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Plant and Cell Physiology Advance Access originally published online on October 28, 2007
Plant and Cell Physiology 2007 48(12):1764-1774; doi:10.1093/pcp/pcm149
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© The Author 2007. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oxfordjournals.org

Phospholipase D Signaling Regulates Microtubule Organization in the Fucoid Alga Silvetia compressa

Nick T. Peters*, Kyle O. Logan, Anne Catherine Miller and Darryl L. Kropf

University of Utah, Department of Biology, 257 South 1400 East, Salt Lake City, UT 84112, USA

*Corresponding author: E-mail, npeters{at}biology.utah.edu; Fax, +1-801-581-4668.


  Abstract

Recent studies in higher plants or animals have shown that phospholipase D (PLD) signaling regulates many aspects of development, including organization of microtubules (MTs), actin and the endomembrane system. PLD hydrolyzes structural phospholipids to form the second messenger phosphatidic acid (PA). To begin to understand the signaling pathways and molecules that regulate cytoskeletal and endomembrane arrays during early development in the brown alga, Silvetia compressa, we altered PLD activity by applying butyl alcohols to zygotes. 1-Butanol activates PLD and is a preferred substrate, primarily forming phosphatidyl butanol (P-butanol), which is not a signaling molecule. Treatment with 1-butanol inhibited cell division and cytokinesis but not photopolarization or germination, suggesting an MT-based effect. Immunolabeling revealed that 1-butanol treatment rapidly disrupted MT arrays and caused zygotes to arrest in metaphase. MT arrays recovered rapidly following butanol washout, but subsequent development depended on the timing of the treatment regime. Additionally, treatment with 1-butanol early in development disrupted endomembrane organization, known to require functional MTs. Interestingly, treatment with higher concentrations of 2-butanol, which also activates PLD, mimicked the effects of 1-butanol. In contrast, the control t-butanol had no effect on MTs or development. These results indicate that S. compressa zygotes utilize PLD signaling to regulate MT arrays. In contrast, PLD signaling does not appear to regulate actin arrays or endomembrane trafficking directly. This is the first report describing the signaling pathways that regulate cytoskeletal organization in the stramenopile (heterokont) lineage.

Keywords: Brown algae - Cytoskeleton - Development - Endomembrane - Phosphatidic acid - Phospholipase D

Abbreviations: AF, after fertilization; ASW, artificial sea water; CLSM, confocal laser scanning microscope; DMSO, dimethylsulfoxide; L1, unidirectional light; L2, light oriented 180° from L1; MAP, microtubule-associated protein; MT, microtubule; MTOC, microtubule-organizing center; PA, phosphatidic acid; P-butanol, phosphatidyl butanol; PLD, phospholipase D.

(Received August 22, 2007; Accepted October 23, 2007)
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