In new work, researchers report that the ability of plants to defend themselves by accumulating high levels of a toxic element can be overcome by some insects, and that such adaptation potentially echoes in the food web as other predators and parasites may in turn evolve to deal with high levels of the toxic element. The findings, reported by Elizabeth Pilon-Smits of Colorado State University and colleagues there and at the University of California, Berkeley, appear in the November 21st issue of the journal Current Biology, published by Cell Press.
Some plants "hyperaccumulate" the element selenium to extreme levels--up to 1% of the plant's dry weight. Selenium, an element with properties similar to sulfur, is an essential trace element for many organisms, but it typically is toxic at high levels, and the function behind the intriguing tendency of some plants to hyperaccumulate this element has been largely obscure. The so-called elemental-defense hypothesis proposes that hyperaccumulated elements serve a defensive function against herbivory, the predation of plants by animals.
In their new work, the researchers showed that the selenium in the hyperaccumulator plant species known as prince's plume (Stanleya pinnata) protects it from caterpillar herbivory both by deterring feeding and by causing toxicity in the caterpillar. However, the researchers also showed that in the plant's natural habitat, a newly discovered variety of the invasive diamondback moth (Plutella xylostella) has disarmed the plant's elemental defense. The new moth variety in fact thrives on plants containing highly toxic selenium levels and, in contrast to related varieties, was not deterred from either laying eggs or feeding on the plant. Furthermore, the researchers found that a selenium-tolerant wasp (Diadegma insulare) in turn parasitizes the selenium-tolerant diamondback moth.
Chemical analysis showed that the selenium-tolerant moth and its parasite both accumulate selenium in the form of methylselenocysteine, the same form found in the hyperaccumulator plant, whereas related but selenium-sensitive moths accumulate selenium as selenocysteine. The latter form is toxic because of its ability to be incorporated into proteins.
The authors outline a possible course of events in the evolution of selenium tolerance in the newly discovered diamondback moth. Their overall conclusion is that although selenium hyperaccumulation protects plants from herbivory by some invertebrates, it can give rise to the evolution of unique selenium-tolerant herbivores, thereby providing a "portal" for selenium into the local ecosystem--that is, a pathway by which selenium hyperaccumulation may spread within parts of the food web.
The authors point out that in a broader context, the findings potentially have implications for a number of ways in which selenium accumulation might be utilized in different ecological and agricultural circumstances. Applying selenium to plants may be an efficient way to deter herbivory and improve crop productivity, and if managed carefully, the supplied selenium could give added value to the crop (some evidence suggests that selenium has anticarcinogenic properties). Furthermore, the newly discovered selenium-tolerant moth may be used for biological control of plants that hyperaccumulate selenium in areas where such plants cause poisoning of livestock. In addition, the selenium-hyperaccumulator plant may also be useful for removing and dispersing selenium from polluted water and soil. The authors note that such use of native selenium hyperaccumulators or of selenium-enriched agricultural crops--for environmental cleanup or as a source of anti-carcinogenic selenocompounds--may have ecological implications, as is clear from the apparent rapid evolution of selenium-tolerant insects shown in this study.
The researchers include John L. Freeman, Colin F. Quinn, and Elizabeth A.H. Pilon-Smits of Colorado State University in Fort Collins, CO; Matthew A. Marcus and Sirine Fakra of Lawrence Berkeley Laboratory in Berkeley, CA.
This work was supported by National Science Foundation grant #IOB-0444471 to E.A.H.P.-S. The operations of the Advanced Light Source at Lawrence Berkeley National Laboratory are supported by the Director, Office of Science, Office of Basic Energy Sciences, Materials Sciences Division of the US Department of Energy under contract no. DEAC03-76SF00098.
Freeman et al.: "Selenium-Tolerant Diamondback Moth Disarms Hyperaccumulator Plant Defense." Publishing in Current Biology 16, 2181–2192, November 21, 2006 DOI 10.1016/j.cub.2006.09.015. www.current-biology.com
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