland soil in the presence of earthworm (Eisenia fetida). Chemosphere. 2018;192:43-50.

    Not in our library10.1016/j.chemosphere.2017.10.146

  87. 87.

    Ayyanath M.-M., Cutler G.C., Scott-Dupree C.D., Sibley P.K. Transgenerational shifts in reproduction hormesis in green peach aphid exposed to low concentrations of imidacloprid. PLoS ONE. 2013;8:e74532.

    Not in our library10.1371/journal.pone.0074532

  88. 88.

    Hashmi M.Z., Shen H., Zhu S., Yu C., Shen C. Growth, bioluminescence and shoal behavior hormetic responses to inorganic and/or organic chemicals: A review. Environ. Int. 2014;64:28-39.

    Not in our library10.1016/j.envint.2013.11.018

  89. 89.

    Calabrese E.J., Baldwin L.A. Chemical hormesis:its historical foundations as a biological hypothesis. Toxicol. Pathol. 1999;27:195-216.

    Not in our library10.1177/019262339902700207

  90. 90.

    Raulin J. Etudied chimiques sur la vegetation. Ann. Sci. Nat. Bot. 1869;93-299.

    Not in our library

  91. 91.

    Stevens F.L. The effect of aqueous solutions upon the germination of fungus spores. Bot. Gaz. 1898;377-406.

    Not in our library10.1086/327772

  92. 92.

    Clark J.F. Electrolytic dissociation and toxic effect. J. Phys. Chem. 1899;263-316.

    Not in our library10.1021/j150014a001

  93. 93.

    Clark J.F. On the toxic properties of some copper compounds with special reference to Bordeaux mixture. Bot. Gaz. 1902;26-48.

    Not in our library10.1086/328192

  94. 94.

    Clark J.F. On the toxic effect of deleterious agents on the germination and development of certain filamentous fungi. Bot. Gaz. 1899;28:378-404.

    Not in our library10.1086/327931

  95. 95.

    Duggar B.M. Physiological studies with reference to the germination of certain Funous spores. Bot. Gaz. 1901;38-66.

    Not in our library10.1086/328074

  96. 96.

    Collin-Hansen C., Andersen R.A., Steinnes E. Damage to DNA and lipids in Boletus edulis exposed to heavy metals. Mycol. Res. 2005;109:1386-1396.

    Not in our library10.1017/s0953756205004016

  97. 97.

    Lefcort H., Freedman Z., House S., Pendleton M. Hormetic effects of heavy metals in aquatic snails: Is a little bit of pollution good? EcoHealth. 2008;5:10-17.

    Not in our library10.1007/s10393-008-0158-0

  98. 98.

    Becher M., Talke I.N., Krall L., Krämer U. Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J. 2004;37:251-268.

    Not in our library10.1046/j.1365-313x.2003.01959.x

  99. 99.

    Hall J.L., Williams L.E. Transition metal transporters in plants. J. Exp. Bot. 2003;54:2601-2613.

    Not in our library10.1093/jxb/erg303

  100. 100.

    Schat H., van Hoof N.A.L.M., Tervahauta A., Hakvoort H.W.J., Chardonnens A.N., Koevoets P.L.M., Verkleij J.A.C., Ernst W.H.O. Evolutionary responses to zinc and copper stress in Bladder Campion, Silene vulgaris (Moench) Garcke. Plant Tolerance to Abiotic Stresses: Role of Genetic Engineering. 2000;343-360.

    Not in our library

  101. 101.

    Zhao F.J., Wang J.R., Barker J.H.A., Schat H., Bleeker P.M., McGrath S.P. The role of phytochelatins in arsenic tolerance in the hyperaccumulator Pteris vittata. New Phytol. 2003;159:403-410.

    Not in our library10.1046/j.1469-8137.2003.00784.x

  102. 102.

    van Hoof N.A., Hassinen V.H., Hakvoort H.W., Ballintijn K.F., Schat H., Verkleij J.A., Ernst W.H., Karenlampi S.O., Tervahauta A.I. Enhanced copper tolerance in Silene vulgaris (Moench) Garcke populations from copper mines is associated with increased transcript levels of a 2b-type metallothionein gene. Plant Physiol. 2001;126:1519-1526.

    Not in our library10.1104/pp.126.4.1519

  103. 103.

    Ahanger M.A., Akram N.A., Ashraf M., Alyemeni M.N., Wijaya L., Ahmad P. Plant responses to environmental stresses—From gene to biotechnology. AoB Plants. 2017;9.

    Not in our library10.1093/aobpla/plx025

  104. 104.
    Effects of abiotic stress on plants: a systems biology perspective · 2011
    No notice
  105. 105.

    Dinneny J.R., Long T.A., Wang J.Y., Jung J.W., Mace D., Pointer S., Barron C., Brady S.M., Schiefelbein J., Benfey P.N. Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science. 2008;320:942-945.

    Not in our library10.1126/science.1153795

  106. 106.

    Arasimowicz-Jelonek M., Floryszak-Wieczorek J., Drzewiecka K., Chmielowska-Bąk J., Abramowski D., Izbiańska K. Aluminum induces cross-resistance of potato to Phytophthora infestans. Planta. 2014;239:679-694.

    Not in our library10.1007/s00425-013-2008-8

  107. 107.

    Chmielowska J., Veloso J., Gutiérrez J., Silvar C., Díaz J. Cross-protection of pepper plants stressed by copper against a vascular pathogen is accompanied by the induction of a defence response. Plant. Sci. 2010;178:176-182.

    Not in our library10.1016/j.plantsci.2009.11.007

  108. 108.

    Barcelo J., Poschenrieder C. Fast root growth responses, root exudates, and internal detoxification as clues to the mechanisms of aluminium toxicity and resistance: A review. Environ. Exp. Bot. 2002;48:75-92.

    Not in our library10.1016/s0098-8472(02)00013-8

  109. 109.

    Steinberg C.E.W. Stress Ecology: Environmental Stress as Ecological Driving Force and Key Player in Evolution. 2012.

    Not in our library

  110. 110.

    Pollard A.J., Baker A.J.M. Deterrence of herbivory by zinc hyperaccumulation in Thlaspi caerulescens (Brassicae). New Phytol. 1997;135:655-658.

    Not in our library10.1046/j.1469-8137.1997.00689.x

  111. 111.

    Jonak C., Nakagami H., Hirt H. Heavy Metal Stress. Activation of Distinct Mitogen-Activated Protein Kinase Pathways by Copper and Cadmium. Plant Physiol. 2004;136:3276-3283.

    Not in our library10.1104/pp.104.045724

  112. 112.

    Nakagami H., Pitzschke A., Hirt H. Emerging MAP kinase pathways in plant stress signalling. Trends Plant. Sci. 2005;10:339-346.

    Not in our library10.1016/j.tplants.2005.05.009

  113. 113.

    Boyd R.S., Martens S.N. The raison d’etre for metal hyperaccumulation by plants. The Vegetation of Ultramafic (Serpentine) Soils. 1992;279-289.

    Not in our library

  114. 114.

    Tolrà R.P., Poschenrieder C., Alonso R., Barceló D., Barceló J. Influence of zinc hyperaccumulation on glucosinolates in Thlaspi caerulescens. New Phytol. 2001;151:621-626.

    Not in our library10.1046/j.0028-646x.2001.00221.x

  115. 115.

    Rout G.R., Panigrahi J. Analysis of Signaling Pathways during Heavy Metal Toxicity: A Functional Genomics Perspective. Elucidation of Abiotic Stress Signaling in Plants. 2015;295-322.

    Not in our library

  116. 116.
    Heavy Metal Stress, Signaling, and Tolerance Due to Plant-Associated Microbes: An Overview · 2018
    No notice
  117. 117.

    Vollenweider P., Günthardt-Goerg M.S. Diagnosis of abiotic and biotic stress factors using the visible symptoms in foliage. Environ. Pollut. 2005;137:455-465.

    Not in our library10.1016/j.envpol.2005.01.032

  118. 118.

    Llugany M., Martin S.R., Barceló J., Poschenrieder C. Endogenous jasmonic and salicylic acids levels in the Cd-hyperaccumulator Noccaea (Thlaspi) praecox exposed to fungal infection and/or mechanical stress. Plant. Cell. Rep. 2013;32:1243-1249.

    Not in our library10.1007/s00299-013-1427-0

  119. 119.

    Fones H.N., Eyles C.J., Bennett M.H., Smith J.A.C., Preston G.M. Uncoupling of reactive oxygen species accumulation and defence signalling in the metal hyperaccumulator plant Noccaea caerulescens. New Phytol. 2013;199:916-924.

    Not in our library10.1111/nph.12354

  120. 120.

    Sivaguru M., Ezaki B., He Z.-H., Tong H., Osawa H., Baluška F., Volkmann D., Matsumoto H. Aluminum-Induced Gene Expression and Protein Localization of a Cell Wall-Associated Receptor Kinase in Arabidopsis. Plant Physiol. 2003;132:2256-2266.

    Not in our library10.1104/pp.103.022129

  121. 121.

    Suzuki N., Koizumi N., Sano H. Screening of cadmium-responsive genes in Arabidopsis thaliana. Plant Cell Environ. 2001;24:1177-1188.

    Not in our library10.1046/j.1365-3040.2001.00773.x

  122. 122.

    Maksymiec W., Wianowska D., Dawidowicz A.L., Radkiewicz S., Mardarowicz M., Krupa Z. The level of jasmonic acid in Arabidopsis thaliana and Phaseolus coccineus plants under heavy metal stress. J. Plant Physiol. 2005;162:1338-1346.

    Not in our library10.1016/j.jplph.2005.01.013

  123. 123.

    Freeman J.L., Garcia D., Kim D., Hopf A., Salt D.E. Constitutively elevated salicylic acid signals glutathione-mediated nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Physiol. 2005;137:1082-1091.

    Not in our library10.1104/pp.104.055293

  124. 124.

    Peleg Z., Blumwald E. Hormone balance and abiotic stress tolerance in crop plants. Curr. Opin. Plant Biol. 2011;14:290-295.

    Not in our library10.1016/j.pbi.2011.02.001

  125. 125.
    The current status of the elemental defense hypothesis in relation to pathogens · 2013
    Not checked
  126. 126.

    Rascio N., Navari-Izzo F. Heavy metal hyperaccumulating plants: How and why do they do it? And what makes them so interesting? Plant Sci. 2011;180:169-181.

    Not in our library10.1016/j.plantsci.2010.08.016

  127. 127.

    Jhee E.M., Boyd R.S., Eubanks M.D. Nickel hyperaccumulation as an elemental defense of Streptanthus polygaloides (Brassicaceae): Influence of herbivore feeding mode. New Phytol. 2005;168:331-344.

    Not in our library10.1111/j.1469-8137.2005.01504.x

  128. 128.

    Martens S.N., Boyd R.S. The ecological significance of nickel hyperaccumulation: A plant chemical defense. Oecologia. 1994;98:379-384.

    Not in our library10.1007/bf00324227

  129. 129.

    Boyd R.S. The defense hypothesis of elemental hyperaccumulation: Status, challenges and new directions. Plant Soil. 2007;293:153-176.

    Not in our library10.1007/s11104-007-9240-6

  130. 130.

    Jiang R.F., Ma D.Y., Zhao F.J., McGrath S.P. Cadmium hyperaccumulation protects Thlaspi caerulescens from leaf feeding damage by thrips (Frankliniella occidentalis). New Phytol. 2005;167:805-814.

    Not in our library10.1111/j.1469-8137.2005.01452.x

  131. 131.

    Behmer S.T., Lloyd C.M., Raubenheimer D., Stewart-Clark J., Knight J., Leighton R.S., Harper F.A., Smith J.A.C. Metal hyperaccumulation in plants: Mechanisms of defence against insect herbivores. Funct. Ecol. 2005;19:55-66.

    Not in our library10.1111/j.0269-8463.2005.00943.x

  132. 132.

    Rathinasabapathi B., Rangasamy M., Froeba J., Cherry R.H., McAuslane H.J., Capinera J.L., Srivastava M., Ma L.Q. Arsenic hyperaccumulation in the Chinese brake fern (Pteris vittata) deters grasshopper (Schistocerca americana) herbivory. New Phytol. 2007;175:363-369.

    Not in our library10.1111/j.1469-8137.2007.02099.x

  133. 133.

    Galeas M.L., Klamper E.M., Bennett L.E., Freeman J.L., Kondratieff B.C., Quinn C.F., Pilon-Smits E.A.H. Selenium hyperaccumulation reduces plant arthropod loads in the field. New Phytol. 2008;177:715-724.

    Not in our library10.1111/j.1469-8137.2007.02285.x

  134. 134.

    Martens S.N., Boyd R.S. The defensive role of Ni hyperaccumulation by plants: A field experiment. Am. J. Bot. 2002;89:998-1003.

    Not in our library10.3732/ajb.89.6.998

  135. 135.

    Boyd R.S. High-nickel insects and nickel hyperaccumulator plants: A review. Insect Sci. 2009;16:19-31.

    Not in our library10.1111/j.1744-7917.2009.00250.x

  136. 136.

    Wall M.A., Boyd R.S., Cook J. Melanotrichus boydi (hemiptera: Miridae) is a specialist on the nickel hyperaccumulator streptanthus polygaloides (brassicaceae). Southwest. Nat. 2006;51:481-489.

    Not in our library10.1894/0038-4909(2006)51[481:mbhmia]2.0.co;2

  137. 137.

    Boyd R.S. Plant defense using toxic inorganic ions: Conceptual models of the defensive enhancement and joint effects hypotheses. Plant Sci. 2012;195:88-95.

    Not in our library10.1016/j.plantsci.2012.06.012

  138. 138.

    Boyd R.S., Moar W.J. The defensive function of Ni in plants: Response of the polyphagous herbivore Spodoptera exigua (Lepidoptera: Noctuidae) to hyperaccumulator and accumulator species of Streptanthus (Brassicaceae). Oecologia. 1999;118:218-224.

    Not in our library10.1007/s004420050721

  139. 139.

    Cheruiyot D.J., Boyd R.S., Coudron T.A., Cobine P.A. Biotransfer, bioaccumulation and effects of herbivore dietary Co, Cu, Ni, and Zn on growth and development of the insect predator Podisus maculiventris (Say). J. Chem. Ecol. 2013;39:764-772.

    Not in our library10.1007/s10886-013-0289-9

  140. 140.

    Noret N., Meerts P., Tolrà R., Poschenrieder C., Barceló J., Escarre J. Palatability of Thlaspi caerulescens for snails: Influence of zinc and glucosinolates. New Phytol. 2005;165:763-771.

    Not in our library10.1111/j.1469-8137.2004.01286.x

  141. 141.

    Winter T.R., Borkowski L., Zeier J., Rostás M. Heavy metal stress can prime for herbivore-induced plant volatile emission: Copper primes VOCs. Plant Cell Environ. 2012;35:1287-1298.

    Not in our library10.1111/j.1365-3040.2012.02489.x

  142. 142.

    Wise M.J., Kieffer D.L., Abrahamson W.G. Costs and benefits of gregarious feeding in the meadow spittlebug, Philaenus spumarius. Ecol. Entomol. 2006;31:548-555.

    Not in our library10.1111/j.1365-2311.2006.00814.x

  143. 143.
    Effect of heavy metals (Cd, Cu, and Zn) on feeding indices and energy reserves of the cotton boll worm Helicoverpa armigera Hübner (Lepidoptera: Noctuidae) · 2014
    Not checked
  144. 144.

    Trumble J.T., Jensen P.D. Ovipositional response, developmental effects and toxicity of hexavalent chromium to Megaselia scalaris, a terrestrial detritivore. Arch. Environ. Contam. Toxicol. 2004;46:372-376.

    Not in our library10.1007/s00244-003-3007-8

  145. 145.

    Emre I., Kayis T., Coskun M., Dursun O., Cogun H.Y. Changes in antioxidative enzyme activity, glycogen, lipid, protein, and malondialdehyde content in cadmium-treated Galleria mellonella larvae. Ann. Entomol. Soc. Am. 2013;106:371-377.

    Not in our library10.1603/an12137

  146. 146.

    Sun H.-X., Dang Z., Xia Q., Tang W.-C., Zhang G.-R. The effect of dietary nickel on the immune responses of Spodoptera litura Fabricius larvae. J. Insect Physiol. 2011;57:954-961.

    Not in our library10.1016/j.jinsphys.2011.04.008

  147. 147.

    Satapathy P., Achary V.M.M., Panda B.B. Aluminum-induced abiotic stress counteracts Fusarium infection in Cajanus cajan (L.) Millsp. J. Plant. Interact. 2012;7:121-128.

    Not in our library10.1080/17429145.2011.584133

  148. 148.

    Mittra B., Ghosh P., Henry S.L., Mishra J., Das T.K., Ghosh S., Babu C.R., Mohanty P. Novel mode of resistance to Fusarium infection by a mild dose pre-exposure of cadmium in wheat. Plant Physiol. Biochem. 2004;42:781-787.

    Not in our library10.1016/j.plaphy.2004.09.005

  149. 149.

    Mohapatra S., Mittra B. Protein glutathionylation protects wheat (Triticum aestivum Var. Sonalika) against Fusarium induced oxidative stress. Plant Physiol. Biochem. 2016;109:319-325.

    Not in our library10.1016/j.plaphy.2016.10.014

  150. 150.

    Cabot C., Gallego B., Martos S., Barceló J., Poschenrieder C. Signal cross talk in Arabidopsis exposed to cadmium, silicon, and Botrytis cinerea. Planta. 2013;237:337-349.

    Not in our library10.1007/s00425-012-1779-7

  151. 151.

    Yao Y.A., Wang J., Ma X., Lutts S., Sun C., Ma J., Yang Y., Achal V., Xu G. Proteomic analysis of Mn-induced resistance to powdery mildew in grapevine. J. Exp. Bot. 2012;63:5155-5170.

    Not in our library10.1093/jxb/ers175

  152. 152.

    Ghaderian Y.S.M., Lyon A.J.E., Baker A.J.M. Seedling mortality of metal hyperaccumulator plants resulting from damping off by Pythium spp.: Research seedling mortality of hyperaccumulator plants. New Phytol. 2000;146:219-224.

    Not in our library10.1046/j.1469-8137.2000.00645.x

  153. 153.

    Hanson B. Selenium accumulation protects Brassica juncea from invertebrate herbivory and fungal infection. New Phytol. 2003;159:461-469.

    Not in our library10.1046/j.1469-8137.2003.00786.x

  154. 154.

    Hanson B., Lindblom S.D., Loeffler M.L., Pilon-Smits E.A.H. Selenium protects plants from phloem-feeding aphids due to both deterrence and toxicity. New Phytol. 2004;162:655-662.

    Not in our library10.1111/j.1469-8137.2004.01067.x

  155. 155.

    Nummelin M., Lodenius M., Tulisalo E., Hirvonen H., Alanko T. Predatory insects as bioindicators of heavy metal pollution. Environ. Pollut. 2007;145:339-347.

    Not in our library10.1016/j.envpol.2006.03.002

  156. 156.

    Zhuang P., Zou H., Shu W. Biotransfer of heavy metals along a soil-plant-insect-chicken food chain: Field study. J. Environ. Sci. 2009;21:849-853.

    Not in our library10.1016/s1001-0742(08)62351-7

  157. 157.

    Leita L., Enne G., De Nobili M., Baldini M., Sequi P. Heavy metal bioaccumulation in lamb and sheep bred in smelting and mining areas of S.W. sardinia (Italy). Bull. Environ. Contam. Toxicol. 1991;46:887-893.

    Not in our library10.1007/bf01689734

  158. 158.

    Goodyear K., McNeill S. Bioaccumulation of heavy metals by aquatic macro-invertebrates of different feeding guilds: A review. Sci. Total Environ. 1999;229:1-19.

    Not in our library10.1016/s0048-9697(99)00051-0

  159. 159.

    Zhang Z.-S., Lu X.-G., Wang Q.-C., Zheng D.-M. Mercury, cadmium and lead biogeochemistry in the soil–plant–insect system in Huludao City. Bull. Environ. Contam. Toxicol. 2009;83:255-259.

    Not in our library10.1007/s00128-009-9688-6

  160. 160.

    Wan T.-L., Liu S., Tang Q.-Y., Cheng J.-A. Heavy Metal Bioaccumulation and Mobility from Rice Plants to Nilaparvata lugens (Homoptera: Delphacidae) in China. Environ. Entomol. 2014;43:654-661.

    Not in our library10.1603/en13026

  161. 161.

    Warrington S. Relationship between SO2 dose and growth of the pea aphid, Acyrthosiphon pisum, on peas. Environ. Pollut. 1987;43:155-162.

    Not in our library10.1016/0269-7491(87)90073-x

  162. 162.

    van Ooik T., Rantala M.J., Saloniemi I. Diet-mediated effects of heavy metal pollution on growth and immune response in the geometrid moth Epirrita autumnata. Environ. Pollut. 2007;145:348-354.

    Not in our library10.1016/j.envpol.2006.03.008

  163. 163.

    van Ooik T. Effects of Heavy Metal Pollution and Host Plant Leaf Chemistry on the Immune Defense and Life History Traits of An Insect Herbivore. 2008.

    Not in our library

  164. 164.

    El-Sheikh E.-S.A., Kamita S.G., Vu K., Hammock B.D. Improved insecticidal efficacy of a recombinant baculovirus expressing mutated JH esterase from Manduca sexta. Biol. Control. 2011;58:354-361.

    Not in our library10.1016/j.biocontrol.2011.06.002

  165. 165.

    Mitterboeck F., Fuehrer E. Effects of fluoride-polluted spruce leaves on nun moth caterpillars (Lymantria monacha). J. Appl. Entomol. 1988;105:19-27.

    Not in our library

  166. 166.

    Zhang Y., Lambiase S., Fasola M., Gandini C., Grigolo A., Laudani U. Mortality and tissue damage by heavy metal contamination in the German cockroach, Blattella germanica (Blattaria, Blattellidae). Ital. J. Zool. 2001;68:137-145.

    Not in our library10.1080/11250000109356398

  167. 167.

    Rayms-Keller A., Olson K.E., McGaw M., Oray C., Carlson J.O., Beaty B.J. Effect of heavy metals on Aedes aegypti (Diptera:Culicidae) larvae. Ecotoxicol. Environ. Saf. 1998;39:41-47.

    Not in our library10.1006/eesa.1997.1605

  168. 168.

    Dom N.C., Ahmad P., Mokhtar M.A.M., Rajan S. Assessment of heavy metal concentration on Aedes mosquito breeding sites in urban area, Malaysia. Int. J. Mosq. Res. 2017;4:12-19.

    Not in our library

  169. 169.

    Fountain M.T., Hopkin S.P. Continuous monitoring of Folsomia candida (Insecta: Collembola) in a metal exposure test. Ecotoxicol. Environ. Saf. 2001;48:275-286.

    Not in our library10.1006/eesa.2000.2007

  170. 170.

    Ilijin L., Periać-Mataruga V., Radojičić R., Lazarević J., Nenadović V., Vlahović M., Mrdaković M. Effects of cadmium on protocerebral neurosecretory neurons and fitness components in Lymantria dispar L. Folia Biol. 2009;58:91-99.

    Not in our library10.3409/fb58_1-2.91-99

  171. 171.

    Mogren C.L., Trumble J.T. The impacts of metals and metalloids on insect behavior. Entomol. Exp. Appl. 2010;135:1-17.

    Not in our library10.1111/j.1570-7458.2010.00967.x

  172. 172.

    Posthuma L., Van Straalen N.M. Heavy-metal adaptation in terrestrial invertebrates: A review of occurrence, genetics, physiology and ecological consequences. Comp. Biochem. Physiol. Part C Pharmacol. Toxicol. Endocrinol. 1993;106:11-38.

    Not in our library10.1016/0742-8413(93)90251-f

  173. 173.

    Xie L., Klerks P.L. Fitness cost of resistance to cadmium in the least killifish (Heterandria formosa). Environ. Toxicol. Chem. 2004;23:1499-1503.

    Not in our library10.1897/03-96

  174. 174.

    Bahrndorff S., Holmstrup M., Petersen H., Loeschcke V. Geographic variation for climatic stress resistance traits in the springtail Orchesella cincta. J. Insect Physiol. 2006;52:951-959.

    Not in our library10.1016/j.jinsphys.2006.06.005

  175. 175.

    Wilczek G., Kramarz P., Babczyńska A. Activity of carboxylesterase and glutathione S-transferase in different life-stages of carabid beetle (Poecilus cupreus) exposed to toxic metal concentrations. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2003;134:501-512.

    Not in our library10.1016/s1532-0456(03)00039-5

  176. 176.

    Morgan A.J., Kille P., Stürzenbaum S.R. Microevolution and ecotoxicology of metals in invertebrates. Environ. Sci. Technol. 2007;41:1085-1096.

    Not in our library10.1021/es061992x

  177. 177.

    van Ooik T., Rantala M.J. Local adaptation of an insect herbivore to a heavy metal contaminated environment. Ann. Zool. Fennici. 2010;47:215-222.

    Not in our library10.5735/086.047.0306

  178. 178.

    Ben-Shahar Y. The impact of environmental Mn exposure on insect biology. Front. Genet. 2018;9.

    Not in our library10.3389/fgene.2018.00070

  179. 179.

    Sovik E., Perry C.J., LaMora A., Barron A.B., Ben-Shahar Y. Negative impact of manganese on honeybee foraging. Biol. Lett. 2015;11:20140989.

    Not in our library10.1098/rsbl.2014.0989

  180. 180.

    Kafel A., Rozpędek K., Szulińska E., Zawisza-Raszka A., Migula P. The effects of cadmium or zinc multigenerational exposure on metal tolerance of Spodoptera exigua (Lepidoptera: Noctuidae). Environ. Sci. Pollut. Res. 2014;21:4705-4715.

    Not in our library10.1007/s11356-013-2409-z

  181. 181.

    Mirčić D., Blagojević D., Perić-Mataruga V., Ilijin L., Mrdaković M., Vlahović M., Lazarević J. Cadmium effects on the fitness-related traits and antioxidative defense of Lymantria dispar L. larvae. Environ. Sci. Pollut. Res. 2013;20:209-218.

    Not in our library10.1007/s11356-012-1057-z

  182. 182.

    Wu G.-X., Ye G.-Y., Hu C., Cheng J.-A. Accumulation of cadmium and its effects on growth, development and hemolymph biochemical compositions in Boettcherisca peregrina larvae (Diptera: Sarcophagidae). Insect Sci. 2006;13:31-39.

    Not in our library10.1111/j.1744-7917.2006.00065.x

  183. 183.

    Suganya M., Karthi S., Subramanian Shivakumar M. Effect of cadmium and lead exposure on tissue specific antioxidant response in Spodoptera litura. Free Radic. Antioxid. 2016;6:90-100.

    Not in our library10.5530/fra.2016.1.11

  184. 184.

    Al-Momani F.A., Massadeh A.M. Effect of different heavy-metal concentrations on Drosophila melanogaster larval growth and development. Biol. Trace Elem. Res. 2005;108:271-277.

    Not in our library10.1385/bter:108:1-3:271

  185. 185.

    Shulman M.V., Pakhomov O.Y., Brygadyrenko V.V. Effect of lead and cadmium ions upon the pupariation and morphological changes in Calliphora vicina (Diptera, Calliphoridae). Folia Oecol. 2017;44:28-37.

    Not in our library10.1515/foecol-2017-0004

  186. 186.

    Safaee S., Feridoni M., Mahadavi-Ahdavi N., Haddad F., Mirshamsi O. Effects of lead on the development of Drosophila melanogaster. Period. Biol. 2014;116:259-265.

    Not in our library

  187. 187.

    Haq R. Adverse effect of lead acetate on Drosophila melanogaster. J. Basic Appl. Sci. 2011;157-163.

    Not in our library10.6000/1927-5129.2011.07.02.13

  188. 188.

    Fouda M., Hassan M.I., El-Sheikh T., Abd-Elgaphar A., Hasaballah A. Histopathological effect of certain heavy metals on the mosquito vector Culex pipiens (Diptera:Culcidae). Al-Azhar Bull. Sci. 2011;22:69-83.

    Not in our library

  189. 189.

    Zaman K., MacGill R.S., Johnson J.E., Ahmad S., Pardini R.S. An insect model for assessing mercury toxicity: Effect of mercury on antioxidant enzyme activities of the housefly (Musca domestica) and the cabbage looper moth (Trichoplusia ni). Arch. Environ. Contam. Toxicol. 1994;26:114-118.

    Not in our library10.1007/bf00212802

  190. 190.

    Xie L., Flippin J.L., Deighton N., Funk D.H., Dickey D.A., Buchwalter D.B. Mercury(II) bioaccumulation and antioxidant physiology in four aquatic insects. Environ. Sci. Technol. 2009;43:934-940.

    Not in our library10.1021/es802323r

  191. 191.

    Kafel A., Nadgórska-Socha A., Gospodarek J., Babczyńska A., Skowronek M., Kandziora M., Rozpędek K. The effects of Aphis fabae infestation on the antioxidant response and heavy metal content in field grown Philadelphus coronarius plants. Sci. Total Environ. 2010;408:1111-1119.

    Not in our library10.1016/j.scitotenv.2009.11.013

  192. 192.

    Borowska J., Pyza E. Effects of heavy metals on insect immunocompetent cells. J. Insect Physiol. 2011;57:760-770.

    Not in our library10.1016/j.jinsphys.2011.02.012

  193. 193.

    Yu Y., Shen G., Zhu H., Lu Y. Imidacloprid-induced hormesis on the fecundity and juvenile hormone levels of the green peach aphid Myzus persicae (Sulzer). Pest. Biochem. Physiol. 2010;98:238-242.

    Not in our library10.1016/j.pestbp.2010.06.013

  194. 194.

    Yusmalinar S., Anggraeni T., Kustiati K., Wibowo I., Eka Putra R., Ahmad I. Reproductive ability enhancement of housefly (Musca domestica Linn) (Diptera: Muscidae) through hormesis by application of sublethal doses of imidacloprid and permethrin. J. Entomol. 2017;14:199-207.

    Not in our library10.3923/je.2017.199.207

  195. 195.

    Rabhi K.K., Esancy K., Voisin A., Crespin L., Le Corre J., Tricoire-Leignel H., Anton S., Gadenne C. Unexpected effects of low doses of a neonicotinoid insecticide on behavioral responses to sex pheromone in a pest insect. PLoS ONE. 2014;9:e114411.

    Not in our library10.1371/journal.pone.0114411

  196. 196.

    Sashindran Nair K., Vijayan V.A., Nair J.S., Trivedy K., Chinya P.K. Hormetic influence on silkworm, Bombyx mori L., of the phytojuvenoid ω-formyl longifolene oxime propargyl ether. Int. J. Trop. Insect Sci. 2002;22:145-150.

    Not in our library10.1017/s174275840001523x

  197. 197.

    Morse J.G. Agricultural implications of pesticide- induced hormesis of insects and mites. Hum. Exp. Toxicol. 1998;17:266-269.

    Not in our library10.1177/096032719801700510

  198. 198.

    Gong Y., Xu B., Zhang Y., Gao X., Wu Q. Demonstration of an adaptive response to preconditioning Frankliniella occidentalis (Pergande) to sublethal doses of spinosad: A hormetic-dose response. Ecotoxicology. 2015;24:1141-1151.

    Not in our library10.1007/s10646-015-1461-5

  199. 199.

    Cutler G.C. Insects, insecticides and hormesis: Evidence and considerations for study. Dose-Response. 2013;11.

    Not in our library10.2203/dose-response.12-008.cutler

  200. 200.

    Chen X.D., Seo M., Stelinski L.L. Behavioral and hormetic effects of the butenolide insecticide, flupyradifurone, on Asian citrus psyllid, Diaphorina citri. Crop Protec. 2017;98:102-107.

    Not in our library10.1016/j.cropro.2017.03.017

  201. 201.
    Gene Expression during Imidacloprid-Induced Hormesis in Green Peach Aphid · 2014
    Not checked
  202. 202.

    Ayyanath M.-M., Scott-Dupree C.D., Cutler G.C. Effect of low doses of precocene on reproduction and gene expression in green peach aphid. Chemosphere. 2015;128:245-251.

    Not in our library10.1016/j.chemosphere.2015.01.061

  203. 203.

    Guedes R.N.C., Cutler G.C. Insecticide-induced hormesis and arthropod pest management: Insecticide-induced hormesis. Pest Manag. Sci. 2014;70:690-697.

    Not in our library10.1002/ps.3669

  204. 204.

    Merrington G., Miller D., McLaughlin M.J., Keller M.A. Trophic barriers to fertilizer Cd bioaccumulation through the food chain: A case study using a plant--insect predator pathway. Arch. Environ. Contam. Toxicol. 2001;41:151-156.

    Not in our library10.1007/s002440010232

  205. 205.

    Görür G. Developmental instability in cabbage aphid (Brevicoryne brassicae) populations exposed to heavy metal accumulated host plants. Ecol. Indic. 2006;6:743-748.

    Not in our library10.1016/j.ecolind.2005.09.001

  206. 206.

    Görür G. Zinc and cadmium accumulation in cabbage aphid (Brevicoryne brassicae) host plants and developmental instability. Insect Sci. 2009;16:65-71.

    Not in our library10.1111/j.1744-7917.2009.00255.x

  207. 207.

    Maryański M., Kramarz P., Laskowski R., Nikilińska M. Decreased energetic reserves, morphological changes and accumulation of metals in carabid beetles (Poecilus cupreus L.) exposed to zinc- or cadmium-contaminated food. Ecotoxicology. 2001;11:127-139.

    Not in our library10.1023/a:1014425113481

  208. 208.

    Ernst W.H.O. Effects of heavy metals in plants at the cellulr and organismic level. Bioaccumulation and Biological Effects of Chemicals. 1998.

    Not in our library

  209. 209.

    Görür G. Effects of host plant contaminated with heavy metals on the life history traits of aphids (Breyicoryne brassicae L.). Pol. J. Ecol. 2007;55:113-120.

    Not in our library

  210. 210.

    Culliney T.W., Pimentel D. Ecological effects of organic agricultural practices on insect populations. Agric. Ecosyst. Environ. 1986;15:253-266.

    Not in our library10.1016/0167-8809(86)90124-6

  211. 211.

    Jaworska M., Gospodarek J. Changes in population of pests and beneficial insects caused by soil contamination with heavy metals. Chemia i Inżynieria Ekologiczna. 2000;7:1143-1151.

    Not in our library

  212. 212.

    Jaworska M., Gospodarek J. Aphid (Aphis fabae Scop.) occurence on broan beans (Vicia faba L. ssp Maior) depending on liming and magnesium treatment of soil contaminated with heavy metals. Acta Agrophys. 2003;1:647-652.

    Not in our library

  213. 213.

    Stolpe C., Giehren F., Krämer U., Müller C. Both heavy metal-amendment of soil and aphid-infestation increase Cd and Zn concentrations in phloem exudates of a metal-hyperaccumulating plant. Phytochemistry. 2017;139:109-117.

    Not in our library10.1016/j.phytochem.2017.04.010

  214. 214.

    Crawford L.A., Lepp N.W., Hodkinson I.D. Accumulation and egestion of dietary copper and cadmium by the grasshopper Locusta mihratoria R&F (Orthoptera:Arcididae). Environ. Pollut. 1996;92:241-246.

    Not in our library10.1016/0269-7491(96)00004-8

  215. 215.

    Boyd R.S., Martens S.N. Aphids are unaffected by the elemental defence of the nickel hyperaccumulator Streptanthus polygaloides (Brassicaceae). Chemoecology. 1999;9:1-7.

    Not in our library10.1007/s000490050027

  216. 216.

    Cuero R., Ouellet T., Yu J., Mogongwa N. Metal ion enhancement of fungal growth, gene expression and aflatoxin synthesis in Aspergillus flavus: RT-PCR characterization: Metal ions on gungal grwoth, gene expression and aflatoxin synthesis. J. Appl. Microbiol. 2003;94:953-961.

    Not in our library10.1046/j.1365-2672.2003.01870.x

  217. 217.

    Englander C.M., Corden M.E. Stimulation of mycelial growth of Endothia parasitica by heavy metals. Appl. Microbiol. 1971;22:1012-1016.

    Not in our library10.1128/am.22.6.1012-1016.1971

  218. 218.

    Golubovic Curguz V., Raicevic V., Tabakovic Tosic M., Veselinovic M., Jovanovic L.J. Same physiological characteristics of three ectomycorrhizal fungi from Suillus genus. Miner. Biotecnol. 2010;22:1-7.

    Not in our library

  219. 219.

    Hartikainen E.S., Lankinen P., Rajasärkkä J., Koponen H., Virta M., Hatakka A., Kähkönen M.A. Impact of copper and zinc on the growth of saprotrophic fungi and the production of extracellular enzymes. Boreal Environ. Res. 2012;17:210-218.

    Not in our library

  220. 220.

    Hartikainen E.S., Hatakka A., Kahkonen M.A. Impact of cadmium, chromium, cobalt, lithium and manganese to the growth of fungi and production of enzymes. Expert Opin. Environ. Biol. 2013;2.

    Not in our library10.4172/2325-9655.1000109

  221. 221.

    Abu-Mejdad N.M.J.A. Response of some fungal species to the effect of copper, magnesium and zinc under the laboratory condition. Eur. J. Exp. Biol. 2013;3:535-540.

    Not in our library

  222. 222.

    Binsadiq A., Al-Rahmah A. Growth of Podaxis pistilaria collected from Saudi Arabia at different concentrations of cadmium and lead. J. King Saudi Univ. Sci. 1993;5:127-135.

    Not in our library

  223. 223.

    Anahid S., Yaghmaei S., Ghobadinejad Z. Heavy metal tolerance of fungi. Sci. Iran. 2011;18:502-508.

    Not in our library10.1016/j.scient.2011.05.015

  224. 224.

    Whipps J.M. Microbial interactions and biocontrol in the rhizosphere. J. Exp. Bot. 2001;52:487-511.

    Not in our library10.1093/jxb/52.suppl_1.487

  225. 225.

    Rudawska M., Kieliszewska-Rokicka B., Leski T. Effect of aluminium on Pinus sylvestris seedlings mycorrhizal with aluminium-tolerant and aluminium-sensitive strains of Suillus luteus. Dendrobiology. 2000;45:89-96.

    Not in our library

  226. 226.

    Carter M.R. Seedling growth and mineral nutrition of Scots pine under acidic to calcareous soil condition. Soil Sci. 1987;144:175-180.

    Not in our library10.1097/00010694-198709000-00003

  227. 227.

    Puhe J. Growth and development of the root system of Norway spruce (Picea abies) in forest stands—A review. For. Ecol. Manag. 2003;175:253-273.

    Not in our library10.1016/s0378-1127(02)00134-2

  228. 228.

    Kieliszewska-Rokicka B., Kurczyńska E.U., Leski T. Physiological activity of ectomycorrhizas in a moderately polluted forest (Ratanica catchment, southern Poland). Dendrobiology. 2000;45:47-59.

    Not in our library

  229. 229.

    Agrios G.N. Plant Pathology. 1997.

    Not in our library

  230. 230.

    van West A., Appiah A.A., Gow N.A.R. Advances in research on oomycete root pathogens. Physiol. Mol. Plant Pathol. 2003;62:99-113.

    Not in our library10.1016/s0885-5765(03)00044-4

  231. 231.

    Stroiński A., Floryszak-Wieczorek J. Effect of cadmium on the host—Pathogen system. III. Influence of cadmium and Phytophthora infestans on membrane permeability of potato leaves. Biochem. Physiol. Pflanz. 1990;186:417-421.

    Not in our library10.1016/s0015-3796(11)80244-1

  232. 232.

    Stroiński A., Floryszak-Wieczorek J. Effects of cadmium on the host-pathogen system. IV. Influence of cadmium and Phytophthora infestans on membrane permeability of potato tuber. J. Plant Physiol. 1993;142:575-578.

    Not in our library10.1016/s0176-1617(11)80401-3

  233. 233.

    Zhang Q., Zeng G., Chen G., Yan M., Chen A., Du J., Huang J., Yi B., Zhou Y., He X., et al. The effect of heavy metal-induced oxidative stress on the enzymes in white rot fungus Phanerochaete chrysosporium. Appl. Biochem. Biotechnol. 2015;175:1281-1293.

    Not in our library10.1007/s12010-014-1298-z

  234. 234.

    Gadd G.M. Interactions of fungi with toxic metals. The Genus Aspergillus. 1994;361-374.

    Not in our library

  235. 235.

    Hasanzadeh M., Mohammadifar M., Norabadi M.T., Dashtipoor S., Sahebani N., Etebarian H.R. The effect of different salts (heavy metals) on the mycelium growth of Nematophagus fungi. Arch. Phytopathol. Plant Prot. 2012;45:2087-2094.

    Not in our library10.1080/03235408.2012.721681

  236. 236.

    Gąsecka M., Rzymski P., Mleczek M., Siwulski M., Budzyńska S., Magdziak Z., Niedzielski P., Sobieralski K. The relationship between metal composition, phenolic acid and flavonoid content in Imleria badia from non-polluted and polluted areas. J. Environ. Sci. Health B. 2017;52:171-177.

    Not in our library10.1080/03601234.2017.1261541

  237. 237.

    Southam C.M., Ehrlich J. Effects of extracts of western red-cedar heartwood on certain wood-decaying fungi in culture. Phytopathology. 1943;33:517-524.

    Not in our library

  238. 238.

    Hessayon D.G. Double-action of trichothecin and its production in soil. Nature. 1953;167:998-999.

    Not in our library10.1038/168998b0

  239. 239.

    Garzón C.D., Molineros J.E., Yánez J.M., Flores F.J., del Mar Jiménez-Gasco M., Moorman G.W. Sublethal doses of mefenoxam enhance Pythium damping-off of Geranium. Plant Dis. 2011;95:1233-1238.

    Not in our library10.1094/pdis-09-10-0693

  240. 240.

    Baraldi E., Mari M., Chierici E., Pondrelli M., Bertolini P., Pratella G.C. Studies on thiabendazole resistance of Penicillium expansum of pears: Pathogenic fitness and genetic characterization. Plant Pathol. 2003;52:362-370.

    Not in our library10.1046/j.1365-3059.2003.00861.x

  241. 241.

    Landry J., Martinez C., Rochefort L. The use of fungicide Nova to mitigate infection of Sphagnum by parasitic fungi in the greenhouse. Botany. 2011;89:655-661.

    Not in our library10.1139/b11-056

  242. 242.

    Moorman G.W., Kim S.H. Species of Pythium from greenhouses in Pennsylvania exhibit resistance to propamocarb and mefenoxam. Plant Dis. 2004;88:630-632.

    Not in our library10.1094/pdis.2004.88.6.630

  243. 243.

    Zhang S., Panaccione D.G., Gallegly M.E. Metalaxyl stimulation of growth of isolates of Phytophthora infestans. Mycologia. 1997;89:289-292.

    Not in our library10.1080/00275514.1997.12026783

  244. 244.

    Zhou F., Liang H.-J., Di Y.-L., You H., Zhu F.-X. Stimulatory effects of sublethal doses of dimethachlon on Sclerotinia sclerotiorum. Plant Dis. 2014;98:1364-1370.

    Not in our library10.1094/pdis-10-13-1059-re

  245. 245.

    Dixon A.F.G. Aphid Ecology. 1998.

    Not in our library

  246. 246.

    Czylok A., Gorczyca J., Hałaj R., Klimaszewski S.M., Wojciechowski W. Fauna mszyc (Homoptera, Aphidodea) zwałowisk odpadów węglowych i cynkowych województwa katowickiego. Acta Biol. Siles. 1991;18:108-117.

    Not in our library

  247. 247.

    Baker A.J.M., Ernst W.H.O., van der Ent A., Malaisse F., Ginocchio R., Batty L.C., Hallberg K.B. Metallophytes: The unique biological resource, its ecology and conservational status in Europe, central Africa and Latin America. Ecology of Industrial Pollution. 2010;7-40.

    Not in our library

  248. 248.

    Wierzbicka M., Rostański A. Microevolutionary changes in ecotypes of calamine waste heap vegetation near Olkusz, Poland: A review. Acta Biol. Cracoviensia Ser. Bot. 2002;44:7-19.

    Not in our library

  249. 249.

    Osiadacz B., Hałaj R. Aphids under stress. Species groups and ecological functional groups of aphids define heavy metal grasslands of Central Europe. Redia. 2016;35-51.

    Not in our library10.19263/redia-99.16.17

  250. 250.

    Mackoś-Iwaszko E. Arthropods settling Crataegus xmedia Bechst. in the landscape of Lublin City (South-Eastern Poland). Aphids Other Hemipterous Insects. 2012;18:71-82.

    Not in our library

  251. 251.

    Mackoś-Iwaszko E., Lubiarz M., Karczmarz K. The impact of urban conditions on the occurance of aphids on Acer platanoides L. Acta Sci. Pol. Hortorum Cultus. 2015;14:189-207.

    Not in our library

  252. 252.

    Bahadorani S., Hilliker A.J. Biological and behavioral effects of heavy metals in Drosophila melanogaster adults and larvae. J. Insect Behav. 2009;22:399-411.

    Not in our library10.1007/s10905-009-9181-4

  253. 253.

    Clements W.H. Metal tolerance and predator–prey interactions in benthic macroinvertebrate stream communities. Ecol. Appl. 1999;9:1073-1084.

    Not in our library10.1890/1051-0761(1999)009[1073:mtappi]2.0.co;2

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