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The Plant Cell, Vol. 21: 1212–1229, April 2009, www.plantcell.org ã 2009 American Society of Plant Biologists

A Mobile Secretory Vesicle Cluster Involved in Mass Transport from the Golgi to the Plant Cell Exterior
W OA

Kiminori Toyooka,a Yumi Goto,a Satoru Asatsuma,a,b Masato Koizumi,a Toshiaki Mitsui,c and Ken Matsuokaa,b,1
a RIKEN

Plant Science Center, Tsurumi-ku, Yokohama 230-0045,Japan of Plant Nutrition, Faculty of Agriculture, Kyushu University, Higashi-ku, Fukuoka 812-8581, Japan c Laboratories of Plant and Microbial Genome Control, Graduate School of Science and Technology, Niigata University, Ikarashi, Nishi-ku, Niigata 950-2181, Japan
b Laboratory

Secretory proteins and extracellular glycans are transported to the extracellular space during cell growth. Thesematerials are carried in secretory vesicles generated at the trans-Golgi network (TGN). Analysis of the mammalian post-Golgi secretory pathway demonstrated the movement of separated secretory vesicles in the cell. Using secretory carrier membrane protein 2 (SCAMP2) as a marker for secretory vesicles and tobacco (Nicotiana tabacum) BY-2 cell as a model cell, we characterized the transport machinery inplant cells. A combination of analyses, including electron microscopy of quick-frozen cells and four-dimensional analysis of cells expressing fluorescent-tagged SCAMP2, enabled the identification of a clustered structure of secretory vesicles generated from TGN that moves in the cell and eventually fuses with plasma membrane. This structure was termed the secretory vesicle cluster (SVC). The SVCwas also found in Arabidopsis thaliana and rice (Oryza sativa) cells and moved to the cell plate in dividing tobacco cells. Thus, the SVC is a motile structure involved in mass transport from the Golgi to the plasma membrane and cell plate in plant cells.

INTRODUCTION The division and expansion of cells requires trafficking of lipids, proteins, and polysaccharides to the plasma membrane (PM) andextracellular space. These molecules are synthesized and/or modified in the Golgi apparatus and sorted into secretory vesicles at the trans-Golgi network (TGN) for transport to the PM. The Golgi apparatus in plants differs from that in mammals in several aspects, including spatial organization, dynamic properties, and functional activity. Numerous Golgi apparatus are dispersed throughout thecytoplasm in plant cells and move along actin cytoskeletal elements (Nebenfuhr et al., 1999). One function of the plant Golgi apparatus is as the factory for noncellulose extracellular glycans, including hemicellulose and pectin (Cosgrove, 2005). Rapidly dividing plant cells need to synthesize large quantities of these glycans and contain several hundred to thousands of Golgi stacks (Nebenfuhr et al.,1999). The unique features of the plant Golgi apparatus also reflect a difference in the secretory machinery between plants and mammals. Mammalian and yeast cells share a similar transport system for secretory vesicles (Bednarek and Falbel, 2002), and the sorting of proteins at the late secretory pathway is influenced by early, late, and recycling endosomes. In plant cells, the prevacuolarcompartments (PVCs), multivesicular bodies (MVBs), partially

correspondence to kenmat@agr.kyushu-u.ac.jp. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantcell.org) is: Ken Matsuoka (kenmat@agr.kyushu-u.ac.jp). W Online version contains Web-only data. OA Open Accessarticles can be viewed online without a subscription. www.plantcell.org/cgi/doi/10.1105/tpc.108.058933

1 Address

coated reticulum, tubuvesicular endosomes, and vacuoles are involved in secretion and are collectively termed the post-Golgi compartments (Surpin and Raikhel, 2004; Lam et al., 2007b). However, it is not yet clear whether these are the sole elements in the late secretory pathway of...
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