Selenium-Tolerant Diamondback Moth Disarms Hyperaccumulator Plant Defense

Freeman, John L.; Quinn, Colin F.; Marcus, Matthew A.; Fakra, Sirine C.; Pilon-Smits, Elizabeth A. H.

doi:10.1016/j.cub.2006.09.015

Cited by 122 publications

(182 citation statements)

References 48 publications

(63 reference statements)

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“…Third, it can produce microscopic maps of chemical species.To our knowledge, XAS imaging has not been carried out on insects, and relatively little on organisms in general, although µ-XRF imaging of selenium localisation was carried out on high-concentration selenium-fed diamondback moth larvae (Plutella xylostella) inhabiting selenium hyperaccumulating plants. [25] Fig. 2 shows images of two different bertha armyworm larvae.…”

Section: Arsenic Speciation Using X-ray Absorption Spectroscopymentioning

confidence: 99%

Arsenic accumulation, biotransformation and localisation in bertha armyworm moths

Andrahennadi

Pickering

2008

Environ. Chem.

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Environmental context. Insects play an important role in the impact of environmental pollutants such as arsenic. They may accumulate arsenic to high levels, potentially modifying its chemical form, which affects the insects' toxicity to predators such as fish and birds. Here we use synchrotron X-ray techniques to determine the distribution and chemical form of arsenic in larva, pupa and adult of the bertha armyworm moth.Abstract. Insects are important in bioaccumulation and dispersal of environmental contaminants such as arsenic, and biotransformation of arsenic to various chemical forms directly impacts its toxicity to insects and to their predators. In a model study, the toxic effects and biotransformation of arsenic were examined in larvae, pupae and adults of bertha armyworm moth (Mamestra configurata Walker) (Lepidoptera: Noctuidae). A synthetic diet containing 100 µM arsenate caused reduced larval survival and increased pupal stage duration but no effect on pupal weight or larval stage duration. Synchrotron X-ray absorption spectroscopy (XAS) showed that larvae biotransformed dietary arsenate to yield predominantly trivalent arsenic coordinated with three aliphatic sulfurs, modelled as As III -tris-glutathione. Similar species were found in pupae and adults. XAS imaging with micro X-ray fluorescence imaging revealed highly localised arsenic species, and zinc and copper within the gut. The implication of these arsenic species in the diets of predators is discussed.

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Section: Arsenic Speciation Using X-ray Absorption Spectroscopymentioning

confidence: 99%

Arsenic accumulation, biotransformation and localisation in bertha armyworm moths

Andrahennadi

Pickering

2008

Environ. Chem.

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“…These larvae were documented through laboratory tests to tolerate the hyperaccumulated Se (2,000 mg kg 21 dry weight) in S. pinnata leaves and not to be deterred by high-Se plants. In contrast, a diamondback moth population collected and reared from a nonseleniferous area in the eastern United States quickly died after feeding on high-Se leaves and was deterred by high-Se S. pinnata plants (Freeman et al, 2006a). A potential mechanism for the difference in Se tolerance between the two moth populations was revealed by mXANES and LC-MS analyses, which demonstrated that the Se-tolerant moth accumulated MeSeCys, similar to its host plant S. pinnata, whereas the Se-sensitive population accumulated SeCys and had obvious disintegration of internal organs (Freeman et al, 2006a).…”

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“…Hyperaccumulator plants may host Se-tolerant herbivores, as shown in a previous study that reported a Se-tolerant moth species associated with S. pinnata (Freeman et al, 2006a). Larvae from a population of Setolerant Plutellidae closely resembling the diamondback moth (Plutella xylostella), a damaging agricultural pest, were collected from S. pinnata in a seleniferous area (Fort Collins, CO).…”

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confidence: 99%

“…Se can protect plants from a wide variety of Se-sensitive invertebrate and vertebrate herbivores, due to deterrence and toxicity (for review, see Boyd, 2007Boyd, , 2010Quinn et al, 2007;El Mehdawi and Pilon-Smits, 2012). Se has been shown to protect plants from aphids (Hurd-Karrer and Poos, 1936;Hanson et al, 2004), moth and butterfly larvae (Vickerman et al, 2002;Hanson et al, 2003;Freeman et al, 2006a), crickets and grasshoppers , thrips and spider mites , and prairie dogs Freeman et al, 2009). The hyperaccumulators A. bisulcatus and Stanleya pinnata also harbored fewer arthropods in their native seleniferous habitat when compared with adjacent nonhyperaccumulators .…”

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confidence: 99%

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Selenium Distribution and Speciation in the Hyperaccumulator Astragalus bisulcatus and Associated Ecological Partners

Barillas

Quinn²,

Freeman³

et al. 2012

Plant Physiology

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The goal of this study was to investigate how plant selenium (Se) hyperaccumulation may affect ecological interactions and whether associated partners may affect Se hyperaccumulation. The Se hyperaccumulator Astragalus bisulcatus was collected in its natural seleniferous habitat, and x-ray fluorescence mapping and x-ray absorption near-edge structure spectroscopy were used to characterize Se distribution and speciation in all organs as well as in encountered microbial symbionts and herbivores. Se was present at high levels (704–4,661 mg kg−1 dry weight) in all organs, mainly as organic C-Se-C compounds (i.e. Se bonded to two carbon atoms, e.g. methylselenocysteine). In nodule, root, and stem, up to 34% of Se was found as elemental Se, which was potentially due to microbial activity. In addition to a nitrogen-fixing symbiont, the plants harbored an endophytic fungus that produced elemental Se. Furthermore, two Se-resistant herbivorous moths were discovered on A. bisulcatus, one of which was parasitized by a wasp. Adult moths, larvae, and wasps all accumulated predominantly C-Se-C compounds. In conclusion, hyperaccumulators live in association with a variety of Se-resistant ecological partners. Among these partners, microbial endosymbionts may affect Se speciation in hyperaccumulators. Hyperaccumulators have been shown earlier to negatively affect Se-sensitive ecological partners while apparently offering a niche for Se-resistant partners. Through their positive and negative effects on different ecological partners, hyperaccumulators may influence species composition and Se cycling in seleniferous ecosystems.

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“…The hyperaccumulators Astragalus bisulcatus and Stanleya pinnata were found to predominantly accumulate Se in peripheral tissues of young leaves and reproductive organs: in structures important to protect, prone to herbivore and pathogen attacks, and/or typically associated with playing a defensive role (Pickering et al, 2003a;Freeman et al, 2006b;Galeas et al, 2007). Indeed, laboratory and field studies have shown that Se can protect plants from various herbivores and fungal pathogens (Vickerman and Trumble, 1999;Bañ uelos et al, 2002;Hanson et al, 2003Hanson et al, , 2004Freeman et al, 2006aFreeman et al, , 2007Freeman et al, , 2009Galeas et al, 2008;Quinn et al, 2008).…”

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Molecular Mechanisms of Selenium Tolerance and Hyperaccumulation in Stanleya pinnata

Freeman

Tamaoki²,

Stushnoff³

et al. 2010

Plant Physiol.

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The molecular mechanisms responsible for selenium (Se) tolerance and hyperaccumulation were studied in the Se hyperaccumulator Stanleya pinnata (Brassicaceae) by comparing it with the related secondary Se accumulator Stanleya albescens using a combination of physiological, structural, genomic, and biochemical approaches. S. pinnata accumulated 3.6-fold more Se and was tolerant to 20 mM selenate, while S. albescens suffered reduced growth, chlorosis and necrosis, impaired photosynthesis, and high levels of reactive oxygen species. Levels of ascorbic acid, glutathione, total sulfur, and nonprotein thiols were higher in S. pinnata, suggesting that Se tolerance may in part be due to increased antioxidants and up-regulated sulfur assimilation. S. pinnata had higher selenocysteine methyltransferase protein levels and, judged from liquid chromatography-mass spectrometry, mainly accumulated the free amino acid methylselenocysteine, while S. albescens accumulated mainly the free amino acid selenocystathionine. S. albescens leaf x-ray absorption near-edge structure scans mainly detected a carbon-Se-carbon compound (presumably selenocystathionine) in addition to some selenocysteine and selenate. Thus, S. albescens may accumulate more toxic forms of Se in its leaves than S. pinnata. The species also showed different leaf Se sequestration patterns: while S. albescens showed a diffuse pattern, S. pinnata sequestered Se in localized epidermal cell clusters along leaf margins and tips, concentrated inside of epidermal cells. Transcript analyses of S. pinnata showed a constitutively higher expression of genes involved in sulfur assimilation, antioxidant activities, defense, and response to (methyl)jasmonic acid, salicylic acid, or ethylene. The levels of some of these hormones were constitutively elevated in S. pinnata compared with S. albescens, and leaf Se accumulation was slightly enhanced in both species when these hormones were supplied. Thus, defense-related phytohormones may play an important signaling role in the Se hyperaccumulation of S. pinnata, perhaps by constitutively up-regulating sulfur/Se assimilation followed by methylation of selenocysteine and the targeted sequestration of methylselenocysteine.

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Selenium-Tolerant Diamondback Moth Disarms Hyperaccumulator Plant Defense

Cited by 122 publications

References 48 publications

Arsenic accumulation, biotransformation and localisation in bertha armyworm moths

Arsenic accumulation, biotransformation and localisation in bertha armyworm moths

Selenium Distribution and Speciation in the Hyperaccumulator Astragalus bisulcatus and Associated Ecological Partners

Molecular Mechanisms of Selenium Tolerance and Hyperaccumulation in Stanleya pinnata

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