Getting to the Root of Selenium Hyperaccumulation—Localization and Speciation of Root Selenium and Its Effects on Nematodes

Elemental hyperaccumulation protects plants from many aboveground herbivores. Little is known about effects of hyperaccumulation on belowground herbivores or their ecological interactions. To examine effects of plant selenium (Se) hyperaccumulation on nematode root herbivory, we investigated spatial...

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Main Authors: Christine N. Prins, Laura J. Hantzis, Jose R. Valdez-Barillas, Jennifer J. Cappa, Sirine C. Fakra, Cecilia Milano de Tomasel, Diana H. Wall, Elizabeth A. H. Pilon-Smits
Format: Article
Language:English
Published: MDPI AG 2019-07-01
Series:Soil Systems
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Online Access:https://www.mdpi.com/2571-8789/3/3/47
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author Christine N. Prins
Laura J. Hantzis
Jose R. Valdez-Barillas
Jennifer J. Cappa
Sirine C. Fakra
Cecilia Milano de Tomasel
Diana H. Wall
Elizabeth A. H. Pilon-Smits
author_facet Christine N. Prins
Laura J. Hantzis
Jose R. Valdez-Barillas
Jennifer J. Cappa
Sirine C. Fakra
Cecilia Milano de Tomasel
Diana H. Wall
Elizabeth A. H. Pilon-Smits
author_sort Christine N. Prins
collection DOAJ
description Elemental hyperaccumulation protects plants from many aboveground herbivores. Little is known about effects of hyperaccumulation on belowground herbivores or their ecological interactions. To examine effects of plant selenium (Se) hyperaccumulation on nematode root herbivory, we investigated spatial distribution and speciation of Se in hyperaccumulator roots using X-ray microprobe analysis, and effects of root Se concentration on root-associated nematode communities. Perennial hyperaccumulators <i>Stanleya pinnata</i> and <i>Astragalus bisulcatus</i>, collected from a natural seleniferous grassland contained 100&#8722;1500 mg Se kg<sup>&#8722;1</sup> root dry weight (DW). Selenium was concentrated in the cortex and epidermis of hyperaccumulator roots, with lower levels in the stele. The accumulated Se consisted of organic (C-Se-C) compounds, indistinguishable from methyl-selenocysteine. The field-collected roots yielded 5&#8722;400 nematodes g<sup>&#8722;1</sup> DW in Baermann funnel extraction, with no correlation between root Se concentration and nematode densities. Even roots containing &gt; 1000 mg Se kg<sup>&#8722;1</sup> DW yielded herbivorous nematodes. However, greenhouse-grown <i>S. pinnata</i> plants treated with Se had fewer total nematodes than those without Se. Thus, while root Se hyperaccumulation may protect plants from non-specialist herbivorous nematodes, Se-resistant nematode taxa appear to associate with hyperaccumulators in seleniferous habitats, and may utilize high-Se hyperaccumulator roots as food source. These findings give new insight into the ecological implications of plant Se (hyper)accumulation.
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spelling doaj.art-a29f9fd059724e4ebf927fdda975b7942022-12-22T02:58:04ZengMDPI AGSoil Systems2571-87892019-07-01334710.3390/soilsystems3030047soilsystems3030047Getting to the Root of Selenium Hyperaccumulation—Localization and Speciation of Root Selenium and Its Effects on NematodesChristine N. Prins0Laura J. Hantzis1Jose R. Valdez-Barillas2Jennifer J. Cappa3Sirine C. Fakra4Cecilia Milano de Tomasel5Diana H. Wall6Elizabeth A. H. Pilon-Smits7Biology Department, Colorado State University, Fort Collins, CO 80523-1878, USABiology Department, Colorado State University, Fort Collins, CO 80523-1878, USABiology Department, Colorado State University, Fort Collins, CO 80523-1878, USABiology Department, Colorado State University, Fort Collins, CO 80523-1878, USAAdvanced Light Source, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USABiology Department, Colorado State University, Fort Collins, CO 80523-1878, USABiology Department, Colorado State University, Fort Collins, CO 80523-1878, USABiology Department, Colorado State University, Fort Collins, CO 80523-1878, USAElemental hyperaccumulation protects plants from many aboveground herbivores. Little is known about effects of hyperaccumulation on belowground herbivores or their ecological interactions. To examine effects of plant selenium (Se) hyperaccumulation on nematode root herbivory, we investigated spatial distribution and speciation of Se in hyperaccumulator roots using X-ray microprobe analysis, and effects of root Se concentration on root-associated nematode communities. Perennial hyperaccumulators <i>Stanleya pinnata</i> and <i>Astragalus bisulcatus</i>, collected from a natural seleniferous grassland contained 100&#8722;1500 mg Se kg<sup>&#8722;1</sup> root dry weight (DW). Selenium was concentrated in the cortex and epidermis of hyperaccumulator roots, with lower levels in the stele. The accumulated Se consisted of organic (C-Se-C) compounds, indistinguishable from methyl-selenocysteine. The field-collected roots yielded 5&#8722;400 nematodes g<sup>&#8722;1</sup> DW in Baermann funnel extraction, with no correlation between root Se concentration and nematode densities. Even roots containing &gt; 1000 mg Se kg<sup>&#8722;1</sup> DW yielded herbivorous nematodes. However, greenhouse-grown <i>S. pinnata</i> plants treated with Se had fewer total nematodes than those without Se. Thus, while root Se hyperaccumulation may protect plants from non-specialist herbivorous nematodes, Se-resistant nematode taxa appear to associate with hyperaccumulators in seleniferous habitats, and may utilize high-Se hyperaccumulator roots as food source. These findings give new insight into the ecological implications of plant Se (hyper)accumulation.https://www.mdpi.com/2571-8789/3/3/47<i>Astragalus bisulcatus</i>elemental defenseherbivory<i>Stanleya pinnata</i>
spellingShingle Christine N. Prins
Laura J. Hantzis
Jose R. Valdez-Barillas
Jennifer J. Cappa
Sirine C. Fakra
Cecilia Milano de Tomasel
Diana H. Wall
Elizabeth A. H. Pilon-Smits
Getting to the Root of Selenium Hyperaccumulation—Localization and Speciation of Root Selenium and Its Effects on Nematodes
Soil Systems
<i>Astragalus bisulcatus</i>
elemental defense
herbivory
<i>Stanleya pinnata</i>
title Getting to the Root of Selenium Hyperaccumulation—Localization and Speciation of Root Selenium and Its Effects on Nematodes
title_full Getting to the Root of Selenium Hyperaccumulation—Localization and Speciation of Root Selenium and Its Effects on Nematodes
title_fullStr Getting to the Root of Selenium Hyperaccumulation—Localization and Speciation of Root Selenium and Its Effects on Nematodes
title_full_unstemmed Getting to the Root of Selenium Hyperaccumulation—Localization and Speciation of Root Selenium and Its Effects on Nematodes
title_short Getting to the Root of Selenium Hyperaccumulation—Localization and Speciation of Root Selenium and Its Effects on Nematodes
title_sort getting to the root of selenium hyperaccumulation localization and speciation of root selenium and its effects on nematodes
topic <i>Astragalus bisulcatus</i>
elemental defense
herbivory
<i>Stanleya pinnata</i>
url https://www.mdpi.com/2571-8789/3/3/47
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