DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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 (mXANES) and micro-X-Ray Fluorescence mapping (mXRF) 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 Secompounds 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 c-glutamyl-methyl-selenocysteine. Micro-XRF and mXANES revealed Se ingested from hyperaccumulator seeds redistributed throughout seed herbivore tissues, and portions of seed C-Se-C were biotransformed into selenocysteine,more » selenocystine, selenodiglutathione, selenate and selenite. Astragalus bisulcatus seeds contained on average 5,750 mg Se g21 , however adult beetles and adult chalcid wasps emerging from A. bisulcatus seed pods contained 4–6 mg Se g21 . Stanleya pinnata seeds contained 1,329 mg Se g21 on average; however chalcid wasp larvae and adults emerging from S. pinnata seed pods contained 9 and 47 mg Se g21 . 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.« less

Authors:
 [1];  [2];  [2];  [3];  [3];  [4];  [4]
  1. California State Univ. (CalState), Fresno, CA (United States). Dept. of Biology; NASA Ames Research Center (ARC), Moffett Field, Mountain View, CA (United States). Intrinsyx Technologies Corporation and Space Biosciences
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Advanced Light Source (ALS)
  3. Rothamsted Research, Harpenden, Hertfordshire (United Kingdom)
  4. Colorado State Univ., Fort Collins, CO (United States). Biology Dept.
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Earth and Environmental Systems Science Division
OSTI Identifier:
1627564
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 7; Journal Issue: 12; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Science & Technology - Other Topics

Citation Formats

Freeman, John L., Marcus, Matthew A., Fakra, Sirine C., Devonshire, Jean, McGrath, Steve P., Quinn, Colin F., and Pilon-Smits, Elizabeth A. H. Selenium Hyperaccumulator Plants Stanleya pinnata and Astragalus bisulcatus Are Colonized by Se-Resistant, Se-Excluding Wasp and Beetle Seed Herbivores. United States: N. p., 2012. Web. doi:10.1371/journal.pone.0050516.
Freeman, John L., Marcus, Matthew A., Fakra, Sirine C., Devonshire, Jean, McGrath, Steve P., Quinn, Colin F., & Pilon-Smits, Elizabeth A. H. Selenium Hyperaccumulator Plants Stanleya pinnata and Astragalus bisulcatus Are Colonized by Se-Resistant, Se-Excluding Wasp and Beetle Seed Herbivores. United States. https://doi.org/10.1371/journal.pone.0050516
Freeman, John L., Marcus, Matthew A., Fakra, Sirine C., Devonshire, Jean, McGrath, Steve P., Quinn, Colin F., and Pilon-Smits, Elizabeth A. H. Mon . "Selenium Hyperaccumulator Plants Stanleya pinnata and Astragalus bisulcatus Are Colonized by Se-Resistant, Se-Excluding Wasp and Beetle Seed Herbivores". United States. https://doi.org/10.1371/journal.pone.0050516. https://www.osti.gov/servlets/purl/1627564.
@article{osti_1627564,
title = {Selenium Hyperaccumulator Plants Stanleya pinnata and Astragalus bisulcatus Are Colonized by Se-Resistant, Se-Excluding Wasp and Beetle Seed Herbivores},
author = {Freeman, John L. and Marcus, Matthew A. and Fakra, Sirine C. and Devonshire, Jean and McGrath, Steve P. and Quinn, Colin F. and Pilon-Smits, Elizabeth A. H.},
abstractNote = {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 (mXANES) and micro-X-Ray Fluorescence mapping (mXRF) 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 Secompounds 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 c-glutamyl-methyl-selenocysteine. Micro-XRF and mXANES 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 mg Se g21 , however adult beetles and adult chalcid wasps emerging from A. bisulcatus seed pods contained 4–6 mg Se g21 . Stanleya pinnata seeds contained 1,329 mg Se g21 on average; however chalcid wasp larvae and adults emerging from S. pinnata seed pods contained 9 and 47 mg Se g21 . 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.},
doi = {10.1371/journal.pone.0050516},
journal = {PLoS ONE},
number = 12,
volume = 7,
place = {United States},
year = {Mon Dec 03 00:00:00 EST 2012},
month = {Mon Dec 03 00:00:00 EST 2012}
}

Works referenced in this record:

The Use of Indicator Plants in Locating Seleniferous Areas in Western United States. I. General
journal, April 1939

  • Beath, O. A.; Gilbert, C. S.; Eppson, H. F.
  • American Journal of Botany, Vol. 26, Issue 4
  • DOI: 10.2307/2436499

The Use of Indicatior Plants in Locating Seleniferous Areas in Western United States. II. Correlation Studies by States
journal, May 1939

  • Beath, O. A.; Gilbert, C. S.; Eppson, H. F.
  • American Journal of Botany, Vol. 26, Issue 5
  • DOI: 10.2307/2436464

Ecological aspects of plant selenium hyperaccumulation: Ecology of selenium hyperaccumulation
journal, December 2011


Selenium protects the hyperaccumulator Stanleya pinnata against black-tailed prairie dog herbivory in native seleniferous habitats
journal, June 2009

  • Freeman, John L.; Quinn, Colin F.; Lindblom, Stormy Dawn
  • American Journal of Botany, Vol. 96, Issue 6
  • DOI: 10.3732/ajb.0800287

Selenium protects plants from phloem-feeding aphids due to both deterrence and toxicity
journal, June 2004


Selenium accumulation protects Brassica juncea from invertebrate herbivory and fungal infection
journal, August 2003


Selenium accumulation protects plants from herbivory by Orthoptera via toxicity and deterrence
journal, August 2007


Selenium hyperaccumulation reduces plant arthropod loads in the field
journal, February 2008


Toxicology of selenium: A review
journal, January 1980


Selenium uptake, translocation, assimilation and metabolic fate in plants
journal, November 2005


Selenium Biochemistry
journal, June 1990


Spatial Imaging, Speciation, and Quantification of Selenium in the Hyperaccumulator Plants Astragalus bisulcatus and Stanleya pinnata
journal, August 2006

  • Freeman, John L.; Zhang, Li Hong; Marcus, Matthew A.
  • Plant Physiology, Vol. 142, Issue 1
  • DOI: 10.1104/pp.106.081158

Molecular Mechanisms of Selenium Tolerance and Hyperaccumulation in Stanleya pinnata
journal, May 2010

  • Freeman, John L.; Tamaoki, Masanori; Stushnoff, Cecil
  • Plant Physiology, Vol. 153, Issue 4
  • DOI: 10.1104/pp.110.156570

Selenium accumulation in flowers and its effects on pollination
journal, July 2011


Influence of microbial associations on selenium localization and speciation in roots of Astragalus and Stanleya hyperaccumulators
journal, April 2013


Selenium-Tolerant Diamondback Moth Disarms Hyperaccumulator Plant Defense
journal, November 2006


Seasonal fluctuations of selenium and sulfur accumulation in selenium hyperaccumulators and related nonaccumulators
journal, November 2006


Seleno amino compounds from Astragalus bisulcatus isolation and identification of γ-L-glutamyl-Se-methyl-seleno-L-cysteine and Se-methylseleno-L-cysteine
journal, November 1969

  • Nigam, S. N.; McConnell, W. B.
  • Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 192, Issue 2
  • DOI: 10.1016/0304-4165(69)90354-7

Toxicity to Insects and Mammals of Foods Containing Selenium
journal, July 1937

  • Trelease, Sam F.; Trelease, Helen M.
  • American Journal of Botany, Vol. 24, Issue 7
  • DOI: 10.2307/2436430

Quantitative Elemental Analyses by Plasma Emission Spectroscopy
journal, October 1978


Nitric acid digestion and multi‐element analysis of plant material by inductively coupled plasma spectrometry
journal, January 1987

  • Zarcinas, B. A.; Cartwright, B.; Spouncer, L. R.
  • Communications in Soil Science and Plant Analysis, Vol. 18, Issue 1
  • DOI: 10.1080/00103628709367806

Beamline 10.3.2 at ALS: a hard X-ray microprobe for environmental and materials sciences
journal, April 2004

  • Marcus, Matthew A.; MacDowell, Alastair A.; Celestre, Richard
  • Journal of Synchrotron Radiation, Vol. 11, Issue 3
  • DOI: 10.1107/S0909049504005837

Aspects of Selenium Metabolism in Higher Plants
journal, June 1969


Reduction of Selenite to Elemental Red Selenium by Rhizobium sp. Strain B1
journal, July 2007


Changes in Selenium Speciation Associated with Increasing Tissue Concentrations of Selenium in Wheat Grain
journal, February 2010

  • Cubadda, Francesco; Aureli, Federica; Ciardullo, Silvia
  • Journal of Agricultural and Food Chemistry, Vol. 58, Issue 4
  • DOI: 10.1021/jf903004a

Tooth hardness increases with zinc-content in mandibles of young adult leaf-cutter ants
journal, December 2002

  • Schofield, Robert M. S.; Nesson, Michael H.; Richardson, Kathleen A.
  • Naturwissenschaften, Vol. 89, Issue 12
  • DOI: 10.1007/s00114-002-0381-4

Toxicity to Insects and Mammals of Foods Containing Selenium
journal, July 1937


The use of Indicator Plants in Locating Seleniferous Areas in Western United States. ii. Correlation Studies by States
journal, May 1939


The use of Indicator Plants in Locating Seleniferous Areas in Western United States. i. General
journal, April 1939


Reduction of selenium oxyanions by unicellular, polymorphic and filamentous fungi: Cellular location of reduced selenium and implications for tolerance
journal, March 1995

  • Gharieb, M. M.; Wilkinson, S. C.; Gadd, G. M.
  • Journal of Industrial Microbiology, Vol. 14, Issue 3-4
  • DOI: 10.1007/bf01569943

Reduction of Selenite to Elemental Red Selenium by Rhizobium sp. Strain B1
journal, July 2007


Seleno amino compounds from Astragalus bisulcatus isolation and identification of γ-L-glutamyl-Se-methyl-seleno-L-cysteine and Se-methylseleno-L-cysteine
journal, November 1969

  • Nigam, S. N.; McConnell, W. B.
  • Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 192, Issue 2
  • DOI: 10.1016/0304-4165(69)90354-7

Evolution: The Ecological Reverberations of Toxic Trace Elements
journal, November 2006


Nitric acid digestion and multi‐element analysis of plant material by inductively coupled plasma spectrometry
journal, January 1987

  • Zarcinas, B. A.; Cartwright, B.; Spouncer, L. R.
  • Communications in Soil Science and Plant Analysis, Vol. 18, Issue 1
  • DOI: 10.1080/00103628709367806

Molecular Mechanisms of Selenium Tolerance and Hyperaccumulation in Stanleya pinnata
journal, May 2010

  • Freeman, John L.; Tamaoki, Masanori; Stushnoff, Cecil
  • Plant Physiology, Vol. 153, Issue 4
  • DOI: 10.1104/pp.110.156570

Seasonal fluctuations of selenium and sulfur accumulation in selenium hyperaccumulators and related nonaccumulators
journal, November 2006


Selenium and the elemental defense hypothesis
journal, January 2008


Selenium accumulation in flowers and its effects on pollination
journal, July 2011


Selenium Biochemistry
journal, June 1990


Aspects of Selenium Metabolism in Higher Plants
journal, June 1969


Toxicology of selenium: A review
journal, January 1980


Selenium protects the hyperaccumulator Stanleya pinnata against black-tailed prairie dog herbivory in native seleniferous habitats
journal, June 2009

  • Freeman, John L.; Quinn, Colin F.; Lindblom, Stormy Dawn
  • American Journal of Botany, Vol. 96, Issue 6
  • DOI: 10.3732/ajb.0800287

Works referencing / citing this record:

Selenium in Plants
book, August 2014


Phytoremediation of the Metalloid Selenium in Soil and Water
book, January 2015


Evolutionary aspects of elemental hyperaccumulation
journal, October 2013


Elemental defense of nickel hyperaccumulator seeds against a generalist insect granivore
journal, March 2018


The fascinating facets of plant selenium accumulation – biochemistry, physiology, evolution and ecology
journal, November 2016

  • Schiavon, Michela; Pilon‐Smits, Elizabeth A. H.
  • New Phytologist, Vol. 213, Issue 4
  • DOI: 10.1111/nph.14378

Selenium Biofortification and Phytoremediation Phytotechnologies: A Review
journal, January 2017

  • Schiavon, Michela; Pilon-Smits, Elizabeth A. H.
  • Journal of Environment Quality, Vol. 46, Issue 1
  • DOI: 10.2134/jeq2016.09.0342

Effect of Selenium on Control of Postharvest Gray Mold of Tomato Fruit and the Possible Mechanisms Involved
journal, January 2016


On the Ecology of Selenium Accumulation in Plants
journal, June 2019


Getting to the Root of Selenium Hyperaccumulation—Localization and Speciation of Root Selenium and Its Effects on Nematodes
journal, July 2019


Selenium in Plants
journal, July 1879


Selenium tolerance, accumulation, localization and speciation in a Cardamine hyperaccumulator and a non-hyperaccumulator
journal, February 2020


The defensive benefit and flower number cost of selenium accumulation in Brassica juncea
journal, August 2019


Effect of Selenium on Control of Postharvest Gray Mold of Tomato Fruit and the Possible Mechanisms Involved
journal, January 2016


On the Ecology of Selenium Accumulation in Plants
journal, June 2019