Insect herbivore counteradaptations to the plant glucosinolate–myrosinase system

Abstract

The glucosinolate–myrosinase system found in plants of the Brassicales order is one of the best studied plant chemical defenses. Glucosinolates and their hydrolytic enzymes, myrosinases, are stored in separate compartments in the intact plant tissue. Upon tissue disruption, bioactivation of glucosinolates is initiated, i.e. myrosinases get access to their glucosinolate substrates, and glucosinolate hydrolysis results in the formation of toxic isothiocyanates and other biologically active products. The defensive function of the glucosinolate–myrosinase system has been demonstrated in a variety of studies with different insect herbivores. However, a number of generalist as well as specialist herbivores uses glucosinolate-containing plants as hosts causing large agronomical losses in oil seed rape and other crops of the Brassicaceae. While our knowledge of counteradaptations in generalist insect herbivores is still very limited, considerable progress has been made in understanding how specialist insect herbivores overcome the glucosinolate–myrosinase system and even exploit it for their own defense. All mechanisms of counteradaptation identified to date in insect herbivores specialized on glucosinolate-containing plants ensure that glucosinolate breakdown to toxic isothiocyanates is avoided. This is accomplished in many different ways including avoidance of cell disruption, rapid absorption of intact glucosinolates, rapid metabolic conversion of glucosinolates to harmless compounds that are not substrates for myrosinases, and diversion of plant myrosinase-catalyzed glucosinolate hydrolysis. One of these counteradaptations, the nitrile-specifier protein identified in Pierid species, has been used to demonstrate mechanisms of coevolution of plants and their insect herbivores.

Introduction

The ability of plants to produce the astonishing diversity of secondary metabolites has long been thought to be tightly linked to their ability to defend themselves against biotic stresses (Hartmann, 2007). For example, plant secondary metabolites may act as toxins to herbivores and bacterial or fungal pathogens, as deterrents or repellants, or as signals in indirect defense responses, and thus serve as chemical defenses (Dicke and Baldwin, 2010, Hopkins et al., 2009, Kessler and Halitschke, 2007, Wittstock and Gershenzon, 2002). While effective in many cases, the chemical arsenal of plants, in turn, puts selection pressure on plant enemies (e.g. insect herbivores) to acquire counteradaptions that enable them to overcome these defenses. Among others, these include the development of binding sites insensitive to a certain toxin (Holzinger et al., 1992), rapid excretion (Self et al., 1964), metabolic detoxification (Ivie et al., 1983) and/or sequestration (Hartmann, 1999, Lindigkeit et al., 1997) as well as behavioral means of preventing intoxications (Dussourd and Eisner, 1987). Depending on the effectiveness of the counteradaptation as well as sensory adaptations, a herbivore may be able to use a broad range of host plants defended by a diversity of compounds (generalist herbivores) or become specialized to plants defended by a certain group of chemicals (specialist herbivores). As a consequence, modification of existing defense pathways and recruitment of new plant defenses will provide selective advantages for the plant and open up a new round of the “evolutionary arms race” (Ehrlich and Raven, 1964).

In contrast to many other chemical defenses, glucosinolates, a group of anionic thioglucosides present in the Brassicales (Fahey et al., 2001), do not seem to be toxic themselves. However, when brought together with myrosinases, thioglucosidases (EC 3.2.1.147) co-occurring with glucosinolates, they are rapidly hydrolyzed to toxic isothiocyanates (mustard oils) and other biologically active products (Halkier and Gershenzon, 2006). The sudden release of high levels of these compounds upon tissue damage (“mustard oil bomb”; Matile, 1980), e.g. by a chewing herbivore, is a very effective defense against some generalist herbivores (Hopkins et al., 2009, Li et al., 2000, Müller et al., 2010). In contrast, several specialist insect species feed with impunity on glucosinolate-containing plants even though they are sensitive to isothiocyanates, and they may even use the presence of glucosinolates in a plant as host recognition cue (Agrawal and Kurashige, 2003, Hopkins et al., 2009, Li et al., 2000, Müller et al., 2010, Mumm et al., 2008). This has a large impact on agricultural practices and yield as many important crop plants are glucosinolate-containing, e.g. oilseed rape and Brassica vegetables such as broccoli and various cabbages (Ahuja et al., 2010). Nevertheless, there are also some generalist lepidopteran species that use glucosinolate-containing plants as major hosts throughout larval development and cause considerable agronomical damage (Ahuja et al., 2010). This raises questions about the biochemical bases of counteradaptations to the glucosinolate–myrosinase system and their similarities and differences in generalist vs. specialist herbivores. The fact that the glucosinolate–myrosinase system is an activated defense system may offer the possibility for a herbivore to not only detoxify harmful compounds but to prevent their formation by interfering with the process of activation. Furthermore, when dealing with an activated defense system such as the glucosinolate–myrosinase system, the feeding mode of a herbivore may be of special importance in terms of adaptation as a chewing herbivore may be confronted with different chemicals than a sucking herbivore due to a different degree of tissue damage upon feeding.

In the past decade, considerable progress has been made in our understanding of how sucking and chewing herbivores overcome the glucosinolate–myrosinase system. In this review, we survey the mechanisms of counteradaptation identified in generalist as well as specialist insect herbivores, identify some general principles of insect adaptation to an activated plant defense system and pinpoint prospects for future research.