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Vol. 15, Issue 1, 207-218, January 2004

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Roles of Phosphoinositides and of Spo14p (phospholipase D)-generated Phosphatidic Acid during Yeast Sporulation

Simon A. Rudge ^* , Vicki A. Sciorra ^* , Michelle Iwamoto , Chun Zhou , Thomas Strahl , Andrew J. Morris  , Jeremy Thorner , and JoAnne Engebrecht  ^¶ ||

^* Department of Cellular and Molecular Medicine, School of Medicine, and Howard Hughes Medical Institute, University of California, San Diego, La Jolla, California 92093-0668; Department of Pharmacological Sciences, State University of New York at Stony Brook, Stony Brook, New York 11794-8651; Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, California 94720-3202; Department of Cell and Developmental Biology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599; and ^¶ Section of Molecular and Cellular Biology, University of California, Davis, Davis, California 95616

Submitted April 19, 2003; Revised September 10, 2003; Accepted September 12, 2003
Monitoring Editor: John Pringle

During yeast sporulation, internal membrane synthesis ensures that each haploid nucleus is packaged into a spore. Prospore membrane formation requires Spo14p, a phosphatidylinositol 4,5-bisphosphate [PtdIns(4,5)P₂]-stimulated phospholipase D (PLD), which hydrolyzes phosphatidylcholine (PtdCho) to phosphatidic acid (PtdOH) and choline. We found that both meiosis and spore formation also require the phosphatidylinositol (PtdIns)/PtdCho transport protein Sec14p. Specific ablation of the PtdIns transport activity of Sec14p was sufficient to impair spore formation but not meiosis. Overexpression of Pik1p, a PtdIns 4-kinase, suppressed the sec14-1 meiosis and spore formation defects; conversely, pik1-ts diploids failed to undergo meiosis and spore formation. The PtdIns(4)P 5-kinase, Mss4p, also is essential for spore formation. Use of phosphoinositide-specific GFP-PH domain reporters confirmed that PtdIns(4,5)P₂ is enriched in prospore membranes. sec14, pik1, and mss4 mutants displayed decreased Spo14p PLD activity, whereas absence of Spo14p did not affect phosphoinositide levels in vivo, suggesting that formation of PtdIns(4,5)P₂ is important for Spo14p activity. Spo14p-generated PtdOH appears to have an essential role in sporulation, because treatment of cells with 1-butanol, which supports Spo14p-catalyzed PtdCho breakdown but leads to production of Cho and Ptd-butanol, blocks spore formation at concentrations where the inert isomer, 2-butanol, has little effect. Thus, rather than a role for PtdOH in stimulating PtdIns(4,5)P₂ formation, our findings indicate that during sporulation, Spo14p-mediated PtdOH production functions downstream of Sec14p-, Pik1p-, and Mss4p-dependent PtdIns(4,5)P₂ synthesis.

^|| Corresponding author. E-mail address: jengebrecht{at}ucdavis.edu.

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