DONGLE and DEFECTIVE IN ANTHER DEHISCENCE1 Lipases Are Not Essential for Wound- and Pathogen-Induced Jasmonate Biosynthesis: Redundant Lipases Contribute to Jasmonate Formation      

Abstract

(N.S., S.B., M.J.M.)Lipases are involved in the generation of jasmonates, which regulate responses to biotic and abiotic stresses. Two sn-1-specific acyl hydrolases, DEFECTIVE IN ANTHER DEHISCENCE1 (DAD1) and DONGLE (DGL), have been reported to be localized in plastids and to be essential and sufficient for jasmonate biosynthesis in Arabidopsis (Arabidopsis thaliana) leaves. Here, we show that levels of 12-oxo-phytodienoic acid (OPDA) and jasmonic acid in three different DGL RNA interference lines and the dad1 mutant were similar to wild-type levels during the early wound response as well as after Pseudomonas infection. Due to the lack of sn-2 substrate specificity, synthesis of dinor OPDA was not expected and also not found to be affected in DGL knockdown and DGL-overexpressing lines. As reported, DAD1 participates in jasmonate formation only in the late wound response. In addition, DGL protein was found to be localized in lipid bodies and not in plastids. Furthermore, jasmonate levels in 16 additional mutants defective in the expression of lipases with predicted chloroplast localization did not show strong differences from wild-type levels after wounding, except for a phospholipase A (PLA) PLA-Ig1 (At1g06800) mutant line that displayed diminished wound-induced dinor OPDA, OPDA, and jasmonic acid levels. A quadruple mutant defective in four DAD1-like lipases displayed similar jasmonate levels as the mutant line of PLA-Ig1 after wounding. Hence, we identify PLAIg1 as a novel target gene to manipulate jasmonate biosynthesis. Our results suggest that, in addition to DAD1 and PLA-Ig1, still unidentified enzymes with sn-1 and sn-2 hydrolase activity are involved in wound-and pathogen-induced jasmonate formation, indicating functional redundancy within the lipase family.

Jasmonate Biosynthesis, Perception and Function in Plant Development and Stress Responses

“…Mutant lines of 18 different lipases, including DGL and DAD1, have been assessed for wound-induced jasmonate levels. However, none of the single lipase mutants or the quadruple mutant line (pla-Iβ2 / Iγ1 / Iγ2 / Iγ3) were completely abolished in JA formation under basal and wound-induced conditions (Ellinger et al, 2010), indicating that multiple lipases with both sn-1 and sn-2 (or dual sn-1/sn-2) galactolipid substrate specificity participate in JA formation in plant.…”

“…In addition to these seven PLA1 lipases (DAD1-like lipases), Ellinger et al (2010), identified 14 additional putative lipases with predicted plastid transit peptides suggesting, up to 21 lipases may contribute to JA production in Arabidopsis. Mutant lines of 18 different lipases, including DGL and DAD1, have been assessed for wound-induced jasmonate levels.…”

Jasmonic acid regulates spikelet development in rice

“…Two Arabidopsis phospholipases, DONGLE (DGL) and DEFECTIVE IN ANTHER DEHISCENCE1 (DAD1), release a-linolenic acid (C18:3) from chloroplastic membrane lipids as the first step of JA biosynthesis 25,26 . Recent evidence showed that DGL and DAD1 are not essential for wound-or pathogeninduced JA biosynthesis and that other lipases may be involved in stress-induced JA production, suggesting that plants may use different lipases for jasmonate biosynthesis in various biological processes 27 . In the well-characterized Arabidopsis JA signalling pathway, JA is perceived by the receptor CORONATINE-INSENSITIVE1 (COI1), an F-box protein that activates the expression of JA-responsive genes by degrading the JAZ (jasmonate ZIM-domain) repressors [28][29][30][31][32][33][34][35] .…”

Lipases and the biosynthesis of free oxylipins in plants

“…7,8 Ellinger and coworkers have revisited the participation of these and additional lipases in the supply of substrates for JA biosynthesis in Arabidopsis. 9 The results of the study indicated that the woundand pathogen-mediated accumulation of JA in Arabidopsis is determined by multiple lipases acting at different stages of the wound and infection response. Consistent with this conclusion, it has been recently reported that the transcriptional control of Arabidopsis DAD1-like lipases (DLL) is under regulation of a complex signaling network.…”

“…lipid-bound oxylipins), 11,12 the lipase-catalyzed release of these esterified oxylipins into the free oxylipin pool adds an additional level of complexity to the regulation and dynamics of free oxylipin accumulation. 9,13 Similar to DAD1, DGL and AtPLAI, N. attenuata GLA1 belongs to the 14 By definition, phospholipases class A (PLA) de-esterify acyl groups from phospholipids, but several lipases involved in JA formation have been shown to also cleave in vitro acyl groups from galactolipids and triacylglycerols. 1,6 Thus, we have previously adopted the more general name glycerolipase A (GLA) to refer to lipases class A involved in the biogenesis of free oxylipins in plants.…”