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Emerging Physiological Roles for N-Acylphosphatidylethanolamine Metabolism in Plants: Signal Transduction and Membrane Protection

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Emerging Physiological Roles for N-Acylphosphatidylethanolamine Metabolism in Plants: Signal Transduction and Membrane Protection Chemistry and Physics of Lipids 108 (2000) 221–230 www.elsevier.com/locate/chemphyslip Review Emerging physiological roles for N-acylphosphatidylethanolamine metabolism in plants: signal transduction and membrane protection Kent D. Chapman * Department of Biological Sciences, Di6ision of Biochemistry and Molecular Biology, Uni6ersity of North Texas, Denton, TX 76203-5220 USA Received 27 March 2000; received in revised form 24 May 2000; accepted 24 May 2000 Abstract The activation of N-acylphosphatidylethanolamine (NAPE) metabolism in plants appears to be associated mostly with cellular stresses. In response to pathogen elicitors, NAPE is hydrolzyed by phospholipase-D (PLD), and corresponding medium-chain, saturated N-acylethanolamines (NAEs) are released by plant cells where they act as lipid mediators to modulate ion flux and activate defense gene expression. In desiccated seeds of higher plants, long-chain, saturated and unsaturated NAEs are prevalent, but are rapidly metabolized during the first few hours of imbibition, a period of substantial osmotic stress. NAPE synthesis is increased in seeds during this same period of rapid rehydration. A membrane-bound enzyme designated NAPE synthase has been purified from imbibed cotton- seeds and its unusual biochemical properties suggest that it may scavenge free fatty acids in vivo. This feature of NAPE metabolism may be unique to higher plants a may be a mechanism for the rapid recycling of fatty acids back into membrane-associated NAPE. Altogether, increasing evidence indicates that NAPE metabolism in plants shares functional similarities with NAPE metabolism in animal systems, including signal transduction and cellular protec- tion. In particular, the emerging role of released NAEs as lipid mediators in plant defense signaling represents an intriguing parallel to ‘endocannabinoid signaling’ in several mammalian cell types. © 2000 Elsevier Science Ireland Ltd. All rights reserved. Keywords: N-acylethanolamine; N-acylphosphatidylethanolamine; Fatty acid metabolism; Plant-defense signaling; Membrane protection Abbre6iations: PC, phosphatidylcholine; PE, phosphatidylethanolamine; NAE, N-acylethanolamine; NAPE, N-acylphos- phatidylethanolamine; PLD, phospholipase D. * Tel.: +1-940-5652969; fax: +1-940-5654136. E-mail address: [email protected] (K.D. Chapman). 0009-3084/00/$ - see front matter © 2000 Elsevier Science Ireland Ltd. All rights reserved. PII: S0009-3084(00)00198-5 222 K.D. Chapman / Chemistry and Physics of Lipids 108 (2000) 221–229 1. Introduction and perspective min exposure to the fungal elicitor protein-xylanase (Chapman et al., 1998). Xylanase has been shown N-Acylphosphatidylethanolamine (NAPE) was to elicit a variety of cellular responses similar to first reported in the mid 1960s as a minor con- defense responses of intact plants to pathogens stituent in wheat flour (Bomstein, 1965) and its (Anderson et al., 1990; Bailey et al., 1993; Hanania occurrence soon became associated with seeds of and Avni, 1997; Furman-Matarasso et al., 1999), higher plants (Dawson et al., 1969). However in the and its activation of NAPE catabolism suggested early 1970s, an unfortunate misidentification of a possible role in signaling of plant pathogen NAPE (actually phosphatidylmethanol produced perception. The release of NAE into the cell culture as an artifact during lipid extractions; Roughan et medium was confirmed by GC–MS and discovered al., 1978) in a series of metabolic labeling studies to be mostly N-myristoyl- and N-lauroyl- with developing seeds (Wilson and Rinne, 1974), ethanolamine (Chapman et al., 1998). Almost no left many plant lipid biochemists doubting the NAE was recovered with cells. Although poor existence of this unusual phospholipid as an en- recovery from TLC plates and poor GC–MS dogenous component of plant tissues. Not until the properties of the O-acetylated NAEs, left these 1990s, after much work with NAPE metabolism results qualitative, it nonetheless marked the first had been done in mammalian tissues, was the report of a signal-mediated formation of NAE by existence and metabolism of NAPE in plants re-ex- plant cells, and indicated that released NAEs accu- amined. Experimental evidence from a combina- mulated extracellularly. These preliminary results tion of biochemical and biophysical approaches now have been supported by more quantitative indeed supported the existence of NAPE as a experiments with leaves of intact tobacco plants minor, endogenous constituent of plant seeds treated either with xylanase or cryptogein elicitors (Chapman and Moore, 1993a; Sandoval et al., (Tripathy et al., 1999). For example, NAE14:0 1995). In fact, radiolabeling experiments with [1,2- content in tobacco leaves increased from 694to 14C]-ethanolamine in vivo indicated that a variety 64929 ng g−1 fresh weight following infiltration of plant cells and tissues (not just seeds) had the of xylanase and incubation for 10 min. capacity to synthesize NAPE de novo via a PE A microsomal PLD-type activity was identified intermediate (Chapman and Moore, 1993a). In in tobacco cell suspensions that catalyzed the addition, recent evidence has indicated that NAPE formation of [14C]NAE from [14C]NAPE, and its serves as a precursor for the signal-activated forma- activity was stimulated about 20-fold by masto- tion of NAEs (Chapman et al., 1998) which appear paran, suggesting that G-proteins might be in- to function as lipid mediators in plant cell signaling volved in the activation of this pathway (Chapman (Tripathy et al., 1999). et al., 1998). Several PLD isoforms have been cloned from plants, and a survey of expressed Arabidopsis recombinant PLD activities in vitro 2. NAPE catabolism in elicited cell cultures and revealed some interesting differences among the plants individual isoforms in their capacity for NAPE hydrolysis (Pappan et al., 1998). The PLDa iso- N-Acylation of PE in plant cells was stimulated form, mostly associated with membrane degrada- for several h following treatment with pathogen tive processes, was inactive toward NAPE, while elicitors (Chapman et al., 1995), which raised the both the PLDb and g isoforms formed NAE from possibility that NAPE metabolism was involved in NAPE. In fact, the PLDg isoform actually ap- signaling pathogen perception. In radiolabeling peared to prefer NAPE over PC as a substrate experiments in vivo with tobacco cell suspensions, under equivalent reaction conditions. Thus it ap- [14C]NAE (labeled on the ethanolamine carbons) pears that PLDb and/or g is/are likely to be increased approximately six-fold in the culture involved in the formation of NAEs in plants. medium whereas [14C]NAPE associated with cells However, these in vitro studies should be inter- decreased by about five-fold following a brief 10 preted with some caution since the PLDa K.D. Chapman / Chemistry and Physics of Lipids 108 (2000) 221–229 223 isoform, previously thought to require millimolar several abiotic environmental stresses), and allows amounts of Ca2+ for optimum activity, was re- for the metabolic channeling of carbon into antimi- cently reported to be active in vitro at near-physi- crobial phenylpropanoids (Rasmussen and Dixon, ological Ca2+ concentrations in acidic pH (Pappan 1999). The activation of PAL expression was re- and Wang, 1999). cently shown to involve a NO-mediated pathway that when activated in conjunction with the pro- duction of reactive oxygen intermediates (ROI) 3. NAEs as lipid mediators in plant defense leads to hypersensitive cell death and confinement signaling of the pathogen (Alvarez et al., 1998; Delledonne et al., 1998; Durner et al., 1998). Exogenously A number of predictable short (min)- and long- applied NAE14:0 activated PAL expression inde- term (h–d) cellular responses are known to occur pendent of the addition of elicitors both in cell when resistant host plants encounter pathogens, suspensions and in leaves of tobacco plants (Tripa- and these events collectively help to establish sys- thy et al., 1999). Activation of PAL expression was temic immunity in the plant to subsequent patho- evident at submicromolar concentrations of gen invasion (Dixon and Lamb, 1990; Dixon et al., NAE14:0 but was not activated by even high 1994; Alvarez et al., 1998). Many of these defense micromolar concentrations of myristic acid (Tripa- responses (although not all) can be invoked in cell thy et al., 1999). Even more interesting, like the suspension cultures by the addition of pathogen alkalinization response, the effect of NAE14:0 was elicitors such as the fungal protein xylanase (Fur- reduced in the presence of equimolar concentra- man-Matarasso et al., 1999). tions of AM281 (Tripathy and Chapman; unpub- Among the earliest detectable changes of plant lished results). In summary, we hypothesize that cells in response to elicitor treatment is rapid ion PLD-mediated NAE release which is triggered in flux (influx of H+ and Ca2+ and efflux of K+)at vivo by perception of pathogen elicitors, functions the plasma membrane (Ebel and Scheel, 1992). in both the attentuation of the primary signal, and Addition of exogenous NAE14:0 to tobacco cells activation of defense gene expression likely through reduced the characteristic medium alkalinization the action of a CB-like receptor, which may involve triggered by a number of elicitors (Tripathy et al., the NO second messenger system (see Fig. 1). 1999). A number of synthetic NAE species were effective at inhibiting this alkalinization response at micromolar levels, but inhibition was time- and 4. NAE quantification and catabolism
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