Elemental Defense Hypothesis Research Articles

The elemental defense effect of cadmium on Alternaria brassicicola in Brassica juncea

BackgroundThe elemental defense hypothesis states a new defensive strategy that hyperaccumulators defense against herbivores or pathogens attacks by accumulating heavy metals. Brassica juncea has an excellent ability of cadmium (Cd) accumulation. However, the elemental defense effect and its regulation mechanism in B. juncea remain unclear.ResultsIn this study, we profiled the elemental defense effect and the molecular regulatory mechanism in Cd-accumulated B. juncea after Alternaria brassicicola infection. B. juncea treated with 180 mg Kg− 1 DW CdCl2 2.5H2O exhibited obvious elemental defense effect after 72 h of infection with A. brassicicola. The expression of some defense-related genes including BjNPR1, BjPR12, BjPR2, and stress-related miRNAs (miR156, miR397, miR398a, miR398b/c, miR408, miR395a, miR395b, miR396a, and miR396b) were remarkably elevated during elemental defense in B. juncea.ConclusionsThe results indicate that Cd-accumulated B. juncea may defend against pathogens by coordinating salicylic acid (SA) and jasmonic acid (JA) mediated systemic acquired resistance (SAR) and elemental defense in a synergistic joint effect. Furthermore, the expression of miRNAs related to heavy metal stress response and disease resistance may regulate the balance between pathogen defense and heavy metal stress-responsive in B. juncea. The findings provide experimental evidence for the elemental defense hypothesis in plants from the perspectives of phytohormones, defense-related genes, and miRNAs.

Soil cadmium stress reduced host plant odor selection and oviposition preference of leaf herbivores through the changes in leaf volatile emissions

The Elemental defense hypothesis suggested that metal accumulation in plant tissues could serve as direct defense to reduce herbivore feeding preference as metals are toxic to phytophagous insects. However, the indirectly defensive role of heavy metals on host plant odor selection and oviposition preference of leaf herbivores through the changes in leaf volatile organic compounds (VOCs) is still unknown. In this study, we used a local woody plant species, Populus yunnanensis, to investigate whether soil cadmium (Cd) stress could affect plant VOC production and whether Cd-mediated changes in leaf VOC emissions will further influence the host plant odor and oviposition preferences of female adults of a specialist and a generalist herbivore species. The results clearly showed that the soil Cd stress could prominently induce leaf total VOC emissions of P. yunnanensis and such induction was positively correlated with leaf Cd accumulation. Herbivore olfactometer bioassays further demonstrated that the VOCs released by P. yunnanensis under Cd exposure are far less attractive to both of the specialist and generalist female adults compared to control plants, leading to significant reduction in oviposition on Cd-treated plants. Moreover, the host plant odor selection and oviposition preference of the two herbivore species were all negatively correlated with leaf total VOC emissions, which confirmed the defensive role of Cd-induced VOCs for deterring the female insects. The result will extend the existing knowledge of the Elemental defense hypothesis and provide new insight into predicting the herbivore damage level of poplar species that naturally occurred in metal-polluted habitats.

Sexual differences in above- and belowground herbivore resistance between male and female poplars as affected by soil cadmium stress

Dioecious plant species presented sexual differences in metal accumulation and allocation between male and female conspecifics that grown on metal contaminated soil. As the Elemental defense hypothesis postulates that metals accumulated in plant tissues could protect plants from herbivory, whether such sexual dimorphism in response to metal stress of a dioecious plant will lead to differences in herbivore resistance between male and female conspecifics is still unknown. In this study, we used female and male siblings of Populus deltoides to investigate the effect of plant sex on the growth and feeding preferences of four leaf herbivores and a root herbivore under soil cadmium (Cd) stress. The results showed that the male plants accumulated significantly higher Cd in the leaves while the females allocated more Cd in the roots. Leaf herbivores fed on male leaves grew worse than those fed on female leaves under Cd exposure, while the root herbivore showed the opposite results. In addition, all leaf herbivores strongly preferred the leaves from Cd-stressed female plants than male ones. The quantification of gene expression further showed that Cd stress could significantly upregulate more genes involved in Cd uptake, transport and detoxification pathways in male leaves and female roots. In combination with the correlation tests, we postulated that such sexual differences in herbivore resistance between the two plant sexes was most likely due to the different Cd allocation patterns in plant leaves and roots.

Broomrape Species Parasitizing Odontarrhena lesbiaca (Brassicaceae) Individuals Act as Nickel Hyperaccumulators.

The elemental defense hypothesis supports that metal hyperaccumulation in plant tissues serves as a mechanism underpinning plant resistance to herbivores and pathogens. In this study, we investigate the interaction between Odontarrhena lesbiaca and broomrape parasitic species, in the light of the defense hypothesis of metal hyperaccumulation. Plant and soil samples collected from three serpentine sites in Lesbos, Greece were analyzed for Ni concentrations. Phelipanche nowackiana and Phelipanche nana were found to infect O. lesbiaca. In both species, Ni concentration decreased gradually from tubercles to shoots and flowers. Specimens of both species with shoot nickel concentrations above 1000 mg.kg−1 were found, showing that they act as nickel hyperaccumulators. Low values of parasite to O. lesbiaca leaf or soil nickel quotients were observed. Orobanche pubescens growing on a serpentine habitat but not in association with O. lesbiaca had very low Ni concentrations in its tissues analogous to excluder plants growing on serpentine soils. Infected O. lesbiaca individuals showed lower leaf nickel concentrations relative to the non-infected ones. Elevated leaf nickel concentration of O. lesbiaca individuals did not prevent parasitic plants to attack them and to hyperaccumulate metals to their tissues, contrary to predictions of the elemental defense hypothesis.

Effects of exogenous spermidine on poplar resistance to leaf and root herbivory as affected by soil cadmium stress

Elemental defense hypothesis (EDH) proposed that metal accumulation in plants could increase plant resistance to herbivores. However, the over-accumulation of metals in low-accumulators such as woody plants will cause adverse effects on plant health. Thus, the application of EDH on low-accumulators in metal contaminated areas is strongly limited. Since the supplement of exogenous spermidine (Spd) was reported to alleviate metal-induced toxicity in plants while stimulating metal accumulation in plant tissues, we hypothesized that such application will further improve plant resistance to herbivores. In this study, we employed a woody plant species, Populus yunnanensis, to test this hypothesis. We first tested a Spd concentration series applied on plants subjected to soil cadmium (Cd) stress and found that the 1 mM Spd strongly promoted plant growth while stimulated Cd accumulation in plant leaves and roots. We further conducted herbivore bioassays to test the growth performance and feeding preference of two leaf herbivore species and a root herbivore species that fed on plants from different treatments. The results showed that the inhibition effect of Cd stressed-plants on herbivore growth was significantly magnified by the addition of Spd. The growth weight of all the three tested herbivores were negatively correlated with increased Cd concentrations in plant tissues. In addition, the feeding preferences of the two leaf herbivore species were strongly repelled by leaf discs from Cd-treated plants with Spd supplement. The results suggested that the application of exogenous Spd at a certain dose could enhance elemental defense of plants against herbivory.

Exogenous nitrogen enhances poplar resistance to leaf herbivory and pathogen infection after exposure to soil cadmium stress

Elemental defense hypothesis suggests that toxic metals accumulated in plant tissues could enhance plant defense against herbivores and pathogens. Since over-accumulation of metals in plant organs will pose negative effects on plant health, it is necessary to find a way to alleviate metal-induced toxicity in plants while keeping or even improving plant resistance. Exogenous nitrogen (N) application was reported to have such alleviation effect while stimulating metal accumulation in plant tissues. In this study, we examined whether soil N addition in three different doses to a poplar species under cadmium (Cd) stress can simultaneously improve plant growth and resistance to four herbivorous insects and a leaf pathogen. The results showed that N application to Cd-amended soil prominently enhanced plant growth and leaf Cd accumulation. While N addition in three doses all remarkably reduced herbivore growth than control plants, only the highest N dose exerted stronger inhibition than the sole Cd-treated plants. In the paired-choice experiment, plants supplied with the highest N dose showed an enhanced deterrent effect on herbivore preference than plants exposed to sole Cd. Furthermore, plant resistance to the leaf pathogen infection was strongly enhanced as the levels of N addition increased. Leaf sugar and three main defensive chemicals were not affected by N application implied that such enhanced effect of N on plant resistance was due to increased leaf Cd accumulation. Our results suggested that the application of exogenous N over a certain amount could enhance the resistance of Cd-treated plants to leaf herbivory and pathogen infection.

Testing the elemental defense hypothesis with a woody plant species: Cadmium accumulation protects Populus yunnanensis from leaf herbivory and pathogen infection

Elemental defense hypothesis states that metals accumulated in plant tissues may serve as defense against herbivores and pathogens. However, evidences collected so far are inconsistent and studies using woody plants as model species are still lacking. In this study we used a local woody plant species, Populus yunnanensis, to investigate whether cadmium (Cd) accumulation in leaves can protect plants from leaf herbivory and pathogen infection. Plants grown with or without Cd supplementation in the soil were subjected to herbivory by a specialist (Botyodes diniasalis) and a generalist (Spodoptera exigua), or to pathogen infection by a leaf pathogenic fungus (Pestalotiopsis microspora). Two additional tests with artificial media amended with a series of Cd concentrations were conducted for S. exigua and P. microspora to investigate the toxicity of Cd independently of other organic defenses present in P. yunnanensis leaves. The results showed that both herbivores strongly preferred control leaves over leaves containing high Cd. Feeding on leaves from Cd-treated plants significantly reduced the growth and survivals of both herbivores. Furthermore, plants grown on Cd-amended soil were more resistant to fungal infection. Growth of S. exigua and P. microspora on artificial media decreased with increasing Cd concentrations. In conclusion, we found that Cd accumulated in P. yunnanensis leaves could effectively reduce leaf herbivory and pathogen infection, which fully supported the Elemental defense hypothesis.

Heavy metal (hyper)accumulation in leaves of Arabidopsis halleri is accompanied by a reduced performance of herbivores and shifts in leaf glucosinolate and element concentrations

Abiotic and biotic factors can significantly influence and modify the chemical composition of a plant. In this study the influences of exposure to cadmium and zinc and of herbivory on plant-insect interactions were investigated. We studied the performance of two herbivore species with different feeding modes (chewing versus sucking) on the metal-hyperaccumulator species Arabidopsis halleri (Brassicaceae) as well as individual glucosinolate (GLS) and element concentrations of young and old leaves in response to different soil and herbivore treatments. The performance of both insect species was reduced on plants grown on metal-amended soil compared to plants grown on unamended soil. This result supports the elemental defense hypothesis, which postulates that high internal metal concentrations can protect plants from herbivores and which was mostly tested with chewing herbivores so far. Alongside higher levels of heavy metals in plants grown on metal-amended soil, GLS and element concentrations were differentially affected in young versus old leaves and responded differently to herbivory. Concentrations of most GLS and elements were higher in young compared to old leaves, which is in line with the optimal defense theory, which predicts a better defense in more valuable tissue. Our results highlight that various organic as well as inorganic compounds in plants can be affected in different directions by the complex interplay between plants, herbivores, and heavy metal contamination of soil.

Zinc triggers signaling mechanisms and defense responses promoting resistance to Alternaria brassicicola in Arabidopsis thaliana

According to the elemental defense hypothesis the accumulation of trace elements by plants may substitute for organic defenses, while the joint effects hypothesis proposes that trace elements and organic defenses can have additive or synergistic effects against pathogens or herbivores. To evaluate these hypotheses the response of the pathosystem Alternaria brassicicola-Arabidopsis thaliana to control (2μM) and surplus (12μM) Zn was evaluated using the camalexin deficient mutant pad3-1 and mtp1-1, a mutant with impaired Zn vacuolar storage, along with the corresponding wildtypes. In vitro, a 50% inhibition of fungal growth was achieved by 440μM Zn. A. thaliana leaves could accumulate equivalent concentrations without harm. In fact, surplus Zn enhanced the resistance of A. thaliana to fungal attack in Columbia (Col-0), Wassilewskija (WS), and mtp1-1. However, surplus Zn was unable to protect pad3-1 demonstrating that Zn cannot substitute for camalexin, the main organic defense in A. thaliana. High, non phytotoxic leaf Zn concentrations enhanced the resistance to A. brassicicola of A. thaliana genotypes able to produce camalexin. This was mainly due to Zn-induced enhancement of the JA/ETH signaling pathway leading to enhanced PAD3 expression. These results support the joint effects hypothesis and highlight the importance of adequate Zn supply for reinforced pathogen resistance.

The current status of the elemental defense hypothesis in relation to pathogens.

Metal hyperaccumulating plants are able to accumulate exceptionally high concentrations of metals, such as zinc, nickel, or cadmium, in their aerial tissues. These metals reach concentrations that would be toxic to most other plant species. This trait has evolved multiple times independently in the plant kingdom. Recent studies have provided new insight into the ecological and evolutionary significance of this trait, by showing that some metal hyperaccumulating plants can use high concentrations of accumulated metals to defend themselves against attack by pathogenic microorganisms and herbivores. Here, we review the evidence that metal hyperaccumulation acts as a defensive trait in plants, with particular emphasis on plant–pathogen interactions. We discuss the mechanisms by which defense against pathogens might have driven the evolution of metal hyperaccumulation, including the interaction of this trait with other forms of defense. In particular, we consider how physiological adaptations and fitness costs associated with metal hyperaccumulation could have resulted in trade-offs between metal hyperaccumulation and other defenses. Drawing on current understanding of the population ecology of metal hyperaccumulator plants, we consider the conditions that might have been necessary for metal hyperaccumulation to be selected as a defensive trait, and discuss the likelihood that these were fulfilled. Based on these conditions, we propose a possible scenario for the evolution of metal hyperaccumulation, in which selective pressure for resistance to pathogens or herbivores, combined with gene flow from non-metallicolous populations, increases the likelihood that the metal hyperaccumulating trait becomes established in plant populations.

Selenium hyperaccumulation offers protection from cell disruptor herbivores.

BackgroundHyperaccumulation, the rare capacity of certain plant species to accumulate toxic trace elements to levels several orders of magnitude higher than other species growing on the same site, is thought to be an elemental defense mechanism against herbivores and pathogens. Previous research has shown that selenium (Se) hyperaccumulation protects plants from a variety of herbivores and pathogens. Selenium hyperaccumulating plants sequester Se in discrete locations in the leaf periphery, making them potentially more susceptible to some herbivore feeding modes than others. In this study we investigate the protective function of Se in the Se hyperaccumulators Stanleya pinnata and Astragalus bisulcatus against two cell disrupting herbivores, the western flower thrips (Frankliniella occidentalis) and the two-spotted spider mite (Tetranychus urticae).ResultsAstragalus bisulcatus and S. pinnata with high Se concentrations (greater than 650 mg Se kg-1) were less subject to thrips herbivory than plants with low Se levels (less than 150 mg Se kg-1). Furthermore, in plants containing elevated Se levels, leaves with higher concentrations of Se suffered less herbivory than leaves with less Se. Spider mites also preferred to feed on low-Se A. bisulcatus and S. pinnata plants rather than high-Se plants. Spider mite populations on A. bisulcatus decreased after plants were given a higher concentration of Se. Interestingly, spider mites could colonize A. bisulcatus plants containing up to 200 mg Se kg-1 dry weight, concentrations which are toxic to many other herbivores. Selenium distribution and speciation studies using micro-focused X-ray fluorescence (μXRF) mapping and Se K-edge X-ray absorption spectroscopy revealed that the spider mites accumulated primarily methylselenocysteine, the relatively non-toxic form of Se that is also the predominant form of Se in hyperaccumulators.ConclusionsThis is the first reported study investigating the protective effect of hyperaccumulated Se against cell-disrupting herbivores. The finding that Se protected the two hyperaccumulator species from both cell disruptors lends further support to the elemental defense hypothesis and increases the number of herbivores and feeding modes against which Se has shown a protective effect. Because western flower thrips and two-spotted spider mites are widespread and economically important herbivores, the results from this study also have potential applications in agriculture or horticulture, and implications for the management of Se-rich crops.

Selenium and the elemental defense hypothesis

Selenium and the elemental defense hypothesis

Selenium hyperaccumulation reduces plant arthropod loads in the field

The elemental defense hypothesis proposes that some plants hyperaccumulate toxic elements as a defense mechanism. In this study the effectiveness of selenium (Se) as an arthropod deterrent was investigated under field conditions. Arthropod loads were measured over two growing seasons in Se hyperaccumulator habitats in Colorado, USA, comparing Se hyperaccumulator species (Astragalus bisulcatus and Stanleya pinnata) with nonhyperaccumulators (Camelina microcarpa, Astragalus americanus, Descurainia pinnata, Medicago sativa, and Helianthus pumilus). The Se hyperaccumulating plant species, which contained 1000-14 000 microg Se g(-1) DW, harbored significantly fewer arthropods (c. twofold) and fewer arthropod species (c. 1.5-fold) compared with nonhyperaccumulator species that contained < 30 microg Se g(-1) DW. Arthropods collected on Se-hyperaccumulating plants contained three- to 10-fold higher Se concentrations than those found on nonhyperaccumulating species, but > 10-fold lower Se concentrations than their hyperaccumulator hosts. Several arthropod species contained > 100 microg Se g(-1) DW, indicating Se tolerance and perhaps feeding specialization. These results support the elemental defense hypothesis and suggest that invertebrate herbivory may have contributed to the evolution of Se hyperaccumulation.

Selenium: Deterrence, toxicity, and adaptation

Introduction The element selenium (Se), named after the moon (Greek selene), has long been known for its toxicity. In 1295, Marco Polo was the 1st to describe the typical symptoms of selenosis in his pack animals. Centuries later, selenosis may have played a role in the demise of General Custer in the battle of Little Big Horn. Still today, chronic or acute Se poisoning is responsible for the loss of thousands of head of livestock every year in the western United States, where Se is prevalent in soils. Due to its chemical similarity to sulfur, Se in excess will nonspecifi cally replace sulfur in proteins, leading to the observed toxicity. At low levels, however, Se is also an essential trace element for many organisms, including humans, as a component of specifi c selenoproteins that often play a role in cancer prevention. Selenosis in animals mostly is due to ingestion of Se hyperaccumulator plants, commonly termed “locoweeds” by ranchers. These plants can accumulate Se to around 1% of their dry weight, 100-fold higher levels than those found in surrounding vegetation, and 1,000-fold higher than soil Se. Selenium hyperaccumulator species mainly occur in the genera Astragalus (Fabaceae) and Stanleya (Brassicaceae), and predominantly are found on Se-rich soils as seen in the western United States. Several hypotheses exist for the functional signifi cance of the intriguing phenomenon of hyperaccumulation. We currently study the elemental defense hypothesis, which proposes that the accumulated Se protects the plants from herbivory or microbial infection. We also are interested in how accumulated Se in plants affects local ecological interactions (Pilon-Smits and Freeman 2006; Fig. 1A). In this paper, we give an overview of our fi ndings so far, followed by an overall discussion of their implications with respect to the evolution of hyperaccumulator plants and the management of Se-rich plants in natural and agricultural settings.

Extending the Elemental Defense Hypothesis: Dietary Metal Concentrations Below Hyperaccumulator Levels Could Harm Herbivores

Previous work has shown that hyperaccumulator levels of some metals can defend plants against herbivores, but the possibility of defense by metal concentrations at accumulator or normal levels is unexplored. This study tested the hypothesis that metals can defend plants at low concentrations. We determined the relative toxicities of eight metals commonly acquired by plants: Cd, Co, Cr, Cu, Mn, Ni, Pb, and Zn. Larvae of the diamondback moth (Plutella xylostella), a representative crucifer specialist, were fed with artificial diet amended with concentrations of metal varying from 2 to 3,000 microg/g. Different concentration ranges were used for each of the eight metals, and larval survival at 10-14 days was calculated for each concentration. All metals were toxic to diamondback moth larvae at hyperaccumulator levels. All metals, however, were also toxic to larvae at accumulator concentrations, far below those found in hyperaccumulating plants. Five metals (Cd, Mn, Ni, Pb, and Zn) were toxic below accumulator levels, Cd and Pb were toxic near the concentration ranges of normal plants, and Zn was toxic at a concentration within the normal range. Our results indicate that uptake of certain metals may provide a defensive benefit for plants, and that elemental defenses may be effective at concentrations far lower than previously hypothesized. This study implies that elemental defenses are more widespread in plants than previously believed, and that the ecological consequences of even low levels of metal accumulation need to be explored.