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Ecological aspects of plant selenium hyperaccumulation: effects of selenium hyperaccumulation on plant-plant interactions




Mehdawi, Ali Farag El, author
Pilon-Smits, Elizabeth, advisor
Pilon, Marinus, committee member
Paschke, Mark, committee member
Vivanco, Jorge, committee member

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Hyperaccumulators are plants that accumulate toxic elements to extraordinary levels. Selenium (Se) hyperaccumulators such as Astragalus bisulcatus and Stanleya pinnata can contain 0.1-1.5% of their dry weight in Se (1,000 - 15,000 mg Se kg-1 DW), levels toxic to most other organisms. Selenium promotes hyperaccumulator growth and also offers the plant several ecological advantages through negative effects on Se-sensitive partners. Previous work has shown that high tissue Se levels reduce herbivory and pathogen infection. On the other hand, hyperaccumulators may offer an exclusive niche for Se-tolerant ecological partners. The focus of this dissertation study was on the effects of Se hyperaccumulation on plant-plant interactions. The first Chapter presents a literature review of the phenomenon of Se hyperaccumulation, how Se hyperaccumulators are different from other plants, and an overview of previous studies on the effects of hyperaccumulated Se on ecological processes related to herbivore-plant interactions, microbe-plant interactions and pollinator-plant interactions. In addition, evolutionary aspects of Se hyperaccumulation are discussed, and their implications for their ecological partners. The findings presented in this overview formed the platform for the experiments carried out in this dissertation research, on the topic of plant-plant interactions. In Chapter 2, experiments are described to address the question whether Se hyperaccumulation can negatively affect neighboring plants. Soil collected around hyperaccumulators on a seleniferous field site was measured and shown to contain more Se (up to 266 mg Se kg-1) than soil around non-hyperaccumulators. Vegetative ground cover was somewhat lower around Se hyperaccumulators compared to non-hyperaccumulators. Thus, Se hyperaccumulators may increase surrounding soil Se concentration (phytoenrichment). The enhanced soil Se levels around hyperaccumulators were shown to impair growth of a Se-sensitive plant species, Arabidopsis thaliana, pointing to a possible role of Se hyperaccumulation in elemental allelopathy. In Chapter 3, potential positive effects of hyperaccumulator Se on neighboring plants are explored. It was found for two plant species, Artemisia ludoviciana and Symphyotrichum ericoides, that growing next to Se hyperaccumulators increased their Se content 10-20 fold (up to 800-2,000 mg Se kg-1 DW) compared to when they were growing next to non-accumulators. Moreover, these neighbors of hyperaccumulators were 2-fold bigger, showed 2-fold less herbivory damage and harbored 3-4 fold fewer arthropods than when growing next to non-hyperaccumulators. When used in laboratory choice and non-choice grasshopper herbivory experiments, Se-rich neighbors of hyperaccumulators experienced less herbivory and caused higher grasshopper Se accumulation (10-fold) and mortality (4-fold). These results suggest that Se hyperaccumulators can facilitate the growth of Se-tolerant neighboring plants. The fourth Chapter describes a more controlled greenhouse pot cocultivation study that investigated how Se affects relationships between Se hyperaccumulators (A. bisulcatus and S. pinnata) and related non-accumulator species (A. drummondii and S. elata), in terms of how these plants influence their neighbor’s Se accumulation and growth. Selenium affected growth differently in hyperaccumulators and nonaccumulators: The hyperaccumulators performed 2.5-fold better on seleniferous than non-seleniferous soil, and grew up to 4-fold better with increasing Se supply, while the non-accumulators showed opposite results. Both hyperaccumulators and non-accumulators could affect growth (up to 3-fold) and Se accumulation (up to 6-fold) of neighboring plants. The mechanisms for these effects are largely unknown but may involve concentration of soil Se via exudation, root turnover and litter deposition. Exudate of selenate-supplied A. bisulcatus was shown by x-ray absorption spectroscopy to contain mainly C-Se-C. In conclusion, Se hyperaccumulators may enhance the soil Se levels under their canopy, and also convert inorganic Se to organic Se. The Se-enriched soil around hyperaccumulators enhances Se levels in neighboring plants, which may negatively affect Se-sensitive neighboring plants via toxicity, but facilitate Se-tolerant neighbors through reduced herbivory. The latter is an interesting finding, as it constitutes facilitation via enrichment with a non-essential element. It is also interesting that Se enrichment of neighbors by hyperaccumulators can result in competition when neighbors are Se-sensitive and in facilitation when neighbors are Se-tolerant. Via these competitive and facilitating effects, Se hyperaccumulators may affect plant species composition and, consequently, higher trophic levels. Hyperaccumulators may favor Se resistant species at different trophic levels, while selecting against Se sensitive species. If indeed Se hyperaccumulators affect soil Se distribution and speciation and local species composition and Se tolerance, Se hyperaccumulators may play an important role in Se entry into and Se cycling through their seleniferous ecosystems.


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