The Jasmonate Signal Pathway

Abstract

Plant responses to many biotic and abiotic stresses are orchestrated locally and systemically by signaling molecules known as the jasmonates (JAs). JAs also regulate such diverse processes as pollen maturation and wound responses in Arabidopsis. Here we review recent advances in our understanding of how JA biosynthesis is regulated, the signaling functions of different JAs, and how the JA signal may be transduced via an E3 ubiquitin ligase. We also examine how outputs from the JA, salicylic acid (SA), and ethylene signal pathways are integrated in the regulation of stress response and plant development. We use the term jasmonate to include the biologically active intermediates in the pathway for jasmonic acid biosynthesis, as well as the biologically active derivatives of jasmonic acid. These compounds are widely distributed in plants and affect a variety of processes (Creelman and Mullet, 1997), including fruit ripening, production of viable pollen, root growth, tendril coiling, plant response to wounding and abiotic stress, and defenses against insects and pathogens. The function of JAs in defense was proposed by Farmer and Ryan (Farmer and Ryan, 1992), who provided evidence for a causal link between wounding (as caused by insect herbivores), the formation of JAs, and the induction of genes for proteinase inhibitors that deter insect feeding. In particular, they proposed that wounding caused release of linolenic acid (LA), the presumed precursor of JAs, from membrane lipids. New evidence indicates that JA signaling in plants is generally as proposed by Farmer and Ryan, but more complex than they envisaged. This new evidence indicates that intermediates in JA biosynthesis have distinctive biological activity, that an E3 ubiquitin ligase probably regulates most JA responses in Arabidopsis, and that the JA signaling pathway interacts with other defense signal pathways. A great deal of what we currently know about JA signaling comes from studies on Arabidopsis and tomato. However, there are several discrepancies between the proposed JA signaling pathways of these species, and it is not yet clear whether these reflect gaps in knowledge or reveal fundamental differences in mechanism. For example, Arabidopsis mutants defective in JA biosynthesis or perception are deficient in defense responses and are male sterile (Feys et al., 1994; McConn and Browse, 1996; Vijayan et al., 1998), whereas tomato mutants apparently defective in JA biosynthesis or perception have deficient defenses but are male fertile (Howe et al., 1996; Li et al., 2001). Similarly, the systemic induction of JA responses in tomato is through the well-characterised systemin signal pathway (Constabel et al., 1995; Ryan, 2000; Ryan et al., 2002), but in Arabidopsis there is no evidence for an equivalent pathway, even though systemic signaling can be demonstrated (Kubigsteltig et al., 1999). The JA signal pathway involves several signal transduction events: the perception of the primary wound or stress stimulus and transduction of the signal locally and systemically; the perception of this signal and induction of JA biosynthesis; the perception of JA and induction of responses; and finally, integration of JA signaling with outputs from the SA, ethylene, and other signaling pathways. JA signaling can be induced by a range of abiotic stresses, including osmotic stress (Kramell et al., 1995), wounding, drought, and exposure to “elicitors,” which include chitins, oligosaccharides, oligogalaturonides (Doares et al., 1995), and extracts from yeast (Parchmann et al., 1997; Leon et al., 2001). JA biosynthesis in Arabidopsis is also regulated by cues in the developing stamen, where jasmonic acid is required for pollen development. However, we do not yet know how these stresses or developmental cues are perceived. One approach has been to search for the earliest response to stress, which would therefore be a candidate for a component of the stress perception/signal transduction pathway. Gene Expression in JA Mutants Reveals Interaction between Defense Signal Transduction Pathways. Two μg of total RNA from each sample was analyzed on gel blots on nylon filters. Filters were probed with radiolabeled, polymerase chain reaction–generated DNA fragments from PR1, PDF1.2, Thi2.1, and 18S rRNA genes. (A) Seedlings were grown for 10 days on Murashige and Skoog (MS) agar, then transferred to fresh MS agar (−) or MS agar supplemented with 50 μM SA for 2 further days (+). (B) Seedlings were grown for 12 days on MS agar. (C) Model for positive (arrows) and negative (bars) interactions between the JA, ethylene, and SA signal pathways during response to pathogens, and pests or wounding. Gene symbols (in italics) are defined in the text; proteins are upper case, not italic. Similarly, in Arabidopsis, a mitogen-activated protein kinase named MPK4 is activated 2 to 5 min after wounding (Ichimura et al., 2000). The mpk4 mutant is dwarfed, has elevated levels of SA, and has const