title: 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 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.
authors.affiliation: Department of Biology, California State University Fresno, Fresno, California, United States of America. John.L.Freeman@NASA.gov
authors.forename: John L
authors.initials: JL
authors.lastname: Freeman
authors.forename: Matthew A
authors.initials: MA
authors.lastname: Marcus
authors.forename: Sirine C
authors.initials: SC
authors.lastname: Fakra
authors.forename: Jean
authors.initials: J
authors.lastname: Devonshire
authors.forename: Steve P
authors.initials: SP
authors.lastname: McGrath
authors.forename: Colin F
authors.initials: CF
authors.lastname: Quinn
authors.forename: Elizabeth A H
authors.initials: EA
authors.lastname: Pilon-Smits
mesh_terms: D000818:Animals; D027883:Astragalus Plant / Q000196:embryology / Q000378:metabolism* / Q000469:parasitology; D019607:Brassicaceae / Q000196:embryology / Q000378:metabolism* / Q000469:parasitology; D001517:Coleoptera / Q000502:physiology*; D012639:Seeds / Q000469:parasitology*; D012643:Selenium / Q000378:metabolism*; D014863:Wasps / Q000502:physiology*; D056928:X-Ray Absorption Spectroscopy
chemical_list: D012643:Selenium