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Title: Selenium hyperaccumulation offers protection from cell disruptor herbivores

Abstract

Background: Hyperaccumulation, the rare capacity of certain plant species to accumulate toxic trace elements to levels several orders of magnitude higher than other species growing on the same site, is thought to be an elemental defense mechanism against herbivores and pathogens. Previous research has shown that selenium (Se) hyperaccumulation protects plants from a variety of herbivores and pathogens. Selenium hyperaccumulating plants sequester Se in discrete locations in the leaf periphery, making them potentially more susceptible to some herbivore feeding modes than others. In this study we investigate the protective function of Se in the Se hyperaccumulators Stanleya pinnata and Astragalus bisulcatus against two cell disrupting herbivores, the western flower thrips (Frankliniella occidentalis) and the two-spotted spider mite (Tetranychus urticae). Results: Astragalus bisulcatus and S. pinnata with high Se concentrations (greater than 650 mg Se kg-1) were less subject to thrips herbivory than plants with low Se levels (less than 150 mg Se kg-1). Furthermore, in plants containing elevated Se levels, leaves with higher concentrations of Se suffered less herbivory than leaves with less Se. Spider mites also preferred to feed on low-Se A. bisulcatus and S. pinnata plants rather than high-Se plants. Spider mite populations on A. bisulcatus decreased aftermore » plants were given a higher concentration of Se. Interestingly, spider mites could colonize A. bisulcatus plants containing up to 200 mg Se kg-1 dry weight, concentrations which are toxic to many other herbivores. Selenium distribution and speciation studies using microfocused X-ray fluorescence (μXRF) mapping and Se K-edge X-ray absorption spectroscopy revealed that the spider mites accumulated primarily methylselenocysteine, the relatively non-toxic form of Se that is also the predominant form of Se in hyperaccumulators. Conclusions: This is the first reported study investigating the protective effect of hyperaccumulated Se against cell-disrupting herbivores. The finding that Se protected the two hyperaccumulator species from both cell disruptors lends further support to the elemental defense hypothesis and increases the number of herbivores and feeding modes against which Se has shown a protective effect. Because western flower thrips and two-spotted spider mites are widespread and economically important herbivores, the results from this study also have potential applications in agriculture or horticulture, and implications for the management of Se-rich crops.« less

Authors:
 [1];  [2];  [1];  [1];  [3];  [3];  [1];  [1];  [1];  [1]
  1. Colorado State Univ., Fort Collins, CO (United States). Dept. of Biology
  2. Colorado State Univ., Fort Collins, CO (United States). Dept. of Biology; U.S. Department of Agriculture, Parlier, CA (United States). Agricultural Research Service (ARS); California State Univ. (CalState), Fresno, CA (United States). Center for Irrigation Technology
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Advanced Light Source (ALS)
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). Biological Systems Science Division; National Science Foundation (NSF)
OSTI Identifier:
1629612
Grant/Contract Number:  
AC02-05CH11231; IOB-0444471; IOS-0817748
Resource Type:
Accepted Manuscript
Journal Name:
BMC Ecology (Online)
Additional Journal Information:
Journal Name: BMC Ecology (Online); Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 1472-6785
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Quinn, Colin F., Freeman, John L., Reynolds, Ray JB, Cappa, Jennifer J., Fakra, Sirine C., Marcus, Matthew A., Lindblom, Stormy D., Quinn, Erin K., Bennett, Lindsay E., and Pilon-Smits, Elizabeth AH. Selenium hyperaccumulation offers protection from cell disruptor herbivores. United States: N. p., 2010. Web. doi:10.1186/1472-6785-10-19.
Quinn, Colin F., Freeman, John L., Reynolds, Ray JB, Cappa, Jennifer J., Fakra, Sirine C., Marcus, Matthew A., Lindblom, Stormy D., Quinn, Erin K., Bennett, Lindsay E., & Pilon-Smits, Elizabeth AH. Selenium hyperaccumulation offers protection from cell disruptor herbivores. United States. https://doi.org/10.1186/1472-6785-10-19
Quinn, Colin F., Freeman, John L., Reynolds, Ray JB, Cappa, Jennifer J., Fakra, Sirine C., Marcus, Matthew A., Lindblom, Stormy D., Quinn, Erin K., Bennett, Lindsay E., and Pilon-Smits, Elizabeth AH. Fri . "Selenium hyperaccumulation offers protection from cell disruptor herbivores". United States. https://doi.org/10.1186/1472-6785-10-19. https://www.osti.gov/servlets/purl/1629612.
@article{osti_1629612,
title = {Selenium hyperaccumulation offers protection from cell disruptor herbivores},
author = {Quinn, Colin F. and Freeman, John L. and Reynolds, Ray JB and Cappa, Jennifer J. and Fakra, Sirine C. and Marcus, Matthew A. and Lindblom, Stormy D. and Quinn, Erin K. and Bennett, Lindsay E. and Pilon-Smits, Elizabeth AH},
abstractNote = {Background: Hyperaccumulation, the rare capacity of certain plant species to accumulate toxic trace elements to levels several orders of magnitude higher than other species growing on the same site, is thought to be an elemental defense mechanism against herbivores and pathogens. Previous research has shown that selenium (Se) hyperaccumulation protects plants from a variety of herbivores and pathogens. Selenium hyperaccumulating plants sequester Se in discrete locations in the leaf periphery, making them potentially more susceptible to some herbivore feeding modes than others. In this study we investigate the protective function of Se in the Se hyperaccumulators Stanleya pinnata and Astragalus bisulcatus against two cell disrupting herbivores, the western flower thrips (Frankliniella occidentalis) and the two-spotted spider mite (Tetranychus urticae). Results: Astragalus bisulcatus and S. pinnata with high Se concentrations (greater than 650 mg Se kg-1) were less subject to thrips herbivory than plants with low Se levels (less than 150 mg Se kg-1). Furthermore, in plants containing elevated Se levels, leaves with higher concentrations of Se suffered less herbivory than leaves with less Se. Spider mites also preferred to feed on low-Se A. bisulcatus and S. pinnata plants rather than high-Se plants. Spider mite populations on A. bisulcatus decreased after plants were given a higher concentration of Se. Interestingly, spider mites could colonize A. bisulcatus plants containing up to 200 mg Se kg-1 dry weight, concentrations which are toxic to many other herbivores. Selenium distribution and speciation studies using microfocused X-ray fluorescence (μXRF) mapping and Se K-edge X-ray absorption spectroscopy revealed that the spider mites accumulated primarily methylselenocysteine, the relatively non-toxic form of Se that is also the predominant form of Se in hyperaccumulators. Conclusions: This is the first reported study investigating the protective effect of hyperaccumulated Se against cell-disrupting herbivores. The finding that Se protected the two hyperaccumulator species from both cell disruptors lends further support to the elemental defense hypothesis and increases the number of herbivores and feeding modes against which Se has shown a protective effect. Because western flower thrips and two-spotted spider mites are widespread and economically important herbivores, the results from this study also have potential applications in agriculture or horticulture, and implications for the management of Se-rich crops.},
doi = {10.1186/1472-6785-10-19},
journal = {BMC Ecology (Online)},
number = 1,
volume = 10,
place = {United States},
year = {Fri Aug 27 00:00:00 EDT 2010},
month = {Fri Aug 27 00:00:00 EDT 2010}
}

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Pests
book, January 1986


The role of selenium in protecting plants against prairie dog herbivory: implications for the evolution of selenium hyperaccumulation
journal, November 2007


Protection against reactive oxygen species by selenoproteins
journal, November 2009

  • Steinbrenner, Holger; Sies, Helmut
  • Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1790, Issue 11
  • DOI: 10.1016/j.bbagen.2009.02.014

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


Deterrence of herbivory by zinc hyperaccumulation in Thlaspi caerulescens (Brassicaceae)
journal, April 1997


Ecotypic variation in selenium accumulation among populations of Stanleya pinnata
journal, January 2001


Plant resistance towards insect herbivores: a dynamic interaction
journal, November 2002


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


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

Selenium Decreases Thyroid Cancer Cell Growth by Increasing Expression of GADD153 and GADD34
journal, December 2009

  • Kato, Meredith A.; Finley, David J.; Lubitz, Carrie C.
  • Nutrition and Cancer, Vol. 62, Issue 1
  • DOI: 10.1080/01635580903191569

Field Reversion of Organotin Resistance in the Twospotted Spider Mite (Acari: Tetranychidae) Following Relaxation of Selection Pressure
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Western Flower Thrips (Thysanoptera: Thripidae) Resistance to Insecticides in Coastal California Greenhouses
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Spatial Imaging, Speciation, and Quantification of Selenium in the Hyperaccumulator Plants Astragalus bisulcatus and Stanleya pinnata
journal, August 2006

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  • DOI: 10.1104/pp.106.081158

Habitat-specific population structure in native western flower thrips Frankliniella occidentalis (Insecta, Thysanoptera)
journal, April 2010


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


Palatability of Thlaspi caerulescens for snails: influence of zinc and glucosinolates
journal, December 2004


Nickel hyperaccumulation as an elemental defense of Streptanthus polygaloides (Brassicaceae): influence of herbivore feeding mode
journal, July 2005


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


Arsenic hyperaccumulation in the Chinese brake fern ( Pteris vittata ) deters grasshopper ( Schistocerca americana ) herbivory
journal, April 2007


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


Quantitative Elemental Analyses by Plasma Emission Spectroscopy
journal, October 1978


Selenium Biochemistry
journal, June 1990


Herbivore Offense
journal, November 2002


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

Decline of photosynthetic capacity with leaf age and position in two tropical pioneer tree species
journal, December 2002

  • Kitajima, Kaoru; Mulkey, Stephen S.; Samaniego, Mirna
  • American Journal of Botany, Vol. 89, Issue 12
  • DOI: 10.3732/ajb.89.12.1925

Biomass crops can be used for biological disinfestation and remediation of soils and water
journal, May 2008

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  • DOI: 10.3733/ca.v063n01p41

Enhanced lung cancer cell killing by the combination of selenium and ionizing radiation
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Works referencing / citing this record:

Prediction of Agro-Morphological and Nutritional Traits in Ethiopian Mustard Leaves (Brassica Carinata A. Braun) by Visible-Near-Infrared Spectroscopy
journal, December 2018

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Effect of Selenium on Control of Postharvest Gray Mold of Tomato Fruit and the Possible Mechanisms Involved
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Molecular basis of natural variation and environmental control of trichome patterning
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Selenium hyperaccumulators harbor a diverse endophytic bacterial community characterized by high selenium resistance and plant growth promoting properties
journal, March 2015

  • Sura-de Jong, Martina; Reynolds, Ray J. B.; Richterova, Klara
  • Frontiers in Plant Science, Vol. 6
  • DOI: 10.3389/fpls.2015.00113

An Overview of Selenium Uptake, Metabolism, and Toxicity in Plants
journal, January 2017


Effect of Cadmium Accumulation on the Performance of Plants and of Herbivores That Cope Differently With Organic Defenses
journal, November 2018

  • Godinho, Diogo Prino; Serrano, Helena Cristina; Da Silva, Anabela Bernardes
  • Frontiers in Plant Science, Vol. 9
  • DOI: 10.3389/fpls.2018.01723

Prediction of Agro-Morphological and Nutritional Traits in Ethiopian Mustard Leaves (Brassica Carinata A. Braun) by Visible-Near-Infrared Spectroscopy
journal, December 2018

  • Martínez-Valdivieso, Damián; Font, Rafael; Del Río-Celestino, Mercedes
  • Foods, Vol. 8, Issue 1
  • DOI: 10.3390/foods8010006

Selenium Enrichment of Horticultural Crops
journal, June 2017


Selenium Cycling Across Soil-Plant-Atmosphere Interfaces: A Critical Review
journal, May 2015

  • Winkel, Lenny; Vriens, Bas; Jones, Gerrad
  • Nutrients, Vol. 7, Issue 6
  • DOI: 10.3390/nu7064199