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

John L Freeman,Colin F Quinn,Steve P Mcgrath,Elizabeth A H Pilon-Smits,Jean Devonshire,Sirine C Fakra,Matthew A Marcus,Martin Heil

doi:10.1371/journal.pone.0050516

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 γ-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.

Highlights

Selenium (Se) occurs naturally in certain soils, such as Cretaceous shale, at levels between 1 and 100 mg Se kg21 [1,2]
Micro-XRF mapping shows that in seeds of both S. pinnata and A. bisulcatus Se was mainly concentrated throughout the embryo and a much lower level was present in the seed coat (Fig. 1B, 1C)
Micro-XANES analysis revealed that the majority of Se (,63–100%) in both the S. pinnata and A. bisulcatus seeds was in C-Se-C forms, such as SeMet, MeSeCys, c-glutamylMeSeCys or seleno-cystathionine (Table 1)

Summary

Introduction

Selenium (Se) occurs naturally in certain soils, such as Cretaceous shale, at levels between 1 and 100 mg Se kg21 [1,2]. Some plant species grow almost exclusively on seleniferous soils, and are characterized by extremely high Se concentrations in their tissues, reaching levels between 0.1 and 1.5% of dry weight (1,000– 15,000 mg Se kg DW). These plants, called Se hyperaccumulators, typically contain 100-fold higher Se levels than surrounding vegetation [1,2]. Selenium hyperaccumulation defends plants via both deterrence and toxicity from a wide variety of herbivores (for a recent review see [3]). Selenium hyperaccumulator plants cause devastating Se toxicity to livestock (e.g., cows, sheep and horses) [10]

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Conclusion