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J. Biol. Chem., Vol. 280, Issue 45, 37846-37852, November 11, 2005

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Differential Requirement for Phospholipase D/Spo14 and Its Novel Interactor Sma1 for Regulation of Exocytotic Vesicle Fusion in Yeast Meiosis^*

From the Cell Biology and Biophysics Unit, European Molecular Biology Laboratory, D-69117 Heidelberg, Germany

During sporulation and meiosis of budding yeast a developmental program determines the formation of the new plasma membranes of the spores. This process of prospore membrane (PSM) formation leads to the formation of meiotic daughter cells, the spores, within the lumen of the mother cell. It is initiated at the spindle pole bodies during meiosis II. Spore formation, but not meiotic cell cycle progression, requires the function of phospholipase D (PLD/Spo14). Here we show that PLD/Spo14 forms a complex with Sma1, a meiotically expressed protein essential for spore formation. Detailed analysis revealed that both proteins are required for early steps of prospore membrane assembly but with distinct defects in the respective mutants. In the spo14 mutant the initiation of PSM formation is blocked and aggregated vesicles of homogenous size are detected at the spindle pole bodies. In contrast, initiation of PSM formation does occur in the sma1 mutant, but the enlargement of the membrane is impaired. During PSM growth both Spo14 and Sma1 localize to the membrane, and localization of Spo14 is independent of Sma1. Biochemical analysis revealed that Sma1 is not necessary for PLD activity per se and that PLD present in a complex with Sma1 is highly active. Together, our results suggest that yeast PLD is involved in two distinct but essential steps during the regulated vesicle fusion necessary for the assembly of the membranous encapsulations of the spores.

Received for publication, April 19, 2005 , and in revised form, August 8, 2005.

^* This work was financially supported in part by the European Molecular Biology Laboratory and by Deutsche Forschungsgemeinschaft Grant KN498/2-2. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ These authors contributed equally to this work.

² Present address: Institute of Molecular Pathology, Dr. Bohrgasse 7, A-1030 Vienna, Austria.

³ Present Address: Max-Planck-Institut für Biochemie, Am Klopferspitz 18A, D-82152 Martinsried, Germany.

⁴ To whom correspondence should be addressed. Tel.: 49-6221-387631; Fax: 49-6221-387512; E-mail: knop{at}embl.de.

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