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Elevated levels of N-lauroylethanolamine, an endogenous constituent of desiccated seeds, disrupt normal root development in Arabidopsis thaliana seedlings

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Abstract

N-Acylethanolamines (NAEs) are prevalent in desiccated seeds of various plant species, and their levels decline substantially during seed imbibition and germination. Here, seeds of Arabidopsis thaliana (L.) Heynh. were germinated in, and seedlings maintained on, micromolar concentrations of N-lauroylethanolamine (NAE 12:0). NAE 12:0 inhibited root elongation, increased radial swelling of root tips, and reduced root hair numbers in a highly selective and concentration-dependent manner. These effects were reversible when seedlings were transferred to NAE-free medium. Older seedlings (14 days old) acclimated to exogenous NAE by increased formation of lateral roots, and generally, these lateral roots did not exhibit the severe symptoms observed in primary roots. Cells of NAE-treated primary roots were swollen and irregular in shape, and in many cases showed evidence, at the light- and electron-microscope levels, of improper cell wall formation. Microtubule arrangement was disrupted in severely distorted cells close to the root tip, and endoplasmic reticulum (ER)-localized green fluorescent protein (mGFP5-ER) was more abundant, aggregated and distributed differently in NAE-treated root cells, suggesting disruption of proper cell division, endomembrane organization and vesicle trafficking. These results suggest that NAE 12:0 likely influences normal cell expansion in roots by interfering with intracellular membrane trafficking to and/or from the cell surface. The rapid metabolism of NAEs during seed imbibition/germination may be a mechanism to remove this endogenous class of lipid mediators to allow for synchronized membrane reorganization associated with cell expansion.

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Fig. 1a–d.
Fig. 2a–c.
Fig. 3a–c.
Fig. a–d.
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Fig. 6a–f.
Fig. 7a–c.
Fig. 8a, b.

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Abbreviations

ER:

Endoplasmic reticulum

DMSO:

dimethyl sulfoxide

GFP:

green fluorescent protein

LA:

lauric acid

NAE:

N-acylethanolamine

NAPE:

N-acylphosphatidylethanolamine

PLD:

phospholipase D

numerical designation for acyl groups, number of carbons in acyl chain::

number of double bonds in acyl chain

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Acknowledgments

Financial support for this work was provided in part by USDA-NRICGP agreement number 99-35304-8002 to K.D.C., NASA grant number NAG 2-1518 to E.B.B. and the Samuel Roberts Noble Foundation. We thank the Arabidopsis stock center (Ohio State University) for the root expressing mGFP5-ER seeds and Dr. Richard A. Dixon, Samuel R. Noble Foundation, for critical reading of the manuscript. We also thank Mr. David Garret, University of North Texas, for assistance with transmission electron microscopy.

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Authors and Affiliations

  1. Division of Biochemistry and Molecular Biology, Department of Biological Sciences, University of North Texas, Denton, TX 76203, USA

    Kent D. Chapman

  2. Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, OK 73401, USA

    Elison B. Blancaflor & Guichuan Hou

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  1. Elison B. Blancaflor
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  2. Guichuan Hou
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  3. Kent D. Chapman
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Correspondence to Kent D. Chapman.

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Blancaflor, E.B., Hou, G. & Chapman, K.D. Elevated levels of N-lauroylethanolamine, an endogenous constituent of desiccated seeds, disrupt normal root development in Arabidopsis thaliana seedlings. Planta 217, 206–217 (2003). https://doi.org/10.1007/s00425-003-0985-8

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