Yeast cells can select bud sites in either of two distinct spatial patterns. a cells and alpha cells typically bud in an axial pattern, in which both mother and daughter cells form new buds adjacent to the preceding division site. In contrast, a/alpha cells typically bud in a bipolar pattern, in which new buds can form at either pole of the cell. The BUD3 gene is specifically required for the axial pattern of budding: mutations of BUD3 (including a deletion) affect the axial pattern but not the bipolar pattern. The sequence of BUD3 predicts a product (Bud3p) of 1635 amino acids with no strong or instructive similarities to previously known proteins. However, immunofluorescence localization of Bud3p has revealed that it assembles in an apparent double ring encircling the mother-bud neck shortly after the mitotic spindle forms. The Bud3p structure at the neck persists until cytokinesis, when it splits to yield a single ring of Bud3p marking the division site on each of the two progeny cells. These single rings remain for much of the ensuing unbudded phase and then disassemble. The Bud3p rings are indistinguishable from those of the neck filament-associated proteins (Cdc3p, Cdc10p, Cdc11p, and Cdc12p), except that the latter proteins assemble before bud emergence and remain in place for the duration of the cell cycle. Upon shift of a temperature-sensitive cdc12 mutant to restrictive temperature, localization of both Bud3p and the neck filament-associated proteins is rapidly lost. In addition, a haploid cdc11 mutant loses its axial-budding pattern upon shift to restrictive temperature. Taken together, the data suggest that Bud3p and the neck filaments are linked in a cycle in which each controls the position of the other's assembly: Bud3p assembles onto the neck filaments in one cell cycle to mark the site for axial budding (including assembly of the new ring of neck filaments) in the next cell cycle. As the expression and localization of Bud3p are similar in a, alpha, and a/alpha cells, additional regulation must exist such that Bud3p restricts the position of bud formation in a and alpha cells but not in a/alpha cells.
Genomic studies in yeast have revealed that one eighth of genes are cell cycle regulated in their expression. Almost without exception, the significance of cell cycle periodic gene expression has not been tested. Given that many such genes are critical to cellular morphogenesis, we wanted to examine the importance of periodic gene expression to this process. The expression profiles of two genes required for the axial pattern of cell division, BUD3 and BUD10/AXL2/SRO4, are strongly cell cycle regulated. BUD3 is expressed close to the onset of mitosis. BUD10 is expressed in late G1. Through promotor-swap experiments, the expression profile of each gene was altered and the consequences examined. We found that an S/G2 pulse of BUD3 expression controls the timing of Bud3p localization, but that this timing is not critical to Bud3p function. In contrast, a G1 pulse of BUD10 expression plays a direct role in Bud10p localization and function. Bud10p, a membrane protein, relies on the polarized secretory machinery specific to G1 to be delivered to its proper location. Such a secretion-based targeting mechanism for membrane proteins provides cells with flexibility in remodeling their architecture or evolving new forms.
The elaboration of cell form has fascinated biologists for generations. A vast body of literature details the life cycles, anatomy, and developmental programs of many species. The mechanisms responsible for the observed diversity of structure involve polarization, directed growth, and spatial memory. These issues of morphogenesis are currently under study in the budding yeast Saccharomyces cerevisiae and other fungi. In yeast, a number of genes are known that specifically affect either the orientation or the assembly of a polarity axis. These include the bud-site selection genes, BUDl -BUDS, as well as the polarity establishment genes, CDC24, CDC42, CDC43, and BEMl. Members of each of these classes encode elements in signal transduction type pathways. This review examines our present understanding of the molecular machinery responsible for orienting and assembling cell polarity as best understood in S. cerevisiae, and speculates about how similar machinery might function in other fungi.R6umC : Le dtveloppement des cellules fascine les biologistes depuis des generations. Une importante litteratwe dCcrit les cycles biologiques en details. Les mtcanismes responsables de la diversitt observCe impliquent la polarisation, la croissance orientCe et la mtmoire spatiale. Ces questions sur la morphogCnbse font courramment l'objet d'Ctudes chez une levure i bourgeonnement, le Saccharomyces cerevisiae, et autres champignons. Chez la levure, on connait des gbnes qui affectent sptcifiquement soit l'orientation ou soit la mise en place d'un axe de polaritt. Ceux-~i incluent la selection du site de bourgeonnement, BUDl -BUDS, ainsi que les gbnes de mise en place de la polaritt, CDC24, CDC42, CDC43 et BEMI. Les membres de chacune de ces classes codent pour des tltments des sentiers de signalisation de type transduction. Cette revue examine la comprChension actuelle de la machinerie moltculaire responsable pour l'orientation et la mise en place de la polaritt cellulaire, au meilleur de nos connaissance sur le S. cerevisiae, et sptcule sur le fonctionnement d'une telle mtcanique chez d'autres champignons.
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