Cross Talk in Defense Signaling

Abstract

Plants are equipped with an array of defense mechanisms to protect themselves against attack by herbivorous insects and microbial pathogens. Some of these defense mechanisms are preexisting, whereas others are only activated upon insect or pathogen invasion. Induced defense responses entail fitness costs. Therefore, plants possess elaborate regulatory mechanisms that efficiently coordinate the activation of attacker-specific defenses so that fitness costs are minimized, while optimal resistance is attained (Pieterse and Dicke, 2007). A major focus in plant defense-signaling research is to uncover key mechanisms by which plants tailor their responses to different attackers and to investigate how plants cope with simultaneous interactions with multiple aggressors. During their lifetime, plants encounter numerous herbivorous insects and microbial pathogens with diverse modes of attack. To survive, plants have to perceive attack by these deleterious organisms and respond adequately by activating appropriate defense responses. The primary immune response has evolved to recognize common features of organisms that interact with the plant and to translate this recognition into a defense response that is specifically directed against the invader encountered (Jones and Dangl, 2006). In addition to this attacker-specific primary immune response, plants can activate another line of defense that is referred to as induced resistance. This type of resistance often acts systemically throughout the plant and is typically effective against a broad spectrum of attackers (Walters et al., 2007). Plants are able to activate different types of induced resistance, depending on the organism that interacts with the plant. Well-studied examples of induced resistance are systemic acquired resistance, which is triggered by pathogens causing limited infection, such as hypersensitive necrosis (Durrant and Dong, 2004), rhizobacteria-induced systemic resistance, which is activated upon colonization of roots by selected strains of nonpathogenic rhizobacteria (Van Loon et al., 1998), and wound-induced resistance, which is typically elicited upon tissue damage such as that caused by insect feeding (Kessler and Baldwin, 2002; Howe, 2004). The role of phytohormones in the regulation of these induced defenses is well established. Salicylic acid (SA), jasmonic acid (JA), and ethylene (ET) are recognized as key players in the regulation of the signaling pathways involved (Howe, 2004; Pozo et al., 2004; Lorenzo and Solano, 2005; Grant and Lamb, 2006; Van Loon et al., 2006a; Von Dahl and Baldwin, 2007). Other plant hormones, including abscisic acid (ABA; Mauch-Mani and Mauch, 2005), brassinosteroids (Nakashita et al., 2003), and auxin (Navarro et al., 2006; Wang et al., 2007), have also been implicated in plant defense, but their significance is less well studied. Upon pathogen or insect attack, plants respond with production of a specific blend of the alarm signals SA, JA, and ET, which varies greatly in quantity, composition, and timing. It is thought that this so-called signal signature contributes to the specificity of the plant's primary induced defense response (Reymond and Farmer, 1998; De Vos et al., 2005). The signaling pathways that are activated upon endogenous accumulation of these signals regulate different defense responses that are effective against partially distinct classes of attackers. Although there are exceptions (Thaler et al., 2004), generally it can be stated that pathogens with a biotrophic lifestyle are more sensitive to SA-mediated induced defenses, whereas necrotrophic pathogens and herbivorous insects are resisted more through JA/ET-mediated defenses (Thomma et al., 2001; Kessler and Baldwin, 2002; Glazebrook, 2005). In nature, however, plants often deal with simultaneous or subsequent invasion by multiple aggressors, which can influence the primary induced defense response of the host plant (Van der Putten et al., 2001; Bezemer and Van Dam, 2005; Stout et al., 2006). Hence, plants need regulatory mechanisms to effectively adapt to changes in their hostile environment. Cross talk between induced defense-signaling pathways is thought to provide the plant with such a powerful regulatory potential. Signaling interactions can be either mutually antagonistic or synergistic, resulting in negative or positive functional outcomes. Hence, cross talk can be interpreted as an inclusive term for the interaction between signaling pathways (Bostock, 2005). Cross talk helps the plant to minimize energy costs and create a flexible signaling network that allows the plant to finely tune its defense response to the invaders encountered (Reymond and Farmer, 1998; Pieterse et al., 2001; Bostock, 2005). Yet, it seems that insect herbivores and pathogens have also evolved to manipulate plants for their own benefit by suppressing induced defenses through modulation of the plant's defense-signaling network (Pieterse and Dicke, 2007). Schematic r