Oxo-Phytodienoic Acid-Containing Galactolipids in Arabidopsis: Jasmonate Signaling Dependence

Abstract

The jasmonate family of phytohormones, as represented by 12-oxo-phytodienoic acid (OPDA), dinor-phytodienoic acid (dn-OPDA), and jasmonic acid in Arabidopsis (Arabidopsis thaliana), has been implicated in a vast array of different developmental processes and stress responses. Recent reports indicate that OPDA and dn-OPDA occur not only as free acids in Arabidopsis, but also as esters with complex lipids, so-called arabidopsides. Recently, we showed that recognition of the two bacterial effector proteins AvrRpm1 and AvrRpt2 induced high levels of a molecule consisting of two OPDAs and one dn-OPDA esterified to a monogalactosyl diacylglycerol moiety, named arabidopside E. In this study, we demonstrate that the synthesis of arabidopsides is mainly independent of the prokaryotic lipid biosynthesis pathway in the chloroplast, and, in addition to what previously has been reported, arabidopside E as well as an all-OPDA analog, arabidopside G, described here accumulated during the hypersensitive response and in response to wounding. We also show that different signaling pathways lead to the formation of arabidopsides during the hypersensitive response and the wounding response, respectively. However, the formation of arabidopsides during both responses is dependent on an intact jasmonate signaling pathway. Additionally, we report inhibition of growth of the fungal necrotrophic pathogen Botrytis cinerea and in planta release of free jasmonates in a time frame that overlaps with the observed reduction of arabidopside levels. Thus, arabidopsides may have a dual function: as antipathogenic substances and as storage compounds that allow the slow release of free jasmonates.

12-Oxo-Phytodienoic Acid Accumulation during Seed Development Represses Seed Germination inArabidopsis

“…The upregulation of some of these early JA biosynthesis genes in developing pxa1-1 seeds suggests that there might be an increased flux of precursors including OPDA through the JA biosynthesis pathway. A large amount of OPDA and dnOPDA is found esterified in chloroplast galactolipids in Arabidopsis (Stelmach et al, 2001;Hisamatsu et al, 2003Hisamatsu et al, , 2005Andersson et al, 2006;Buseman et al, 2006;Nakajyo et al, 2006;Bö ttcher and Weiler, 2007;Kourtchenko et al, 2007). Stelmach et al (2001) showed that OPDA esterified at the sn1 position in galactolipids could be released by sn1-specific lipases.…”

“…Dinor-oxo-phytodienoic acid (dnOPDA) is a 16-carbon homolog of OPDA that is synthesized from 16:3 fatty acid via a parallel hexadecanoid pathway (Weber et al, 1997;Acosta and Farmer, 2010). OPDA and dnOPDA containing galactolipids have been found in Arabidopsis, indicating that these compounds also exist in an esterified form (Stelmach et al, 2001;Hisamatsu et al, 2003Hisamatsu et al, , 2005Andersson et al, 2006;Buseman et al, 2006;Nakajyo et al, 2006;Bö ttcher and Weiler, 2007;Kourtchenko et al, 2007;Glauser et al, 2008). OPDA is transported from the plastid to the peroxisome, where CTS has been shown to be involved in its transport into the peroxisome (Theodoulou et al, 2005).…”

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

“…The free hexadecatrienoic acid (16:3) liberated by a phospholipase A2 from the sn-2 position of MGDG or DGDG can also become substrate for JA biosynthesis to form dn-OPDA (Figure 3). Alternatively, 13-LOX may oxygenate 18:3 and 16:3 esterified in galactolipids (Buseman et al, 2006;Kourtchenko et al, 2007). The resulting hydroperoxy galactolipids may then be substrates for AOS and AOC, yielding arabidopsides, which belong to galactolipid species containing esterified OPDA and dnOPDA in plastidic membranes.…”

Another JA/COI1-independent role of OPDA detected in tomato embryo development

“…16,17,45 After disruption of cellular integrity arabidopsides are formed from esterified fatty acids indicating that LOX, AOS and AOC act on membrane-bound substrates. 46 Arabidopsides were discussed to function as a storage pool of OPDA, as active agents against bacterial and fungal pathogens 47 as well as senescence-promoting compounds. 48 There is not mechanistic explanation for OPDA perception, which means existence of a putative OPDA receptor.…”