Multiple Hormones Act Sequentially to Mediate a Susceptible Tomato Pathogen Defense Response

Abstract

Phytohormones regulate plant responses to a wide range of biotic and abiotic stresses. How a limited number of hormones differentially mediate individual stress responses is not understood. We have used one such response, the compatible interaction of tomato (Lycopersicon esculentum) and Xanthomonas campestris pv vesicatoria (Xcv), to examine the interactions of jasmonic acid (JA), ethylene, and salicylic acid (SA). The role of JA was assessed using an antisense allene oxide cyclase transgenic line and the def1 mutant to suppress Xcv-induced biosynthesis of jasmonates. Xcv growth was limited in these lines as was subsequent disease symptom development. No increase in JA was detected before the onset of terminal necrosis. The lack of a detectable increase in JA may indicate that an oxylipin other than JA regulates basal resistance and symptom proliferation. Alternatively, there may be an increase in sensitivity to JA or related compounds following infection. Hormone measurements showed that the oxylipin signal must precede subsequent increases in ethylene and SA accumulation. Tomato thus actively regulates the Xcv-induced disease response via the sequential action of at least three hormones, promoting expansive cell death of its own tissue. This sequential action of jasmonate, ethylene, and SA in disease symptom development is different from the hormone interactions observed in many other plant-pathogen interactions.

Involvement of Ethylene in Stress-Induced Expression of the TLC1.1 Retrotransposon from Lycopersicon chilense Dun.

“…In these experiments, the transcription of TLC1 was activated in response to wounding and Onozuka R10 cellulase in a similar way to that described for other active retrotransposons (Pouteau et al, 1991;Mhiri et al, 1997;Takeda et al, 1998Takeda et al, , 1999. These results correlate with the induction of TLC1 in response to ethylene, methyl jasmonate, and salicylic acid, which were described to be involved in signal transduction pathways associated to the abovementioned stress conditions (O'Donnell et al, 1996(O'Donnell et al, , 2003.…”

“…Several studies have revealed the existence of ethylene-dependent signaling pathways activated in response to pathogen attack (Dong, 1998;Guo et al, 2000;Díaz et al, 2002), wounding (O'Donnell et al, 1996;Watanabe et al, 2001), UV irradiation, and ozone exposure (Wang et al, 2002). In such cases, ethylene acts in a coordinated way with other signaling molecules such as salicylic acid and jasmonic acid, suggesting the existence of a complex network of regulatory pathways (Dong, 1998;Wang et al, 2002;O'Donnell et al, 2003;Guo and Ecker, 2004). Consequently, the residual GUS activity detected in protoplasts transformed with the single or double TRS mutant constructs (Fig.…”

LeMPK3 Is a Mitogen-activated Protein Kinase with Dual Specificity Induced during Tomato Defense and Wounding Responses

“…It has been recently shown, by monitoring bacterial growth in tomato mutants defective in jasmonic acid or ethylene signaling, that these two hormones do not affect resistance to Xcv, but they do affect the extent of cell death (39). Interestingly, activation in tobacco of MAP kinase cascades, which include the NtMEK2 MAPKK and the SIPK and WIPK MAP kinases, has been reported to cause an increase of ethylene levels (18).…”

XopD SUMO Protease Affects Host Transcription, Promotes Pathogen Growth, and Delays Symptom Development inXanthomonas-Infected Tomato Leaves

“…Buchanan-Wollaston et al, 2005). Considering that Xcv infection induces SA levels (O'Donnell et al, 2003;Block et al, 2005) and XopD action delays leaf chlorosis and necrosis ( Figure 1B), we hypothesized that XopD action might be affecting SA levels in the diseased tissue. To test this, we estimated the SA pool (i.e., free SA plus existing methyl salicylate) in susceptible VF36 leaves inoculated with Xcv over the course of 10 d ( Figure 3A).…”