The Rapid Induction of Glutathione S-Transferases AtGSTF2 and AtGSTF6 by Avirulent Pseudomonas syringae is the Result of Combined Salicylic Acid and Ethylene Signaling

Abstract

The expression of two members of the glutathione S-transferase (GST) multigene family was studied in Arabidopsis plants inoculated with an avirulent strain of Pseudomonas syringae pv. tomato (Pst). Accumulation of AtGSTF2 and AtGSTF6 transcripts started 4 and 2 h after inoculation, respectively, and clearly preceded the induction of the pathogenesis-related PR-1 gene. The aim of this work was to find the reason for the faster induction of the two GSTs compared with classical salicylic acid (SA)-regulated PR-proteins. Expression studies in Pst-inoculated SA-signaling mutants NahG and npr1 revealed that induction of both GSTs was SA-dependent and partially NPR1-independent. The induction of AtGSTF2 by Pst was also strongly repressed in the ethylene insensitive etr1 mutant. Both GSTs were induced by low amounts of SA (0.1 mM) and ethylene (0.1 ppm) while PR-1 gene expression was unaffected by ethylene. Interestingly, ethylene was about 50-fold less effective in NahG compared with wild-type plants thus suggesting a potentiation effect of SA on ethylene-induced accumulation of AtGST transcripts. Increased AtGST expression in plants inoculated with Pst correlated with increased production of SA and ethylene. However, the initial phase of AtGSTF6 induction was independent of SA- and ethylene-signaling. The jasmonate (JA)-insensitive mutant jar1 showed normal induction kinetics for both GSTs. Our data support the hypothesis that full expression of the pathogen-induced AtGSTF2 and, to a lesser extent AtGSTF6, is the result of combined SA- and ethylene-signaling and that early AtGSTF6 expression depends on additional unknown signaling mechanisms.

Early genomic responses to salicylic acid in Arabidopsis

“…Consistently, in Arabidopsis, SA was required to restrict the oxidative stress and foster plant acclimation after transient exposure to high light intensity (Mateo et al 2006). Interestingly, we and others found that SA uses a transient kinetics to activate genes coding for detoxifying or antioxidant enzymes such as glutathione S-transferases (GSTs) and glycosyltransferases (GTs) (Wagner et al 2002;Lieberherr et al 2003;Sappl et al 2004;Uquillas et al 2004;Blanco et al 2005;Langlois-Meurinne et al 2005). Besides activating stress defenses, SA is known to inhibit JA-and auxin-mediated responses, as part of the SA-mediated disease-resistance mechanism (Fujita et al 2006;Ndamukong et al 2007;Wang et al 2007).…”

Multilayered Regulation of Ethylene Induction Plays a Positive Role in Arabidopsis Resistance against Pseudomonas syringae

“…This is consistent with a positive role of SA in both local immunity and the SAR response. Previously, it was reported that ethylene production in plants inoculated with Pst-avrRpt2 is partially compromised in NahG plants (Lieberherr et al, 2003). However, ethylene induction by Pst without the avrRpt2 effector was not characterized; therefore, it was unclear whether the SAdependent ethylene induction is part of the PTI or ETI.…”

Glutathione Transferases

“…They are not distinguishable from each other in microarray experiments, but PCR experiments have shown that the two GSTs are similarly responsive to stress treatments (Lieberherr et al, 2003), being strongly and rapidly induced by treatment with avirulent Pseudomonas syringae. Other PCR experiments, together with proteomic data, have shown GSTF7 to be less abundant, but more strongly SA-inducible, than GSTF6 (Sappl et al, 2004).…”

“…GSTF3 (At2g02930) is almost identical to GSTF2, but based on transcript abundance is expressed at much lower levels than GSTF2 (Lieberherr et al, 2003;Smith et al, 2003), and has not been studied in detail.…”