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American Society of Plant Biologists
Some Like It with NitrilesA Nitrile-Specifying Protein Linked to Herbivore Feeding Behavior in Arabidopsis
In their landmark study of coevolution, Ehrlich and Raven (1964)
In Arabidopsis and other members of the Brassicaceae (Cruciferae), it is widely believed that plant-derived glucosinolates are a major determinant of insect oviposition and feeding behavior. However, experimental results often have been unsatisfying, because frequently there is little correlation between glucosinolate content and herbivore behavior or the extent of herbivore damage (Chew, 1988  ). Glucosinolates are anionic thioglucosides found mainly in the Brassicaceae and other families of the order Capparales. After tissues are damaged, glucosinolates come into contact with and are hydrolyzed by myrosinases to yield a variety of products, such as isothiocyanates and nitriles, that are active against a variety of herbivores and pathogens (reviewed by Bones and Rossiter, 1996).
Although glucosinolates themselves are toxic and unpalatable to numerous insect herbivores, the products of myrosinase activity have been found to be more toxic than their glucosinolate precursors to some herbivores. For example, Li et al. (2000)
On the other hand, some glucosinolates, or their hydrolysis products, act as host-finding cues and feeding stimulants for a number of insect specialist herbivores on cruciferous plant species (Chew, 1988
Although it is clear that the potential exists for coevolution among plants and their insect herbivores, definitive links between plant defense genotypes and insect herbivory phenotypes are lacking. Mauricio (1998) showed that there is genetic variation for glucosinolate content (as well as trichome density) among natural populations of Arabidopsis, which is a prerequisite for an evolutionary response to selection; furthermore, they found that these characteristics reduced damage by natural assemblages of herbivores, and represented significant fitness costs to the plant. Fitness costs are an important component of models for the evolution of resistance, because it is assumed that such costs contribute to populations reaching an evolutionary equilibrium at intermediate levels of resistance by counteracting the benefits of reducing herbivory (Mauricio, 1998; Stowe, 1998). Mauricio and Rausher (1997) provided direct evidence that natural enemies, including herbivores and fungal pathogens, exert selection pressure on glucosinolate concentration and trichome density in Arabidopsis by showing that the elimination of natural enemies from an experimental field population altered the pattern of selection on these two traits.
The type of glucosinolate produced and the nature of the hydrolysis products also may be important factors influencing herbivores and pathogens. Kliebenstein et al. (2001a)
Because glucosinolate hydrolysis products often are the most highly active defensive compounds, it is important to include this step in any model designed to explain plant–insect interactions. In this issue of The Plant Cell, Lambrix et al. (pages 2793–2807) identify an Arabidopsis gene for an epithiospecifier (ESP) protein at a quantitative trait locus (QTL) responsible for a distinct polymorphism in the type of glucosinolate hydrolysis products found among Arabidopsis ecotypes, and they show that the activity of the ESP protein has an effect on the feeding behavior of the generalist lepidopteran herbivore Trichoplusia ni (Figure 1) . The group analyzed leaf samples from 122 different ecotypes of Arabidopsis and found that all ecotypes produce mainly isothiocyanates or mainly nitriles. Because the Columbia (Col) ecotype was found to produce mainly isothiocyanates and Landsberg erecta (Ler) produced mainly nitriles, the trait was mapped in 95 Col x Ler recombinant inbred lines. Two loci affecting glucosinolate breakdown profiles were identified, one on chromosome 1 and one on chromosome 3.
The locus on chromosome 1 was examined further and was found to contain a gene for an ESP protein, a myrosinase cofactor that is known to cause the formation of nitriles instead of isothiocyanates in B. napus (Bernardi et al., 2000 ). The ESP genomic sequence was obtained from seven ecotypes, four (including Col) that produced mainly isothiocyanates and three (including Ler) that produced mainly nitriles. Ecotypes such as Ler were found to express a functional copy of the ESP gene, whereas ecotypes represented by Col either did not express the gene or, in the case of one ecotype, expressed a gene product containing a deletion in the cDNA that presumably affected ESP activity. Feeding studies with T. ni larvae on the Col x Ler recombinant inbred lines revealed QTLs associated with the feeding rate of this herbivore that closely overlapped the QTLs associated with glucosinolate hydrolysis profiles. T. ni larvae showed a clear preference for nitrile-producing lines containing the Ler locus.
Jander et al. (2001)
The ESP protein has an unusual type of activity. It does not function in the absence of myrosinase, and neither is myrosinase activity absolutely dependent on the presence of active ESP protein; rather, it appears to direct the myrosinase enzyme to form an altered product (MacLeod and Rossiter, 1985 ). Bernardi et al. (2000) described the ESP protein from B. napus seed as a myrosinase cofactor that drives the hydrolysis of some glucosinolates toward the production of highly toxic cyanoepithioalkanes (epithionitriles) instead of isothiocyanates or simple nitriles. In in vitro experiments with recombinant Arabidopsis ESP protein in the presence of myrosinase, Lambrix et al. found that alkenyl glucosinolates were converted to epithionitriles and nonalkenyl glucosinolates were converted to simple nitriles, whereas in the absence of the ESP protein, these substrates were converted to isothiocyanates. Thus, the Arabidopsis ESP protein seems to be a more general "nitrile-specifying" protein than other ESP proteins that have been characterized. The exact mechanism of action of the ESP protein is unknown. It may act separately from myrosinase on the myrosinase product, or it may complex with myrosinase to alter its catalytic activity. Isolation of the Arabidopsis ESP gene will allow further studies on the chemical activity of this interesting protein.
T. ni is a generalist herbivore that feeds on many different kinds of plants in the wild. It is curious that the presence of functional ESP protein and the production of nitriles were associated with increased herbivory by T. ni larvae. In other words, it is difficult to explain how insect herbivory could be responsible for the selection of the ESP protein as a plant defense mechanism when these critters actually prefer the products of its activity. Lambrix et al. discuss a number of possible situations that could explain this outcome in terms of coevolution. Nitriles may be more toxic than isothiocyanates for certain other herbivores. It should be noted that although T. ni feeds readily on Arabidopsis in experimental situations, it has not been reported as an herbivore on Arabidopsis in the wild (Jander et al., 2001 ). Some studies have suggested that epithionitriles are particularly toxic to certain insects (Peterson et al., 2000; Galletti et al., 2001). Alternatively, some isothiocyanates are volatile and have been shown to act as host-finding cues for specialist herbivores (Städler, 1992); thus, the presence of the ESP protein and alteration from isothiocyanate to nitrile formation may allow the plant to escape detection by such insects. It also is possible that the ESP protein evolved for reasons unrelated to insect herbivory, and then certain herbivores developed a taste for the nitrile products and some plant populations fell under selection pressure to lose the ESP gene. Lambrix et al. found that ESP function has been lost at least twice in the evolutionary history of Arabidopsis, once by complete loss of gene expression and once by the loss of a large segment of the coding region.
Kliebenstein et al. (2001b) It will be of interest to study the effect of the ESP protein on the feeding behavior of other generalist and specialist herbivores. The identification of the ESP gene by Lambrix et al. may allow for a more rigorous test of the coevolution of cruciferous plant species with their insect herbivores. Analyses of the molecular variation at the ESP locus may provide clues about the nature of selection at this locus and whether it is linked to herbivore utilization. The complexity of variation in glucosinolate concentration, glucosinolate type, and type of hydrolysis products generated may reflect the complex interplay between numerous types of insects herbivores and pathogens and the costs associated with mounting an adequate defense system. The identification of the Arabidopsis ESP gene is an important step toward a more complete understanding of plant–insect interactions.
Bartlet, E., Blight, M.M., Hick, A.J., and Williams, I.H. (1993). The responses of the cabbage seed weevil (Ceutorhynchus assimilis) to the odor of oilseed rape (Brassica napus) and to some volatile isothiocyanates. Entomol. Exp. Appl. 68, 295–302.[CrossRef] Bernardi, R., Negri, A., Ronchi, S., and Palmieri, S. (2000). Isolation of the epithiospecifier protein from oil-rape (Brassica napus spp. oleifera) seed and its characterization. FEBS Lett. 467, 296–298.[CrossRef][Medline] Bones, A.M., and Rossiter, J.T. (1996). The myrosinase-glucosinolate system, its organisation and biochemistry. Physiol. Plant. 97, 194–208.[CrossRef] Chew, F. (1988). Do glucosinolates always control interactions of Cruciferae with their potential herbivores and symbionts? No! In Chemical Mediation of Coevolution, K.A. Spencer, ed (New York: Chapman & Hall), pp. 214–238. Donkin, S.G., Eiteman, M.A., and Williams, P.L. (1995). Toxicity of glucosinolates and their enzymatic decomposition products to Caenorhabditis elegans. J. Nematol. 27, 258–262. Ehrlich, P.R., and Raven, P.H. (1964). Butterflies and plants: A study in coevolution. Evolution 18, 586–608.[CrossRef][ISI] Galletti, S., Bernardi, R., Leoni, O., Rollin, P., and Palmieri, S. (2001). Preparation and biological activity of four epiprogoitrin myrosinase–derived products. J. Agric. Food Chem. 49, 471–476.[Medline]
Jander, G., Cui, J., Nhan, B., Pierce, N.E., and Ausubel, F.M. (2001). The TASTY locus on chromosome I of Arabidopsis affects feeding of the insect herbivore Trichoplusia ni. Plant Physiol. 126, 890–898.
Kliebenstein, D.J., Kroymann, J., Brown, P., Figuth, A., Pedersen, D., Gershenzon, J., and Mitchell-Olds, T. (2001a). Genetic control of natural variation in Arabidopsis glucosinolate accumulation. Plant Physiol. 126, 811–825.
Kliebenstein, D.J., Lambrix, V.M., Reichelt, M., Gershenzon, J., and Mitchell-Olds, T. (2001b). Gene duplication in the diversification of secondary metabolism: Tandem 2-oxoglutarate–dependent dioxygenases control glucosinolate biosynthesis in Arabidopsis. Plant Cell 13, 681–693.
Lambrix, V., Reichelt, M., Mitchell-Olds, T., Kliebenstein, D.J., and Gershenzon, J. (2001). The Arabidopsis epithiospecifier protein promotes the hydrolysis of glucosinolates to nitriles and influences Trichoplusia ni herbivory. Plant Cell 13, 2793–2807. Li, Q., Sanford, D., Eigenbrode, G., Stringam, R., and Thiagarajah, M.R. (2000). Feeding and growth of Plutella xylostella and Spodoptera eridania on Brassica juncea with varying glucosinolate concentrations and myrosinase activities. J. Chem. Ecol. 26, 2401–2419.[CrossRef] MacLeod, A.J., and Rossiter, J.T. (1985). The occurrence and activity of epithiospecifier protein in some Cruciferae seeds. Phytochemistry 24, 1895–1898.[CrossRef] Mauricio, R. (1998). Costs of resistance to natural enemies in field populations of the annual plant, Arabidopsis thaliana. Am. Nat. 151, 20–28.[CrossRef] Mauricio, R., and Rausher, M.D. (1997). Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense. Evolution 51, 1435–1444.[CrossRef] Mitchell-Olds, T. (2001). Arabidopsis thal-iana and its wild relatives: A model system for ecology and evolution. Trends Ecol. Evol. 16, 693–700.[CrossRef] Peterson, C.J., Cossé, A., and Coats, J.R. (2000). Insecticidal components in the meal of Crambe abyssinica. J. Agric. Urban Entomol. 17, 27–36. Städler, E. (1992). Behavioral responses of insects to plant secondary compounds. In Herbivores: Their Interactions with Plant Secondary Metabolites, G.A. Rosenthal and M.R. Berenbaum, eds (San Diego: Academic Press), pp. 45–88. Stowe, K.A. (1998). Experimental evolution of resistance in Brassica rapa: Correlated re-sponse of tolerance in lines selected for glucosinolate content. Evolution 52, 703–712.[CrossRef] This article has been cited by other articles:
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GLUCOSINOLATES AND INSECT...
THE CASE FOR COEVOLUTION
