An important feature of many wound-induced direct defense responses is their occurrence in undamaged tissues located far from the site of wounding. Wound-inducible serine proteinase inhibitors (PIs) represent one of the best examples of a systemically induced defense response. In tomato plants, PI genes are expressed in distal leaves within 1-2 hrs after insect attack or mechanical wounding (Ryan 2000; Strassner et al. 2002). The rapid and systemic nature of this response is analogous to vertebrate immune responses in which endocrine signals are delivered to target tissues via the circulatory system (Bergey et al. 1996). However, because plants lack mobile defender cells, systemic signals must be transmitted long distances via mechanisms that are specific to plants (Malone 1996; Leon et al. 2001; Schilmiller and Howe 2005). Ryan's pioneering work on systemic wound signaling inspired generations of plant biologists to investigate the underlying mechanisms of this fascinating response.
The widespread occurrence of systemic defense responses in the plant kingdom implies the existence of common mechanisms to generate, transport, and perceive alarm signals that are generated at the site of tissue damage. Wound-inducible PIs in tomato and other solanaceous plants have been widely used as a model system in which to study the molecular mechanism of systemic wound signaling. Green and Ryan (1972) proposed that chemical signals produced at the wound site travel through the plant and activate PI expression in undamaged leaves. Identification of these signaling compounds was facilitated by a simple bioassay in which test solutions (e.g., containing an elicitor) are supplied to tomato seedlings through the cut stem, followed by measurement of PI accumulation in the leaves. Extensive use of this assay led to the discovery of several distinct classes of PI-inducing compounds, including cell-wall-derived oligogalacturonides (OGAs), systemin, jasmonic acid (JA), and hydrogen peroxide (Ryan 2000; Gatehouse 2002). Physical signals (e.g., hydraulic forces and electrical signals) generated by tissue damage have also been implicated in the systemic signaling process (Wildon et al. 1992; Malone 1996). Currently, a major challenge is to determine how these diverse signals interact with one another to promote intercellular communication across long distances.
Farmer and Ryan (1992) established the current paradigm that extracellular signals such as OGAs and systemin (so-called primary wound signals), generated in response to wounding, trigger the intracellular production of JA via the octadecanoid pathway and that JA, in turn, activates the expression of defensive genes. Wound-induced production of OGAs is catalyzed by a family of polygalacturonases (PGs) that are expressed in various plant tissues (Bergey et al. 1999). OGAs are relatively immobile in the plant vascular system and thus are thought to act as local mediators. However, because PG activity is induced systemically in response to wounding, OGAs could also amplify defense responses in undamaged leaves (Ryan 2000). OGA-mediated signal transduction may result from direct physical effects of these compounds on the plasma membrane or may involve specific receptors (Navazio et al. 2002).
Systemin was the first bioactive peptide discovered in plants (Pearce et al. 1991). This 18-amino-acid peptide is derived from proteolytic cleavage of a larger precursor protein, prosystemin. When used in the tomato seedling bioassay, systemin is >10, 000-fold more active than OGAs in inducing PI expression. Several lines of evidence indicate that systemin serves a key role in induced defense responses in tomato. For example, transgenic plants expressing an antisense prosystemin (Prosys) cDNA are deficient in wound-induced systemic expression of PIs and, as a consequence, are more susceptible to insect herbivores (McGurl et al. 1992; Orozco-Cardenas et al. 1993). Overexpression of prosystemin from a 35S::Prosys transgene constitutively activates PI expression in the absence of wounding, thereby conferring enhanced resistance to herbivores (McGurl et al. 1994; Li et al. 2002; Chen et al. 2005). Forward genetic analysis has shown that genes required for systemin-mediated signaling are essential for wound-induced expression of PI and other defense-related genes (Howe and Ryan 1999; Howe 2004). Thus, wounding and systemin activate defense genes through a common signaling pathway.
Transcriptional activation of defense genes in response to systemin requires the biosynthesis and subsequent action of JA (Farmer and Ryan 1992; Howe, 2004). The systemin signaling pathway is initiated upon binding of the peptide to a 160-kDa plasma membrane-bound receptor (SR160) that was identified as a member of the leucine-rich repeat (LRR) receptor-like kinase family of proteins (Scheer and Ryan 1999, 2002). Binding of systemin to the cell surface is associated with several rapid signaling events, including increased cytosolic Ca2+ levels, membrane depolarization, and activation of a MAP kinase cascade (Felix and Boller 1995; Stratmann and Ryan 1997; Moyen et al. 1998; Schaller and Oecking 1999). The precise mechanism by which systemin activates JA synthesis remains to be determined. There is evidence indicating that a systemin-regulated phospholipase A2 activity in tomato leaves releases linolenic acid, a JA precursor, from lipids in the plasma membrane (Farmer and Ryan 1992; Narvaez-Vasquez et al. 1999). Alternatively, the role of a chloroplast-localized phospholipase A1 in JA biosynthesis (Ishiguro et al. 2001) raises the possibility that systemin perception at the plasma membrane is coupled to the activation of a similar lipase in the chloro-plast. JA synthesized in response to systemin, OGAs, and wounding acts in concert with ethylene (O'Donnell et al. 1996) and hydrogen peroxide (Orozco-Cárdenas et al. 2001; Sagi et al. 2004) to positively regulate the expression of downstream target genes.
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