Role of β-Oxidation in Jasmonate Biosynthesis and Systemic Wound Signaling in Tomato

Abstract

Jasmonic acid (JA) is a lipid-derived signal that regulates plant defense responses to biotic stress. Here, we report the characterization of a JA-deficient mutant of tomato (Lycopersicon esculentum) that lacks local and systemic expression of defensive proteinase inhibitors (PIs) in response to wounding. Map-based cloning studies demonstrated that this phenotype results from loss of function of an acyl-CoA oxidase (ACX1A) that catalyzes the first step in the peroxisomal b-oxidation stage of JA biosynthesis. Recombinant ACX1A exhibited a preference for C12 and C14 straight-chain acyl-CoAs and also was active in the metabolism of C18 cyclopentanoid-CoA precursors of JA. The overall growth, development, and reproduction of acx1 plants were similar to wild-type plants. However, the mutant was compromised in its defense against tobacco hornworm (Manduca sexta) attack. Grafting experiments showed that loss of ACX1A function disrupts the production of the transmissible signal for wound-induced PI expression but does not affect the recognition of this signal in undamaged responding leaves. We conclude that ACX1A is essential for the b-oxidation stage of JA biosynthesis and that JA or its derivatives is required both for antiherbivore resistance and the production of the systemic wound signal. These findings support a role for peroxisomes in the production of lipid-based signaling molecules that promote systemic defense responses.

Role of cis-12-Oxo-Phytodienoic Acid in Tomato Embryo Development

“…SlAOC promoter activity and AOC protein accumulation was analyzed in developing wild-type seeds and isolated embryos. Under the growth conditions used in our experiments, the spr2 mutant was found to be delayed in embryo development, whereas the acx1a mutant exhibited normal seed formation as previously published (Li et al, 2005). Therefore, we analyzed the oxylipin profile of developing wild-type seeds and programmed cell death (PCD) of developing wildtype and spr2 seeds.…”

“…To confine the number of putative oxylipins downstream of the v-3-fatty acid desaturase reaction, we inspected acx1 plants. This mutant is affected in ACX1A, one of the two genes known so far that encode acyl-CoA oxidases in tomato (Li et al, 2005). ACX1A catalyzes the first step in peroxisomal fatty acid b-oxidation and is involved in JA biosynthesis.…”

“…Although the degree of female sterility varies, at least one of the tomato mutants affected in JA biosynthesis also has reduced seed set. This concerns spr2, which is blocked at the plastidic v-3-fatty acid desaturase FAD7 gene required for JA biosynthesis (Li et al, 2003), whereas acx1a, which is blocked in oxylipin b-oxidation during JA biosynthesis, is indistinguishable in seed set to wild type (Li et al, 2005). Under conditions that represent a generally low-stress environment insufficient to induce jasmonate production in wild-type plants, seed set of spr2 plants is strongly affected, whereas acx1a plants exhibit still sufficient seed set.…”

“…Under conditions that represent a generally low-stress environment insufficient to induce jasmonate production in wild-type plants, seed set of spr2 plants is strongly affected, whereas acx1a plants exhibit still sufficient seed set. In contrast, fieldgrown spr2 plants produce a higher number of seeds showing higher germination rates relative to seeds obtained from greenhouse-grown plants (Li et al, 2003(Li et al, , 2005. This suggests that seed set in spr2 is influenced by maternal growing conditions and that stress conditions might result in residual levels of JA or other oxylipins sufficient for female fertility (Li et al, 2003(Li et al, , 2005.…”

Biosynthesis of plant‐derived flavor compounds

“…An acyltransferase catalyzes the formation of 3Z-hexenyl acetate from 3Z-hexenol and acetyl CoA, and 2-alkenal reductase can reduce 2E-hexenal to hexanal Mano et al, 2002). The reaction sequence leading from a-linolenic acid to the signaling molecule jasmonic acid involves the enzymes 13-LOX, allene oxide synthase, allene oxide cyclase and 12-oxo-phytodienoic acid reductase, followed by three successive b-oxidation steps (Figure 7) (Howe and Schilmiller, 2002;Li et al, 2005). Jasmonic acid and its volatile methyl ester act as phytohormones and are involved in plant responses to stress and developmental processes.…”