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. 2006 Jan;140(1):249-62.
doi: 10.1104/pp.105.072348. Epub 2005 Dec 23.

The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death

Luis A J Mur  1 , Paul Kenton, Rainer Atzorn, Otto Miersch, Claus Wasternack
Affiliations

The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death

Luis A J Mur et al. Plant Physiol. 2006 Jan.

Abstract

Salicylic acid (SA) has been proposed to antagonize jasmonic acid (JA) biosynthesis and signaling. We report, however, that in salicylate hydroxylase-expressing tobacco (Nicotiana tabacum) plants, where SA levels were reduced, JA levels were not elevated during a hypersensitive response elicited by Pseudomonas syringae pv phaseolicola. The effects of cotreatment with various concentrations of SA and JA were assessed in tobacco and Arabidopsis (Arabidopsis thaliana). These suggested that there was a transient synergistic enhancement in the expression of genes associated with either JA (PDF1.2 [defensin] and Thi1.2 [thionin]) or SA (PR1 [PR1a-beta-glucuronidase in tobacco]) signaling when both signals were applied at low (typically 10-100 microm) concentrations. Antagonism was observed at more prolonged treatment times or at higher concentrations. Similar results were also observed when adding the JA precursor, alpha-linolenic acid with SA. Synergic effects on gene expression and plant stress were NPR1- and COI1-dependent, SA- and JA-signaling components, respectively. Electrolyte leakage and Evans blue staining indicated that application of higher concentrations of SA + JA induced plant stress or death and elicited the generation of apoplastic reactive oxygen species. This was indicated by enhancement of hydrogen peroxide-responsive AoPR10-beta-glucuronidase expression, suppression of plant stress/death using catalase, and direct hydrogen peroxide measurements. Our data suggests that the outcomes of JA-SA interactions could be tailored to pathogen/pest attack by the relative concentration of each hormone.

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Figures

Figure 1.
Figure 1.
Octadecanoid rises in wild type and salicylate hydroxylase (SH-L)-expressing transgenic tobacco plants following challenge with P. syringae pv phaseolicola. A, JA accumulation in wild type and salicylate hydroxylase (SH-L)-expressing (SH-L) transgenic Samsun NN tobacco at various times following challenge with the avirulent bacterium P. syringae pv phaseolicola detected using JA anti-sera. Inset, SA and JA accumulation in wild-type tobacco cv Samsun NN following challenge with P. syringae pv phaseolicola. All data are presented as mean (n = 3) nmol g−1 fresh weight (fwt) ± se. B, Alternative routes to the synthesis of JA are indicated. Lipoxygenation of chloroplastic C16:3 or C18:3 lipids leads ultimately to the formation of dnOPDA and OPDA, respectively. These are transported to the peroxisome where the acyl chain is shortened by successive rounds of β-oxidation to form JA. C, OPDA, dnOPDA, and JA accumulation in wild-type (wt) tobacco Samsun NN and SH-L transgenic Samsun NN tobacco plants at 12 and 24 h following inoculation with P. syringae pv phaseolicola (Psph) and a HR noneliciting P. syringae pv phaseolicola hrpL strain (Psph hrpL) detected using GC-MS. All data are presented as mean (n = 3) nmol g−1 fwt ± se. Significant differences (P < 0.01) between levels in wild-type and SH-L plants are indicated by two asterisks. NS, Nonsignificant differences.
Figure 2.
Figure 2.
SA interactions with JA or LN on PR1a-GUS expression in transgenic tobacco. GUS activity in explants of transgenic tobacco at 24 h following treatment with water or 10, 100, 250 μm SA with either 0, 10, 100, 250 μm JA (A) or 0, 10, 100, 250 μm α-LN (B). Data are given as mean (n = 6) GUS activity; pmol 4-methylumbelliferone min−1 explant ± se.
Figure 3.
Figure 3.
Effect of SA interactions with JA or LN on PDF1.2, Thi, and PR1 expression in explants of Arabidopsis ecotype Columbia (Col-0). A, PDF1.2 and Thi2.1 transcript accumulation in Arabidopsis Col-0 explants (the central inner 0.5-cm diameter core of a 1-cm disc; see “Materials and Methods”) at 12 h following treatment with 10 μm JA and increasing concentrations of SA (from 8–500 μm) or 4BA (from 125–500 μm), or 500 μm SA alone. The ethidium bromide-stained gel showing ribosomal RNA (rRNA) is presented to demonstrate equal loading. Northern results for two biological replicates for each experiment were scanned by densitometry to obtain numerical values. Values for each replicate were expressed as a percentage of the maximum value within the same replicate. The graph gives the mean percentage for each treatment and the range between replicates. B, Graphical representation of PDF1.2 transcript accumulation in Arabidopsis explants at 12 h following treatment with 10 μm LN and increasing concentrations of SA (from 15–500 μm), or 4BA (from 125–500 μm), or 500 μm SA alone. C, PR1 transcription in Arabidopsis explants at 12 h following treatment with 10 μm SA and increasing concentrations of JA or LN (from 8–500 μm) or only with JA, LN (125–500 μm), or 500 μm SA alone. Graphs B and C were derived as described in A.
Figure 4.
Figure 4.
Effect of SA interactions with JA on PDF1.2 and PR1 transcript accumulation in Arabidopsis npr1-1 and coi1-1. PR1 and PDF1.2 transcription in explants (the central inner 0.5-cm diameter core of a 1-cm disc) from Arabidopsis wild-type Col-0, npr1-1, and coi1-1 in untreated controls and at 12 h following treatment with 50 μm JA and 50 μm SA, either alone or in combination. The ethidium bromide-stained gel showing ribosomal RNA (rRNA) is presented to demonstrate equal loading.
Figure 5.
Figure 5.
SA-JA-mediated initiation of plant stress or cell death in tobacco. A, Visible cell death in tobacco leaf panels at 24 h following injection with 0.5 mm SA and 0.5 mm, either alone or in combination. B, Changes in the conductivity (electrolyte leakage) of solutions bathing explants (1-cm diameter cores) of tobacco at 24 h following treatment with various concentrations of JA (0, 10, 100, 200, and 500 μm) with SA (0, 10, 100, 200, and 500 μm). Results are given as mean conductivity change; μS cm2 (n = 6) ± se. C, Retention of Evans blue stain in explants at 24 and 72 h following treatment with 0, 100, 200, and 500 μm JA in combination with 0, 100, 200, or 500 μm SA. Stain retention is expressed as fold increase in mean staining of untreated explants (0 μm SA + JA) at corresponding time points (n = 6) ± se. D, Changes in the conductivity (electrolyte leakage) of solutions bathing explants (1-cm diameter cores) of tobacco in untreated samples, following treatment with 200 μm SA or treatment with 200 μm SA to which 200 μm JA was added after 2 h, as well as the converse scenario where explants were treated with 200 μm JA and 200 μm JA to which 200 μm SA was added at 2 h. Results are given as mean (n = 6) conductivity change, μS cm2 ± se.
Figure 6.
Figure 6.
SA interactions with jasmonates on AoPR10-GUS expression in transgenic tobacco and the generation of oxidative stress. AoPR10-GUS activity in explants of transgenic tobacco at 24 (A) and 72 h (B) following treatment with water (0) or 10, 100, or 250 μm SA with either 0, 10, 100, or 250 μm JA or at 24 h with 0, 10, 100, or 250 μm α-LN (C). D, AoPR10-GUS activity in tobacco leaves at 24 h following injection of water; 100 μm JA alone or a combination of 100 μm SA + 100 μm JA and also100 μm JA with 50 units mL−1 catalase (CAT) or 100 μm SA + 100 μm JA with CAT. E, Changes in the conductivity (electrolyte leakage) of solutions bathing tobacco explants (1-cm diameter cores) from leaf panels previously inoculated with water and 50 units mL−1 CAT or 250 μm JA + 250 μm SA with or without and 50 units mL−1 CAT. Results are given as mean (n = 6) conductivity change, μS cm2. F, H2O2 content in one third of tobacco leaves at 12 h following injection either with water (0), 100 μm JA, 100 μm SA, or 100 μm JA + 100 μm SA compared to another third of the leaf inoculated where 50 units mL−1 CAT was added to either water (0), 100 μm JA, 100 μm SA, or 100 μm JA + 100 μm SA. For each sample the H2O2 content of the untreated third of the same leaf was subtracted from the value obtained for the treated parts. Results are given as mean (n = 6) samples H2O2 content (pmol g−1 fwt) ± se.
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