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Development in Arabidopsis Thaliana Seedlings

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Development in Arabidopsis Thaliana Seedlings Planta (2003) 217: 206–217 DOI 10.1007/s00425-003-0985-8 ORIGINAL ARTICLE Elison B. Blancaflor Æ Guichuan Hou Æ Kent D. Chapman Elevated levels of N -lauroylethanolamine, an endogenous constituent of desiccated seeds, disrupt normal root development in Arabidopsis thaliana seedlings Received: 21 October 2002 / Accepted: 27 December 2002 / Published online: 12 February 2003 Ó Springer-Verlag 2003 Abstract N-Acylethanolamines (NAEs) are prevalent in ficking to and/or from the cell surface. The rapid me- desiccated seeds of various plant species, and their levels tabolism of NAEs during seed imbibition/germination decline substantially during seed imbibition and germi- may be a mechanism to remove this endogenous class of nation. Here, seeds of Arabidopsis thaliana (L.) Heynh. lipid mediators to allow for synchronized membrane re- were germinated in, and seedlings maintained on, organization associated with cell expansion. micromolar concentrations of N-lauroylethanolamine Electronic Supplementary Material Supplementary (NAE 12:0). NAE 12:0 inhibited root elongation, material is available for this article if you access the increased radial swelling of root tips, and reduced root article at http://dx.doi.org/10.1007/s00425-003-0985-8. hair numbers in a highly selective and concentration- A link in the frame on the left on that page takes you dependent manner. These effects were reversible when directly to the supplementary material. seedlings were transferred to NAE-free medium. Older seedlings (14 days old) acclimated to exogenous NAE by Keywords Arabidopsis Æ Cytoskeleton (microtubules) Æ increased formation of lateral roots, and generally, these Development (roots) Æ N-Acylethanolamine Æ lateral roots did not exhibit the severe symptoms Membrane dynamics Æ Vesicle trafficking observed in primary roots. Cells of NAE-treated primary roots were swollen and irregular in shape, and in many Abbreviations ER: Endoplasmic reticulum Æ DMSO: cases showed evidence, at the light- and electron-micro- dimethyl sulfoxide Æ GFP: green fluorescent protein scope levels, of improper cell wall formation. LA: lauric acid Æ NAE: N-acylethanolamine Æ NAPE: Microtubule arrangement was disrupted in severely N-acylphosphatidylethanolamine Æ PLD: phospholipase distorted cells close to the root tip, and endoplasmic D Æ numerical designation for acyl groups, number of reticulum (ER)-localized green fluorescent protein carbons in acyl chain: number of double bonds in acyl (mGFP5-ER) was more abundant, aggregated and dis- chain tributed differently in NAE-treated root cells, suggesting disruption of proper cell division, endomembrane orga- nization and vesicle trafficking. These results suggest that Introduction NAE 12:0 likely influences normal cell expansion in roots by interfering with intracellular membrane traf- N-Acylethanolamines (NAEs) are lipid mediators derived from the hydrolysis of the membrane phosphol- Electronic Supplementary Material Supplementary material is ipid, N-acylphosphatidylethanolamine (NAPE; Schmid available for this article if you access the article at http:// et al. 1996). In animal systems, this reaction constitutes dx.doi.org/10.1007/s00425-003-0985-8. A link in the frame on the part of the endocannabinoid signaling pathway which left on that page takes you directly to the supplementary material. regulates a variety of physiological processes, including K.D. Chapman (&) cell proliferation (De Petrocellis et al. 2000), immune cell Division of Biochemistry and Molecular Biology, signaling (Berdyshev 2000), neurotransmission (Wilson Department of Biological Sciences, and Nicoll 2002), and embryo development (Paria and University of North Texas, Denton, TX 76203, USA Dey 2000). In addition, this pathway appears to be E-mail: [email protected] Fax: +1-940-5654136 involved in cytoprotection in some tissues (Hansen et al. 2000). E.B. Blancaflor Æ G. Hou Plant Biology Division, NAEs have been identified and quantified in a variety The Samuel Roberts Noble Foundation, of plant tissues (Chapman et al.1998, 1999), and reports Ardmore, OK 73401, USA of biological activities of these lipids in plants are 207 beginning to appear (Chapman 2000). For example, of cells and tissue types in the elongated root is deter- increases in NAE 14:0 in elicited tobacco cell suspen- mined by the positional cues that are established during sions (Chapman et al. 1998) and elicited leaves of embryogenesis (Benfey and Scheres 2000). In the matu- tobacco plants (Tripathy et al. 1999) were sufficient to ration zone, the rapid directional expansion of cells activate phenylalanine-ammonia lyase (PAL) gene eventually ceases with specific cells in the epidermis dif- expression (Tripathy et al. 1999). More recently, NAEs ferentiating to form root hairs, which, in contrast to the were shown to selectively inhibit the activity of phosp- diffuse growth characteristic of cells in the elongation holipase D (PLD) a in vitro in a chain-length-dependent zone, expand primarily by tip growth. Underlying these manner, and application of NAEs to epidermal sections two different mechanisms of cell expansion are various of tobacco and Commelina communis abrogated abscisic dynamic processes that include ion fluxes (Hepler et al. acid (ABA)-induced stomatal closure (Austin-Brown 2001), cytoskeletal reorganization (Bibikova et al. 1999; and Chapman 2002), a process previously shown to Barlow and Baluska 2000), trafficking of membrane involve PLDa activity (Sang et al. 2001). vesicles (Hawes et al. 1999) and modifications in cell wall Desiccated seeds of a variety of plant species con- properties (Cosgrove 2000). tained NAEs with chain lengths of 12C to 18C (sum- The rapid depletion of NAEs in imbibing/germinat- marized in Chapman 2000). Total NAE content ranged ing seeds (Chapman et al. 1999; Shrestha et al. 2002) from about 400 ng g)1 FW in pea to 1,600 ng g)1 FW in points to a physiological role for this metabolic pathway cottonseed (Chapman et al. 1999). Moreover, in cotton, in seed germination and seedling growth. To test this pea and peanut seeds, total NAE content declined hypothesis, we germinated Arabidopsis thaliana seeds sharply after 4–8 h imbibition. Recently, two competing and maintained seedlings on sustained levels of NAE pathways were identified (and shown to be activated by above the physiological concentrations measured in imbibition) for the metabolism of these seed NAEs desiccated seeds. In this paper, we show that NAE 12:0, in vivo – a lipoxygenase (13-LOX)-mediated pathway but not NAE 16:0 or free fatty acid analogues of NAEs, for the peroxidation of polyunsaturated NAE species, induced a multitude of morphological and cellular and an amidohydrolase-mediated pathway for the defects in primary roots of Arabidopsis. Collectively, our hydrolysis of both saturated and unsaturated NAEs results point to a role for NAEs in root cell expansion/ (Shrestha et al. 2002). During the same period of seed elongation, possibly as a lipid mediator regulating imbibition and seed germination, the biosynthesis of membrane trafficking to and from the cell surface. NAPE increased substantially (Sandoval et al. 1995; Chapman and Sprinkle 1996) and the enzymatic machinery for NAPE biosynthesis was localized to Materials and methods membranes derived from the ER, Golgi, and plasma membranes (Chapman and Sriparameswaran 1997). It Plant material and treatment may be that the rapid metabolism of NAEs during seed imbibition and germination is an important requisite for Seeds of Arabidopsis thaliana L. Heynh. (ecotype: Columbia) were normal seedling growth. surface-sterilized in 95% ethanol and 20% bleach followed by extensive washing with sterile, deionized water prior to spreading Seed germination involves the breaking of dormancy onto sterile filter paper. Individual seeds were planted on 0.8% and the resumption of growth processes in the embryo, phyta-agar (Gibco) layered onto 62 mm·48 mm sterile coverslips. which is triggered partly by imbibition. Early seedling The composition of the medium was essentially as described in growth is sustained by metabolizable substrates stored in Legue et al. (1997). For the different treatments, a stock solution of 10 mM NAE 12:0 in 67% dimethyl sulfoxide (DMSO) was added the seed but subsequent establishment of the plant as a to the medium prior to autoclaving and layering onto coverslips to self-sustaining organism requires a coordinated pattern make final NAE 12:0 concentrations of 10, 20, 30, 40, 50 or of cell division and expansion that is regulated by a 100 lM. Arabidopsis media with an equivalent amount of DMSO, variety of external stimuli and endogenous factors (Esau NAE 16:0, lauric acid (LA) and palmitic acid were prepared for solvent and specificity controls. After planting, cover glasses were 1977). Although there have been several endogenous placed in 90-mm sterile plastic Petri dishes and placed in a growth compounds (e.g. plant hormones), and a variety of genes chamber with a 16 h light (134 lmol photons m)2 s)1), 8 h dark identified (Benfey and Scheres 2000) that regulate plant cycle at 22 °C. The Petri dishes were positioned at a 60° angle from cell division and expansion, the complexity of these the horizontal so that the roots could grow along the bottom of the processes makes it likely that other yet unidentified coverslip for subsequent microscopic observation and image cap- ture. endogenous constituents regulate these important N-Acylethanolamine types were synthesized from ethanolamine cellular processes. and the corresponding acylchloride and purified as
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