Abstract

Vacuoles/lysosomes function in endocytosis and in storage and digestion of metabolites. These organelles are inherited by the daughter cells in eukaryotes. However, the mechanisms of this inheritance are poorly understood because the cells contain multiple vacuoles that behave randomly. The primitive red alga Cyanidioschyzon merolae has a minimum set of organelles. Here, we show that C. merolae contains about four vacuoles that are distributed equally between the daughter cells by binding to dividing mitochondria. Binding is mediated by VIG1, a 30-kD coiled-coil protein identified by microarray analyses and immunological assays. VIG1 appears on the surface of free vacuoles in the cytosol and then tethers the vacuoles to the mitochondria. The vacuoles are released from the mitochondrion in the daughter cells following VIG1 digestion. Suppression of VIG1 by antisense RNA disrupted the migration of vacuoles. Thus, VIG1 is essential for tethering vacuoles to mitochondria during vacuole inheritance in C. merolae.

Highlights

  • The inheritance of single membrane–bound and DNA-less organelles, such as vacuoles/lysosomes, Golgi bodies, endoplasmic reticulum, and microbodies, as well as double membrane–bound organelles, such as mitochondria and plastids, is an essential feature of eukaryotic cell division

  • In the G1 phase, VIG1 was not detected in the cytosol or around the vacuoles as they released from the mitochondrial region in early G1 (Figure 3A)

  • This work provides evidence that vacuoles are inherited by binding to mitochondria in C. merolae

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Summary

INTRODUCTION

The inheritance of single membrane–bound and DNA-less organelles, such as vacuoles/lysosomes, Golgi bodies, endoplasmic reticulum, and microbodies, as well as double membrane–bound organelles, such as mitochondria and plastids, is an essential feature of eukaryotic cell division. Plants, and yeasts, lysosomes/vacuoles are inherited by the daughter cells (Bergeland et al, 2001; Han et al, 2003; Kutsuna et al, 2003). The segregation structures originate from the vacuole membrane and extend to the daughter bud. This inheritance is based on an actin cable and myosin-V motor protein Myo with Vac and Vac (Han et al, 2003; Weisman, 2006). In the primitive red alga Cyanidioschyzon merolae, the vacuoles are inherited by daughter cells through binding to the dividing mitochondrion regardless of the absence of actin filaments and myosin (Takahashi et al, 1995; Matsuzaki et al, 2004; Yagisawa et al, 2007). Candidate genes with a role in vacuole migration during inheritance and show that one such gene, vacuole inheritance gene (vig1), is essential for this process

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