Rapid and long-distance secretion of membrane components is critical for hyphal formation in filamentous fungi, but the mechanisms responsible for polarized trafficking are not well understood. Here, we demonstrate that in Candida albicans, the majority of the Golgi complex is redistributed to the distal region during hyphal formation. Randomly distributed Golgi puncta in yeast cells cluster toward the growing tip during hyphal formation, remain associated with the distal portion of the filament during its extension, and are almost absent from the cell body. This restricted Golgi localization pattern is distinct from other organelles, including the endoplasmic reticulum, vacuole and mitochondria, which remain distributed throughout the cell body and hypha. Hyphal-induced positioning of the Golgi and the maintenance of its structural integrity requires actin cytoskeleton, but not microtubules. Absence of the formin Bni1 causes a hyphal-specific dispersal of the Golgi into a haze of finely dispersed vesicles with a sedimentation density no different from that of normal Golgi. These results demonstrate the existence of a hyphal-specific, Bni1-dependent cue for Golgi integrity and positioning at the distal portion of the hyphal tip, and suggest that filamentous fungi have evolved a novel strategy for polarized secretion, involving a redistribution of the Golgi to the growing tip.
INTRODUCTIONThe establishment of axes of polarization is crucial for the growth and division of both unicellular and multicellular organisms. A striking example of polarized morphogenesis is the process of hyphal formation in Candida albicans. In response to a number of inductive signals, C. albicans switches from an ovoid yeast form to a highly elongated hyphal form, and its capacity to switch between these forms is postulated to be related to its virulence as a fungal pathogen (Lo et al., 1997;Gow et al., 2002). Within minutes of encountering the inducing signal, growth is restricted to the germ tube, which rapidly extends into a filament that becomes Ͼ10 times the length of the cell body within hours.The mechanism that establishes and maintains rapid apical growth during hyphal formation in C. albicans is not well understood. However, based on our knowledge of how polarized growth occurs in other systems, it is generally accepted to involve the asymmetric deposition of membrane and cell wall at the growing tip. Studies from Saccharomyces cerevisiae have established that in response to certain spatial or positional cues, Golgi-derived secretory vesicles that fuse with the plasma membrane at random sites during isotropic growth of the mother cell are retargeted to fuse at a specified site, resulting in bud emergence and apical growth (for review, see Lew and Reed, 1995;Finger and Novick, 1998). The process of budding requires many proteins that regulate site selection, reorganization of the actin cytoskeleton, and polarization of the secretory apparatus (for review, see Pruyne et al., 2004b). Hyphal growth in C. albicans presents an additi...