Yeast-to-Hyphal Transition Triggers Formin-dependent Golgi Localization to the Growing Tip inCandida albicans

Abstract

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...

Recognition of Yeast by Murine Macrophages Requires Mannan but Not Glucan

“…Yeast cells were seeded on glass coverslips in 24-well plates to analyze hyphal induction of individual cells, as described previously (40). Briefly, overnight yeast cultures were diluted to 0.5 OD 600 units/ml, and 5 l was spread on each coverslip.…”

The Actomyosin Ring Recruits Early Secretory Compartments to the Division Site in Fission Yeast

“…The intimate association between Spitzenkör-per behavior and hyphal morphogenesis suggests that the Spitzenkö rper might function as a "Vesicle Supply Center," producing the secretory vesicles (Bartnicki-Garcia et al, 1989). In fact, it was recently shown that most of the Golgi apparatus is indeed localized near the growing hyphal tips (Rida et al, 2006).…”

“…The intimate association between Spitzenkör-per behavior and hyphal morphogenesis suggests that the Spitzenkö rper might function as a "Vesicle Supply Center," producing the secretory vesicles (Bartnicki-Garcia et al, 1989). In fact, it was recently shown that most of the Golgi apparatus is indeed localized near the growing hyphal tips (Rida et al, 2006).Considering the functional continuum of the secretory pathway (for review see Guo and Novick, 2004), we were interested in investigating the structural and spatial organization of the tER (transitional ER) and cis-and trans-Golgi during polarized tip growth and cell division, which represent major aspects of cellular polarity in fission yeast.In this study we observed an enrichment of tER that was accompanied by the biogenesis of Golgi cisternae at the division site. These processes required assembly of a functional actomyosin ring and, in particular, the function of the EFC domain protein, Cdc15p.…”

Rapid tip-directed movement of Golgi equivalents in growing Aspergillus nidulans hyphae suggests a mechanism for delivery of growth-related materials

“…Evidence from A. nidulans (Breakspear et al, 2007), Aspergillus oryzae (Akao et al, 2006), Candida albicans (Rida et al, 2006) and Saccharomyces cerevisiae (Matsuura-Tokita et al, 2006) suggests that GE distribution in fungi is related to tip growth.…”