IOS-0817748 PI: Elizabeth Pilon-Smits Ecological aspects of plant selenium hyperaccumulation - below and beyond
The element selenium (Se) is essential for many organisms. Dietary Se can boost the immune system and prevent cancer and bacterial and viral infections including HIV. On the other hand, Se is toxic at higher levels and Se is a serious environmental pollutant worldwide. Some plants native to the Western U.S., commonly called ?locoweeds?, hyperaccumulate Se up to 1 percent of their dry weight. The investigators propose that these plants hyperaccumulate Se as a defense compound against herbivory and microbial infection, and are interested in the effects of the accumulated Se on the ecological interactions of hyperaccumulators. Over the past three years they have discovered that Se accumulation protects plants from a variety of herbivores, due to both deterrence and toxicity. At the same time, several Se-tolerant specialist herbivores were found to feed on hyperaccumulators, and to accumulate fairly high Se levels. Continued studies will investigate how the Se in hyperaccumulators affects ecological interactions in their local ecosystem, going "below and beyond" what has been discovered so far. More specifically, effects of accumulated root Se on root-zone interactions of hyperaccumulator plants with neighboring plants, root-associated invertebrates, and root-associated microbes will be examined. Beyond the direct plant-herbivore or plant-microbe interactions, the researchers will investigate the effects of Se accumulation by specialist herbivores or microbes on the ecological interactions of these specialists that may further mobilize Se into the food chain. The findings from this project should have broad implications, and applications in medicine and agriculture. The effects of hyperaccumulation of Se on herbivores and other ecological partners are probably similar for other toxic metals and metalloids. Understanding the movements of hyperaccumulated elements in the food chain will be critical to the practices of phytoremediation (environmental cleanup using plants) and of cultivating element-fortified foods with health-benefiting properties. In addition, knowledge of how plant Se accumulation affects growth and survival of pathogens or herbivores, and identification of specialist Se-tolerant pathogens or herbivores may be used to both control plant pests and Se-hyperaccumulating noxious weeds.
Hyperaccumulators are plants that concentrate one or more toxic elements to levels that are more than a hundred fold higher than surrounding vegetation. Selenium (Se) hyperaccumulators occur naturally on Se-rich soils throughout the Western US, and can contain as much as 1% Se of their dry weight. Selenium is an element similar to sulfur. It is essential at low levels but toxic at higher concentrations. These Se hyperaccumulator plants were studied in this project. Question addressed were: what effects do the extreme Se levels in these plants have on the relationships with other organisms? Does the Se protect the plants from herbivores and pathogens? Are there effects on pollinators such as honey bees? Do the plants harbor specialized microbes, and do they have any effects on neighboring plants? The postdoctoral researcher, graduate students and undergraduate students participating in the project found that, indeed, Se protects hyperaccumulators from a wide variety of herbivores as well as some pathogens. This is due to both deterrence (they avoid high-Se plants) and toxicity. On the other hand, in seleniferous areas, the researchers also found several herbivores and pathogens that could eat hyperaccumulators with no ill effects: they were Se resistant. The Se in the hyperaccumulators did not deter pollinators. Honey bees and bumble bees were found to collect high-Se pollen and nectar, and incorporate the Se into their tissue and (at low levels) honey. The effects of this Se on bee health remains to be investigated. Selenium hyperaccumulators were found to contain a large collection of microbes, both fungi and bacteria, inside their tissues and in their root zone. These microbes were typically very Se resistant, and were able to convert toxic forms of Se (selenite) to non-toxic elemental Se. Interestingly, hyperaccumulators in the field were found to contain up to 30% inorganic Se, while plants in the greenhouse did not. This may be due to microbes present in the field. When some of these microbes were isolated and added back to sterile plants, they could significantly affect plant Se accumulation and plant growth. Other microbes from Se-rich areas were found in high numbers in decomposing litter from hyperaccumulator plants. The soil around Se hyperaccumulators was found to be enriched in Se, perhaps because the hyperaccumulators concentrate the Se in their leaves and then drop them on the soil around their stems. These elevated Se levels around hyperaccumulators resulted in enhanced Se levels in neighboring plants. Depending on the neighbor in question, this added Se can have a negative effect on plant growth if it is Se sensitive, but also a positive effect if it is Se tolerant. Some neighbors actually benefited from their elevated Se levels because it protected them from herbivores. The overall picture that emerges from these studies is that Se hyperaccumulators likely have a profound effect on their natural environment. They concentrate Se around them and inside them. These high Se levels have a negative effect on ecological partners (microbes, plants, animals) that are sensitive to Se, but at the same time offer an opportunity for ecological partners that are resistant to Se. In fact, hyperaccumulators probably have favored the evolution of more and more Se resistance in their ecological partners, which is an example of co-evolution. Through their negative effect Se sensitive, and positive effect on Se resistant local species of microbes, plants and animals, hyperaccumulators may significantly affect which species are successful in their local environment. Species that have such important ecological effects are sometimes called keystone species. Since hyperaccumulators concentrate Se and then distribute it to their ecological partners via Se-tolerant herbivores, microbes and pollinators, they likely are also important factors in Se cycling through their local ecosystem. Why do we care? Selenium is an important nutrient for humans and other mammals, and Se deficiency is a problem worldwide including areas of the USA. Lack of Se can increase the probability of cancer and viral infections. Plants are an important dietary source of Se. Naturally Se-enriched plant products are a form of biofortification that can alleviate Se deficiency in humans and livestock. On the other side of the coin, Se is also toxic. In some areas of the world (and USA) the levels of Se naturally present in soils and waters is too high and can cause toxicity. This is particularly problematic when people locally concentrate Se via irrigated agriculture or mining. Plants may clean up this excess Se by concentrating it in their harvestable tissues, and converting it to Se gas (volatilization). Cleanup using plants is called phytoremediation. If large fields of Se-rich plants are grown for phytoremediation or biofortification, it is vital that we understand the potential ecological implications, to avoid problems and maximize efficiency. The findings from this project are key in this respect, not only for Se but also for other hyperaccumulated elements.
