5.2.1 Necrotrophs vs. Biotrophs
Pathogens can be generally divided into those that infect and feed off living tissue (biotrophs) and those that kill cells prior to feeding on them (necrotrophs) (Parbery 1996). In 1998, Vijayan and coworkers were the first to provide compelling evi- dence of the essential role jasmonates play in mediating plant defenses against pathogens. They showed that the necrotrophic fungus Pythium mastophorum infected and killed theArabidopsistriple mutantfad3-2 fad7-2 fad8andcoi1but not wild-type plants. Exogenous application of JA rescued the fungal resistance of fad3-2 fad7-2 fad8mutant but not that ofcoi1. This confirmed that the JA-mediated protection of the exogenously applied JA against the fungus was due to jasmonate- mediated defense signaling and not due to toxicity of JA on the fungus. Similar observations were also reported for the necrotrophic pathogensBotrytis cinerea, Alternaria brassicicola, andFusarium oxysporum(Thomma et al.1998; Berrocal- Lobo and Molina 2004; Chehab et al. 2008; Chehab et al. 2011). However, jasmonate does not mediate defense against biotrophic Pseudomonas syringae. Instead, salicylic acid (SA) is the phytohormone required for defense at least during the early stages of pathogenesis (Feys et al.1994; Petersen et al.2000; Kloek et al.
2001). Interestingly, JA and SA work antagonistically and reduce each other’s responses (Niki et al.1998; Kunkel and Brooks2002; Traw et al.2003; Cipollini et al. 2004; Bostock 2005; Koornneef and Pieterse 2008). Indeed, P. syringae produces coronatine, a JA-Ile analogue, thereby augmenting the JA signaling pathway and suppressing SA defense against parasitic growth.
Although plants respond to necrotrophic and biotrophic pathogens by activating different defense signaling mechanisms, JA and SA signaling share some common downstream responses; for example, production of camalexin, a primaryArabidopsis phytoalexin important for pathogen growth inhibition (Tsuji et al.1992; Glazebrook and Ausubel1994; Glazebrook et al.1997), accumulates both in response to JA and
SA. Thus, common responses to different pathogens may be controlled by distinct regulatory networks; the mechanisms of this regulation remain to be elucidated.
5.2.2 Cross Talk of JA/SA
The molecular mechanisms responsible for the negative cross talk between SA and JA are not well understood. Repression of JA-induced gene expression by SA requires the function of (nonexpressor of PR genes1) NPR1 (Dong2001; Pieterse and Van Loon 2004). Oxidized NPR1 forms oligomers and is localized in the cytosol (Mou et al.2003). However, the redox state changes associated with SA production reduce NPR1. The resultant monomeric form is subsequently nuclear localized where it interacts with a class of basic domain/leucine zipper transcription factors to mediate the induction of SA-dependent genes (Despres et al.2003; Mou et al.2003; Spoel et al.2003; Dong2004). The transcriptional regulatory region of NPR1contains W-box binding sites for WRKY transcription factors. Interestingly, several WRKY transcription factors are also implicated in regulating SA-dependent defense responses as well as the SA/JA cross talk (Eulgem et al.2000). WRKY70 is one of the few WRKYs demonstrated to play a role in the cross talk by positively regulating SA-mediated defenses and repressing JA responses (Journot-Catalino et al. 2006; Mao et al.2007). Antisense suppression of WRKY70 results in the activation of COI1-dependent genes, whereas overexpression ofWRKY70results in the constitutive SA signaling and the suppression of jasmonate-response genes (Li et al.2002; Li et al.2004).
Mitogen-activated protein kinases (MAPKs) are also key players in JA/SA cross talk. MAPKs regulate plant responses to biotic challenges (Jonak et al. 2002).
Arabidopsis mpk4mutants are JA insensitive, produce high levels of SA, and are resistant toP. syringae(Petersen et al.2000).
5.2.3 Cross Talk of JA/ET
JA has been found to be conjugated to 1-aminocyclopropane-1-carboxylate (ACC), the precursor of ethylene. Although the function of this conjugated product is yet to be identified, its accumulation in plants may be relevant to the reported cross talk between JA and ethylene (ET) in regulating the expression of defense-related genes (Xu et al.1994; O’Donnell et al.1998; Penninckx et al.1998; Rojo and Solano 2003). Ethylene and jasmonates can act in a synergistic or antagonistic manner depending on the stress encountered by the plant.
Pharmacological and mutant studies show that JA and ET act in synergy in plant defense against fungal pathogens (Pieterse et al.1998; van Wees et al.1999; Ellis and Turner2001; Thomma et al.2001; Berrocal-Lobo and Molina2004).PLANT DEFENSIN 1.2(PDF1.2) andETHYLENE RESPONSE FACTOR 1 (ERF1), which
encode an antimicrobial protein and a transcription factor, respectively, are highly induced upon infection with fungi, such asA. brassicicola(Penninckx et al.1996;
Penninckx et al.1998). To achieve full expression of the two genes, the activation of both JA and ET signaling pathways is required (Penninckx et al.1998). Lorenzo et al. (2003) demonstrated that ERF1 regulates the expression ofPDF1.2.There- fore, upon pathogen infection, the JA and ET signaling pathways may converge to activate the expression of ERF1, which in turn regulates PDF1.2 expression. Consistent with this notion, overexpressing ERF1 results in the expression of defense-related genes that are responsive to both JA and ET (Lorenzo et al.
2003). Furthermore, overexpressing ERF1 in coi1 rescues expression of genes involved in fungal defense responses (Lorenzo et al.2003). Therefore, the con- certed action of JA and ET acts concomitantly to activate the defense responses against fungal pathogens.
On the other hand, antagonism between jasmonates and ET is also evident in wounding and insect herbivory responses (Rojo et al. 1999; Shoji et al. 2000;
Lorenzo et al.2004). As previously discussed, MYC2 is required for induction of expression of many JA-regulated genes. Expression of these genes responds to wounding and arthropod herbivory (Boter et al. 2004; Lorenzo et al. 2004;
Dombrecht et al.2007). Interestingly, wound-induced genes through the action of MYC2 are repressed by ERF1 (Lorenzo et al.2004). Therefore, it appears that genes activated by JA but repressed by ET are part of the transcriptional response to insect herbivory attacks, whereas genes that require both phytohormones for full expres- sion are more likely involved in protecting the plant against microbial pathogens.
6 Systemic Resistance
Biotic stress may not only launch defense responses at the wounding site but also systemic expression of defense-related genes and protection of healthy tissue from future attacks (Conrath et al.2006; Frost et al.2007; Ton et al.2007; Chassot et al.
2008; Erb et al.2008; Heil and Ton2008; Vlot et al.2008). Through the use of plant mutants defective in jasmonate synthesis or perception, it has been shown that these oxylipins regulate systemic resistance (Zhang and Baldwin1997; Li et al.2002;
Thorpe et al.2007). For example, tomato grafting experiments between wild-type and COI1-deficient plants show that response to jasmonates is necessary for recognizing the systemic wound signal in distal undamaged leaves but not required for production of the signal in damaged leaves (Li et al.2002). Intact JA biosyn- thetic machinery only in the rootstock is required for the wound-induced systemic expression of JA-dependent genes in the unwounded distal leaves of the scion (Li et al.2002; Lee and Howe2003; Li et al.2005). These findings as well as the ability of jasmonates to translocate through the vascular system indicate that JA and/or its related metabolites that are recognized by COI1 constitute part if not all of the systemic transmitted wound signal.
7 Thigmomorphogenesis and Jasmonates
Plants respond to repetitive touch or mechanostimulation by undergoing changes in growth that generally include a decrease in elongation growth and an increase in radial expansion (Braam2005; Chehab et al.2009). Although molecular responses to touch have been identified (e.g., Braam and Davis1990; Braam1992; Xu et al.
1995; Purugganan et al.1997; Lee et al.2005) and implications for touch-induced genes in mechanoresponses are reported (Sistrunk et al. 1994; McCormack and Braam2003; Delk et al.2005; Wang et al.2011), there have been few insights into how thigmomorphogenesis is regulated. Over the past decade or so, some studies have implicated jasmonates in plant mechanoresponses. For example, Stelmach et al. (1998) showed that the application of coronatine on the common bean (Phaseolus vulgaris) causes physiological responses reminiscent of thigmomor- phogenesis. Mechanically impeding root growth causes an increase in JA produc- tion and a temporary inhibition of root elongation.Arabidopsis cev1mutants with constitutively high levels of JA show thigmomorphogenetic-like phenotypes (Ellis et al.2002). The physical impedance ofBryonia dioicacauses elevation of intra- cellular MeJA levels in the tendrils. The application of MeJA, or its precursor 12- OPDA, onB. dioicaelicits a coiling tendril response (Weiler et al.1993). All these findings suggest jasmonates might be playing a role in linking the touch stimulus with the transduction pathway leading to the observed thigmomorphogenetic responses. However, further investigations are necessary to determine whether jasmonates are required for the mechanoresponsive pathway. Such a task can be achieved by utilizing jasmonate mutants defective either in their ability to synthe- size jasmonates, such asaos(Park et al.2002; Chehab et al.2008), or in their ability to perceive jasmonates, such ascoi1(Feys et al.1994).
8 Concluding Remarks
Jasmonate-mediated defense responses to biotic attacks are crucial to the survival of plants. Since constitutive defense activation is energetically costly and in conflict with biotrophic pathogen defense, perhaps plants have evolved the JA regulatory pathway for switching on these responses only under appropriate conditions for optimal survival and growth. JA responses can be either direct or indirect but can be specific depending on the invading pest. Although major accomplishments have been achieved in understanding the mechanisms and regulation of jasmonate signaling, many unanswered questions remain to be resolved. The use of existing jasmonate mutants as well as the identification of new ones is crucial for further unraveling of the remaining mysteries of these powerful signaling molecules.
Acknowledgment Research in our lab related to this topic is based upon work supported by the National Science Foundation under Grant No. MCB 0817976 to JB
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