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Selenium hyperaccumulator plants Stanleya pinnata and Astragalus bisulcatus are colonized by Se-resistant, Se-excluding wasp and beetle seed herbivores.

ABSTRACT: Selenium (Se) hyperaccumulator plants can concentrate the toxic element Se up to 1% of shoot (DW) which is known to protect hyperaccumulator plants from generalist herbivores. There is evidence for Se-resistant insect herbivores capable of feeding upon hyperaccumulators. In this study, resistance to Se was investigated in seed chalcids and seed beetles found consuming seeds inside pods of Se-hyperaccumulator species Astragalus bisulcatus and Stanleya pinnata. Selenium accumulation, localization and speciation were determined in seeds collected from hyperaccumulators in a seleniferous habitat and in seed herbivores. Astragalus bisulcatus seeds were consumed by seed beetle larvae (Acanthoscelides fraterculus Horn, Coleoptera: Bruchidae) and seed chalcid larvae (Bruchophagus mexicanus, Hymenoptera: Eurytomidae). Stanleya pinnata seeds were consumed by an unidentified seed chalcid larva. Micro X-ray absorption near-edge structure (µXANES) and micro-X-Ray Fluorescence mapping (µXRF) demonstrated Se was mostly organic C-Se-C forms in seeds of both hyperaccumulators, and S. pinnata seeds contained ?24% elemental Se. Liquid chromatography-mass spectrometry of Se-compounds in S. pinnata seeds detected the C-Se-C compound seleno-cystathionine while previous studies of A. bisulcatus seeds detected the C-Se-C compounds methyl-selenocysteine and ?-glutamyl-methyl-selenocysteine. Micro-XRF and µXANES revealed Se ingested from hyperaccumulator seeds redistributed throughout seed herbivore tissues, and portions of seed C-Se-C were biotransformed into selenocysteine, selenocystine, selenodiglutathione, selenate and selenite. Astragalus bisulcatus seeds contained on average 5,750 µg Se g(-1), however adult beetles and adult chalcid wasps emerging from A. bisulcatus seed pods contained 4-6 µg Se g(-1). Stanleya pinnata seeds contained 1,329 µg Se g(-1) on average; however chalcid wasp larvae and adults emerging from S. pinnata seed pods contained 9 and 47 µg Se g(-1). The results suggest Se resistant seed herbivores exclude Se, greatly reducing tissue accumulation; this explains their ability to consume high-Se seeds without suffering toxicity, allowing them to occupy the unique niche offered by Se hyperaccumulator plants.

SUBMITTER: Freeman JL

PROVIDER: S-EPMC3513300 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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Selenium hyperaccumulator plants Stanleya pinnata and Astragalus bisulcatus are colonized by Se-resistant, Se-excluding wasp and beetle seed herbivores.

Freeman John L JL Marcus Matthew A MA Fakra Sirine C SC Devonshire Jean J McGrath Steve P SP Quinn Colin F CF Pilon-Smits Elizabeth A H EA

PloS one 20121203 12

Selenium (Se) hyperaccumulator plants can concentrate the toxic element Se up to 1% of shoot (DW) which is known to protect hyperaccumulator plants from generalist herbivores. There is evidence for Se-resistant insect herbivores capable of feeding upon hyperaccumulators. In this study, resistance to Se was investigated in seed chalcids and seed beetles found consuming seeds inside pods of Se-hyperaccumulator species Astragalus bisulcatus and Stanleya pinnata. Selenium accumulation, localization ...[more]

PMID: 23226523

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Project description:BackgroundThe dung beetle Phelotrupes auratus is a holometabolous insect belonging to the order Coleoptera, and it is widely distributed in Japan. The P. auratus habitat depends on herbivores. P. auratus eats the dung of the herbivores and carries it underground for its young. In this process, herbivore droppings disappear from the ground, not only keeping the ground hygienic but also maintaining good soil conditions for plant growth. In this way, a rich ecosystem is maintained. In recent years, the population of P. auratus has decreased, and the main cause has been the decrease in grazing land. It seems that Japanese dung beetles are mainly dependent on herbivores for nutrient sources. However, the physiological relationship between herbivores and P. auratus has not been well investigated. Here, we investigated the nutritional metabolism system of P. auratus by performing whole gene expression analysis of individuals collected from two areas where the ecosystem is occupied by different herbivores.ResultsWe obtained 54,635 transcripts from P. auratus from Nara Park and Cape Toi and identified 2,592 differentially expressed genes in the fat bodies of the Nara Park and Cape Toi groups. We annotated P. auratus transcripts using Homo sapiens and Drosophila melanogaster genes as references; 50.5% of P. auratus transcripts were assigned to H. sapiens genes, and 54.0% of P. auratus transcripts were assigned to D. melanogaster genes. To perform gene set enrichment analysis, we chose H. sapiens genes for P. auratus transcript annotation. Principal component analysis and gene set enrichment analysis revealed that the nutritional metabolism of P. auratus from Cape Toi might differ from that of P. auratus from Nara Park.ConclusionWe analyzed the nutritional metabolism system of P. auratus from Cape Toi and Nara Park and found that the characteristics of the nutritional metabolism process might depend on the plants consumed by the herbivores. Our findings will contribute to elucidating the relationships among habitat plants, herbivores, and dung decomposers and may aid in the maintenance of sustainable land health cycles.

Dataset Information

Selenium hyperaccumulator plants Stanleya pinnata and Astragalus bisulcatus are colonized by Se-resistant, Se-excluding wasp and beetle seed herbivores.

Publications

Selenium hyperaccumulator plants Stanleya pinnata and Astragalus bisulcatus are colonized by Se-resistant, Se-excluding wasp and beetle seed herbivores.

Similar Datasets

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