Recognition of Herbivory-Associated Molecular Patterns

Abstract

A, S. littoralis caterpillar feeding on a barrel medic (Medicago truncatula) leaf. B, Scanning electron micrograph of lima bean leaf damage zone after feeding of S. littoralis larvae (micrograph by G. Wanner, Munich). Up to now, our knowledge of recognition processes in plant-herbivore interactions has been very limited. Thus, it seems justified to look first for similarities and related developments, rather than ignoring what we can learn from other systems. Signaling pathway studies revealed striking similarities in plant-pathogen and plant-herbivore interactions (Walling, 2000; Taylor et al., 2004; Garcia-Brugger et al., 2006; Maffei et al., 2007b). For instance, typical elements of the battery of pathogen-induced plant responses that are also initiated after attempted herbivore infestation include enhanced ion fluxes across the plasma membrane and, very close to the biting zone, collapse of membrane integrity of challenged plant cells (Maffei et al., 2004), activation of kinase cascades (Wu et al., 2007), and generation of reactive oxygen species (Maffei et al., 2006). These localized defenses occur at the site of attack and are restricted to the treated leaf tissue. Moreover, generation of the phytohormones jasmonic acid (JA), salicylic acid (SA), and ethylene (Walling, 2000; Kessler and Baldwin, 2002; Maffei et al., 2007b), activation of defense-related genes (Baldwin et al., 2001; Zavala et al., 2004), and synthesis of (volatile and nonvolatile) secondary compounds (Baldwin and Callahan, 1993; De Moraes et al., 1998; Kessler and Baldwin, 2001; Leitner et al., 2005) also can occur systemically. Thus, it seems tempting to speculate that the initial events concerning the recognition of pathogens or herbivores might be similar as well. Actually, widespread usage of the term “elicitor” for signaling compounds that can stimulate herbivore-induced responses in plants has been borrowed from the pathogen field. Several models are conceivable to explain the basis of plant resistance against aggressors. Recognition of pathogens can be mediated either in a nonhost manner between a plant and pathogen species or in a gene-for-gene interaction between a particular plant cultivar and a pathogen race. The high degree of specificity in the latter case is indicative of the coevolution of the antagonists, host, and pathogen, respectively (Dangl and Jones, 2001; Jones and Dangl, 2006). Nonhost disease resistance envisions a ligand-receptor-like interaction. In this case, plant immunity relies on the perception of chemical cues, general elicitors, which are present either constitutively in the pathogens or generated during pathogen invasion, by specific cell surface-localized receptors (Jones and Dangl, 2006). Such general elicitors are believed to merit the classification as pathogen-associated molecular patterns (PAMPs), whereas the corresponding receptors are referred to as pattern recognition receptors (PRRs). Recently, the more general term, microbe-associated molecular patterns (MAMPs), is preferred (Bittel and Robatzek, 2007). MAMPs/PAMPs are perceived at low concentrations and act as inducers of defense reactions (Boller, 1995; Ebel and Mithöfer, 1998). MAMPs display diverse structures, including carbohydrates, (glyco)-proteins, lipids, peptides, and sterols (Boller, 1995; Ebel and Mithöfer, 1998; Nürnberger et al., 2004). They are constituents of the outer layers of the pathogens, such as chitin fragments (Yamada et al., 1993), β-glucan fragments (Ayers et al., 1976), Pep-13, a peptide of the cell wall transglutaminase of Phytophthora (Brunner et al., 2002), or flg22, a peptide of the bacterial flagellin (Felix et al., 1999), but also an N-acetylated peptide of the bacterial elongation factor (EF)-Tu (Kunze et al., 2004). For most of these MAMPs, the corresponding PRRs or binding sites have been genetically and biochemically identified (Bittel and Robatzek, 2007): for β-glucans, the extracellular glucan-binding protein (Mithöfer et al., 2000; Fliegmann et al., 2004); for chitin, the transmembrane LysM-containing receptor-like proteins, CEBiP (Kaku et al., 2006); and for flg22 and EF-Tu, the transmembrane Leu-rich repeat receptor-like kinases FLS2 (Gomez-Gomez and Boller, 2000; Chinchilla et al., 2006) and EFR (Zipfel et al., 2006), respectively. At least the FLS2 receptor can be internalized followed by subcellular redistribution and accumulation in endosomes (Robatzek et al., 2006). Typically, MAMP-triggered host responses are elicited fast and transiently, a fact that holds true also for responses elicited during herbivory (Maffei et al., 2007b). Moreover, because MAMPs are structurally rather diverse and the variety of induced responses in plant-pathogen and plant-herbivore interactions seems to have similar characteristics, it is tempting to propose that the basic processes in herbivore recognition in plants might be related to the recognition of pathogens. In the following, we will summarize our knowledg