Plant Cell Advance Online Publication
Published on November 13, 2003; 10.1105/tpc.017301
Received September 11, 2003
Accepted October 6, 2003
Plastidial Fatty Acid Signaling Modulates Salicylic Acid- and Jasmonic Acid-Mediated
Defense Pathways in the Arabidopsis ssi2 Mutant
Aardra Kachroo 1, Ludmila Lapchyk 1, Hirotada Fukushigae 2, David Hildebrand 2, Daniel Klessig 3, and Pradeep Kachroo 4*
1
Department of Plant Pathology, University of Kentucky, Lexington, Kentucky 40546
2
Department of Agronomy, University of Kentucky, Lexington, Kentucky 40546
3
Boyce Thompson Institute, Tower Road, Ithaca, New York 14853
4
Department of Plant Pathology, University of Kentucky, Lexington, Kentucky 40546;
Boyce Thompson Institute, Tower Road, Ithaca, New York 14853
* To whom correspondence should be addressed. E-mail: pk62{at}uky.edu.
A mutation in the Arabidopsis gene ssi2/fab2, which encodes stearoyl-acyl
carrier protein desaturase (S-ACP-DES), results in the reduction of oleic acid (18:1)
levels in the mutant plants and also leads to the constitutive activation of NPR1-dependent
and -independent defense responses. By contrast, ssi2 plants are compromised
in the induction of the jasmonic acid (JA)-responsive gene PDF1.2
and in resistance to the necrotrophic pathogen Botrytis cinerea. Although
S-ACP-DES catalyzes the initial desaturation step required for JA biosynthesis, a
mutation in ssi2 does not alter the levels of the JA precursor linolenic
acid (18:3), the perception of JA or ethylene, or the induced endogenous levels of
JA. This finding led us to postulate that the S-ACP-DES-derived fatty acid
(FA) 18:1 or its derivative is required for the activation of certain JA-mediated
responses and the repression of the salicylic acid (SA) signaling pathway. Here,
we report that alteration of the prokaryotic FA signaling pathway in plastids, leading
to increased levels of 18:1, is required for the rescue of ssi2-triggered
phenotypes. 18:1 levels in ssi2 plants were increased by performing epistatic
analyses between ssi2 and several mutants in FA pathways that cause an increase
in the levels of 18:1 in specific compartments of the cell. A loss-of-function mutation
in the soluble chloroplastic enzyme glycerol-3-phosphate acyltransferase (ACT1
) completely reverses SA- and JA-mediated phenotypes in ssi2. In contrast
to the act1 mutation, a loss-of-function mutation in the endoplasmic reticulum-localized
 6 oleate desaturase (FAD2) does not alter SA- or JA-related phenotypes
of ssi2. However, a mutation in the plastidial membrane-localized
6 desaturase (FAD6) mediates a partial rescue of ssi2-mediated
phenotypes. Although ssi2 fad6 plants are rescued in their morphological
phenotypes, including larger size, absence of visible lesions, and straight leaves,
these plants continue to exhibit microscopic cell death and express the PR-1
gene constitutively. In addition, these plants are unable to induce the expression
of PDF1.2 in response to the exogenous application of JA. Because the
act1 mutation rescues all of these phenotypes in ssi2 fad6 act1 triple-mutant
plants, act1-mediated reversion may be mediated largely by an increase in
the free 18:1 content within the chloroplasts. The reversion of JA responsiveness
in ssi2 act1 plants is abolished in the ssi2 act1 coi1 triple-mutant
background, suggesting that both JA- and act1-generated signals are required
for the expression of the JA-inducible PDF1.2 gene. Our conclusion that
FA signaling in plastids plays an essential role in the regulation of SSI2-mediated
defense signaling is further substantiated by the fact that overexpression of the
N-terminal-deleted SSI2, which lacks the putative plastid-localizing transit
peptide, is unable to rescue ssi2-triggered phenotypes, as opposed to overexpression
of the full-length protein.
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