Abstract
Embryophyte genomes typically encode multiple 13-lipoxygenases (13-LOXs) that initiate the synthesis of wound-inducible mediators called jasmonates. Little is known about how the activities of these different LOX genes are coordinated. We found that the four 13-LOX genes in Arabidopsis thaliana have different basal expression patterns. LOX2 expression was strong in soft aerial tissues, but was excluded both within and proximal to maturing veins. LOX3 was expressed most strongly in circumfasicular parenchyma. LOX4 was expressed in phloem-associated cells, in contrast to LOX6, which is expressed in xylem contact cells. To investigate how the activities of these genes are coordinated after wounding, we carried out gene expression analyses in 13-lox mutants. This revealed a two-tiered, paired hierarchy in which LOX6, and to a lesser extent LOX2, control most of the early-phase of jasmonate response gene expression. Jasmonates precursors produced by these two LOXs in wounded leaves are converted to active jasmonates that regulate LOX3 and LOX4 gene expression. Together with LOX2 and LOX6, and working downstream of them, LOX3 and LOX4 contribute to jasmonate synthesis that leads to the expression of the defense gene VEGETATIVE STORAGE PROTEIN2 (VSP2). LOX3 and LOX4 were also found to contribute to defense against the generalist herbivore Spodoptera littoralis. Our results reveal that 13-LOX genes are organised in a regulatory network, and the data herein raise the possibility that other genomes may encode LOXs that act as pairs.
Highlights
Lipoxygenases (LOXs) function to produce lipid mediators that operate in a broad range of processes, many of which are related to defense in animals [1] and in plants [2]
Our results reveal that 13-LOX genes are organised in a regulatory network, and the data raise the possibility that other genomes may encode LOXs that act as pairs
The Arabidopsis thaliana genome encodes six LOXs of which four are 13-LOXs, where “13” refers to the carbon atom in polyunsaturated 18-carbon fatty acids that are preferentially oxygenated by the LOX. 13-LOXs incorporate molecular oxygen into α-linolenic acid to produce its 13(S)-hydroperoxide [3], a molecule that is transformed into jasmonates which regulate wound-induced defense gene expression [4,5]
Summary
Lipoxygenases (LOXs) function to produce lipid mediators that operate in a broad range of processes, many of which are related to defense in animals [1] and in plants [2]. 13-LOXs incorporate molecular oxygen into α-linolenic acid to produce its 13(S)-hydroperoxide [3], a molecule that is transformed into jasmonates which regulate wound-induced defense gene expression [4,5]. In theory, jasmonates produced via the activity of any 13-LOX could be dispersed to different cell types capable of expressing other LOXs that make jasmonate precursors This raises an obvious question: how is the activity of the four 13-LOX genes in Arabidopsis coordinated?. The experiments that revealed this role involved the genetic removal of each of the three other 13-LOXs through producing a lox lox lox triple mutant In this plant, LOX6 functioning alone was capable of maintaining the defense of emerging leaves and shoot apical tissues in Arabidopsis rosettes [15]. Our results revealed a lipoxygenase network that operates to coordinate jasmonate synthesis and defense responses in wounded leaves
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