The Curious Status of the Golgi Apparatus

An organelle is a membrane-bounded intracellular strucNew Evidence for an Old Model ture with a unique molecular composition and function. The Golgi is typically represented as a series of stable Where do organelles come from? Most biologists would compartments, with transport vesicles serving to carry state that each organelle forms by the growth and divithe secretory cargo forward from one compartment to sion of a preexisting organelle of the same type. This the next. By contrast, early morphologists proposed that view has dominated cell biology for decades (Palade, Golgi compartments are transitory structures (Beams 1983; Warren and Wickner, 1996). However, recent eviand Kessel, 1968). New cisternae appeared to be formdence suggests that only a subset of the organelles fit ing at the cis-face of the Golgi stack by the coalescence this picture, and that a different perspective is needed. of ER-derived membranes, while cisternae of the transThe nucleus matches this standard description of an Golgi network (TGN) appeared to be fragmenting into organelle. Certain protein and nucleic acid species are secretory vesicles. The implication was that cisternae found exclusively in the nucleus, and the entire contents move progressively across the stack from the cisto of the nucleus double and divide with each cell cycle. the trans-face. Some of the strongest evidence for this A similar pattern is seen with mitochondria and chloro“cisternal progression” model came from analyzing cellplasts (Birky, 1983). This simple paradigm is often exsurface scales in algae (Becker and Melkonian, 1996). tended to include all of the organelles in the cell. Many These scales are large electron-dense glycoconjugates organelles consist of multiple compartments, and each that are synthesized within Golgi stacks. Scales are not compartment is also viewed as a permanent structure seen in the vesicles that bud from the rims of Golgi with a unique composition. cisternae, and in some species the scales can be more However, the standard view of organelle biogenesis than 20 times the size of a typical transport vesicle. is being challenged by studies of the endomembrane These observations suggested that scales are carried system, which comprises the organelles of the exocytic through the Golgi stack by the cisternae themselves. and endocytic pathways. These organelles exchange Why were the images of algal scales not taken as material by means of transport vesicles (Rothman and conclusive evidence for cisternal progression? One alWieland, 1996). Such vesicles selectively incorporate a ternative view is that algae have evolved a unique mechsubset of the proteins and lipids present in a donor anism for intra-Golgi transport (Farquhar and Palade, compartment, and then deliver their contents by fusing 1981). This explanation seems unlikely, because various with an acceptor compartment. As a result, proteins of animal cells and higher plant cells also transport large the endomembrane system are rarely localized to a sinelectron-dense structures through the Golgi stack, and gle compartment (Mellman and Simons, 1992). While these structures also appear to be excluded from Golgithis point is widely appreciated, vesicular transport also associated vesicles (Clermont et al., 1993; Schnepf, has deeper implications (Helenius et al., 1983). For ex1993). In some cells the secretory cargoes form aggreample, what would happen if vesicles were to fuse not gates that induce large distensions of the Golgi cisternae with a preexisting acceptor compartment, but with one (Mollenhauer and Morré, 1991). Unfortunately, most of another? As shown in Figure 1A, the result would be a these model systems share the problem that the secremembrane-bounded structure with a unique compository cargoes are poorly characterized (Schekman and tion (i.e., a new compartment). The properties of this Mellman, 1997). For instance, it is conceivable that an compartment could then be modified by subsequent immature algal scale can disassemble into subunits, vesicular transport events. By producing and/or receivwhich are carried in transport vesicles to the next cising vesicles, the compartment could undergo compositerna and then reassembled. Another problem is that tional changes in a process termed “maturation” (Figure Golgi organization is ambiguous in many cell types. 1B). By fragmenting into transport vesicles, the compartThus, one could argue that in an algal Golgi apparatus, ment could simply disappear (Figure 1C). all of the scale-containing cisternae actually represent This picture profoundly affects the way we think about an extended TGN compartment, and that no progressive the endomembrane system. Some compartments may transport occurs through this portion of the stack (Mellbe definable only as intermediates in a continuous proman and Simons, 1992). cess of transformation (Helenius et al., 1983). Instead A new paper by Bonfanti et al. (1998 [this issue of of regarding compartments as separate entities, we are Cell]) provides the best evidence to date for cisternal