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. 2004 Dec 28;101(52):18018-23.
doi: 10.1073/pnas.0408256102. Epub 2004 Dec 13.

Golgi inheritance in small buds of Saccharomyces cerevisiae is linked to endoplasmic reticulum inheritance

Catherine A Reinke  1 , Patrycja Kozik, Benjamin S Glick
Affiliations

Golgi inheritance in small buds of Saccharomyces cerevisiae is linked to endoplasmic reticulum inheritance

Catherine A Reinke et al. Proc Natl Acad Sci U S A. .

Abstract

According to the cisternal maturation hypothesis, endoplasmic reticulum (ER)-derived membranes nucleate new Golgi cisternae. The yeast Saccharomyces cerevisiae offers a unique opportunity to test this idea because small buds contain both ER and Golgi structures early in the cell cycle. We previously predicted that mutants defective in ER inheritance also would show defects in Golgi inheritance. Surprisingly, studies of S. cerevisiae have not revealed the expected link between ER and Golgi inheritance. Here, we revisit this issue by generating mutant strains in which many of the small buds are devoid of detectable ER. These strains also show defects in the inheritance of both early and late Golgi cisternae. Strikingly, virtually all of the buds that lack ER also lack early Golgi cisternae. Our results fit with the idea that membranes exported from the ER coalesce with vesicles derived from existing Golgi compartments to generate new Golgi cisternae. This basic mechanism of Golgi inheritance may be conserved from yeast to vertebrate cells.

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Figures

Fig. 1.
Fig. 1.
ER inheritance is compromised in several mutant strains. (A) The ER marker Hmg1p-GFP was used to image small buds in wild-type, aux1Δ, myo4Δ, and sec8–599 cells that had been grown at 23°C. Representative micrographs display either a single image plane near the center of the bud or a projected z-stack of image planes spanning the entire cell. The sec8–599 micrographs show class 1 and 2 buds, whereas the other three sets of micrographs show class 1 and 5 buds. (Scale bar: 2 μm.) (B) ER inheritance was quantified for the aux1Δ (Left Upper), myo4Δ (Right Upper), and sec8–599 (Lower) strains. The presence or absence of detectable ER membranes was determined for at least 40 buds in each of five different bud size classes, ranging from the smallest visible buds (class 1) to buds that were ≈10% of the mother cell volume (class 5). aux1Δ and myo4Δ cells were examined by using the ER marker Sec61p-GFP, and sec8–599 cells were examined by using Sec61p-GFP and Hmg1p-GFP. For each experiment, wild-type cells were analyzed in parallel with the mutant strain.
Fig. 2.
Fig. 2.
Early Golgi inheritance is delayed in sec8–599 and seb1Δ seb2Δ strains but not in aux1Δ and myo4Δ strains. (A) sec8–599 cells were examined by using the early Golgi markers Sec21p-GFP (Left Upper) and Sec35p-GFP (Right Upper), and aux1Δ and myo4Δ cells were examined by using Sec35p-GFP (Lower). The presence or absence of early Golgi cisternae was determined for at least 40 buds in each of five different bud size classes. (B) seb1Δ seb2Δ cells were examined by using the ER marker Hmg1p-CFP (Upper) and the early Golgi marker Sec21p-YFP (Lower).
Fig. 4.
Fig. 4.
Late Golgi inheritance is delayed in the sec8–599 mutant. (A) Wild-type and sec8–599 cells were labeled with the late Golgi marker Sec7p-GFP. In these projected images, the arrowheads indicate typical small buds that either contain Golgi cisternae in the wild-type cells or lack Golgi cisternae in the sec8–599 cells. (Scale bar: 2 μm.) (B) The late Golgi inheritance defect in the sec8–599 strain was quantified as in Fig. 2.
Fig. 3.
Fig. 3.
Small buds that lack ER membranes also lack early Golgi cisternae. Representative micrographs are shown of sec8–599 cells that were double-labeled with the ER marker Hmg1p-CFP (blue) and the early Golgi marker Sec21p-YFP (yellow). In these projected images, the arrowheads indicate typical small buds devoid of both the ER and the early Golgi marker. (Scale bar: 2 μm.)
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