Why Does Herbivore Attack Reconfigure Primary Metabolism?

Abstract

A plant's resistance to herbivore attack is thought to be principally determined by its secondary metabolism, which can be remarkably plastic and responsive to different grades and types of herbivory. Newer unbiased “omic” approaches, which characterize transcriptomic, metabolomic, and proteomic changes in herbivore-attacked plants, have laid to rest the notion that metabolism can be neatly parsed into “secondary metabolism,” which functions to meet environmental challenges, and “primary metabolism,” which supports growth. The hundreds of genes regulated during the plant-herbivore or -pathogen interaction have been analyzed with microarray studies, and almost all aspects of metabolism are represented, with a substantial fraction coming from primary metabolism (Hui et al., 2003; Both et al., 2005; Major and Constabel, 2006; Mozoruk et al., 2006; Ralph et al., 2006; Schmidt and Baldwin, 2006; Tian et al., 2006; Kant and Baldwin, 2007) Here, we consider four overlapping functional explanations for this reconfiguration: Dependency of resistance traits (defenses and tolerance) and primary metabolism. Primary metabolism is fueled by energy and resources, which the plant gains from its environment. Primary metabolism involves growth, storage, and reproduction. Tolerance depends on primary metabolites and energy, both of which are taken from pools for reproduction, storage, and/or growth, and later reinvested in reproduction. Defenses from secondary metabolism are based on energy and resources from primary metabolism, which can be partially resupplied to primary metabolism. Parts of primary metabolism can function as direct defense. Rather than supporting defense responses, reconfiguration could support the physiological adjustments plants must make to tolerate herbivory and reduce the negative fitness consequences of herbivore attack (Fig. 1). Resistance signaling is elicited differently from simple wounding when herbivore-specific elicitors (FACs) are introduced into wounds during caterpillar feeding. Signaling depends on primary metabolites. Herbivory induces a large reorganization of primary metabolism, including altered photosynthesis and altered sink/source relations. These changes are coordinated by a signaling network that is only partially understood. The expression of defense and tolerance traits requires changes both in primary and secondary metabolism. Induced changes in primary metabolism could themselves be defensive (Fig. 2). We consider these four hypotheses in an overview of the literature that addresses how assimilation and the partitioning of assimilates are altered by herbivory and how primary metabolites function as signals and as defenses. In conclusion, we consider the challenges that plant biologists face in attempting to falsify these hypotheses. Compared to the falsifications of hypotheses about the defensive function of secondary metabolism, tests of the above hypotheses will seriously challenge the procedures that we use to understand resistance mechanisms and perhaps even challenge the reductionist paradigm that has proved so useful for understanding gene function in much of biology in the last century. If the resource demands of defense production compete with those of growth and reproduction, and defenses are costly to produce (Steppuhn, 2007), then changes in the partitioning of resources among growth, storage, and reproduction would be expected (Fig. 1). Changes in how resources are partitioned according to function can be avoided if the rate of resource assimilation increases. Similar predictions hold for the activation of physiological changes that allow plants to better tolerate the negative fitness consequences of herbivory. Tolerance, which measures a plant's ability to compensate for the negative fitness effects of tissue damage, is usually described as a reaction norm of the fitness of specific genotypes at various damage levels (Strauss and Agrawal, 1999; Stowe et al., 2000). Tolerance is thought to result from the activation of dormant meristems, changes in plant architecture, resource allocation, or photosynthetic capacity. In short, the herbivory-induced activation of both defense and tolerance responses is predicted to alter resource assimilation and source-sink relationships, and the literature provides general support for these predictions. The photosynthetic apparatus frequently responds to herbivore attack, usually with decreases in CO2 assimilation in the attacked leaf that are proportionally greater than the leaf area that is actually damaged (Zangerl et al., 2002). Otherwise, the photosynthetic response depends on the type of attacker and the age of the tissues that are measured (Welter, 1989). Defoliating herbivores can increase the photosynthetic activity of unattacked leaves, whereas stem borers and mesophyll feeders tend to decrease activity. On the other hand, transcript levels of photosynthetically related genes are commonly down-regulated (Hui et al., 2003;