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Plant and Cell Physiology Advance Access originally published online on February 27, 2009
Plant and Cell Physiology 2009 50(4):855-868; doi:10.1093/pcp/pcp031
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© The Author 2009. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oxfordjournals.org

This article appears in the following Plant and Cell Physiology issue: Special Issue Articles: Photosynthesis [View the issue table of contents]

Microtubules Regulate Dynamic Organization of Vacuoles in Physcomitrella patens

Yoshihisa Oda1,8, Aiko Hirata1, Toshio Sano1,2, Tomomichi Fujita3, Yuji Hiwatashi4,7, Yoshikatsu Sato5, Akeo Kadota6, Mitsuyasu Hasebe4,5,7 and Seiichiro Hasezawa1,2,*

1Department of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwanoha 5-1-5, Kashiwa, Chiba, 277-8562 Japan
2Institute for Bioinformatics Research and Development (BIRD), Japan Science and Technology Agency (JST), Chiyoda-ku, Tokyo, 102-8666 Japan
3Department of Biological Sciences, Faculty of Science, Hokkaido University, Kita-ku Kita-10-jo-Nishi-8, Sapporo, 060-0810, Hokkaido, Japan
4Division of Evolutionary Biology, National Institute for Basic Biology, Okazaki, 444-8585 Japan
5ERATO, JST, Okazaki, 444-8585 Japan
6Department of Biological Sciences, Graduate School of Science and Engineering, Tokyo Metropolitan University, Minami-Ohsawa 1-1, Hachioji, Tokyo, 192-0397 Japan
7Department of Basic Biology, School of Life Science, The Graduate University for Advanced Studies, Okazaki, 444-8585 Japan

*Corresponding author: E-mail, hasezawa{at}k.u-tokyo.ac.jp. Fax, +81-4-7136-3706


  Abstract

Eukaryotic cells have developed several essential membrane components. In flowering plants, appropriate structures and distributions of the major membrane components are predominantly regulated by actin microfilaments. In this study, we have focused on the regulatory mechanism of vacuolar structures in the moss, Physcomitrella patens. The high ability of P. patens to undergo homologous recombination enabled us stably to express green fluorescent protein (GFP) or red fluorescent protein (RFP) fusion proteins, and the simple body structure of P. patens enabled us to perform detailed visualization of the intracellular vacuolar and cytoskeletal structures. Three-dimensional analysis and high-speed time-lapse observations revealed surprisingly complex structures and dynamics of the vacuole, with inner sheets and tubular protrusions, and frequent rearrangements by separation and fusion of the membranes. Depolymerization of microtubules dramatically affected these structures and movements. Dual observation of microtubules and vacuolar membranes revealed that microtubules induced tubular protrusions and cytoplasmic strands of the vacuoles, indicative of interactions between microtubules and vacuolar membranes. These results demonstrate a novel function of microtubules in maintaining the distribution of the vacuole and suggest a functional divergence of cytoskeletal functions in land plant evolution.

Keywords: Actin microfilament - Cytoskeleton - Microtubule - Physcomitrella patens - Vacuolar membrane - Vacuole

Abbreviations: BCECF-AM, 2,7-bis-(2-carboxyethyl)-5(6)-carboxyfluoresceine-acetoxymethylester; CLSM, confocal laser scanning microscopy; DMSO, dimethylsulfoxide; GFP, green fluorescent protein; ER, endoplasmic reticulum; FM4-64, N-(3-triethylammoniumpropyl)-4-(6-(4-(diethylamino)phenyl)hexatrienyl pyridinium dibromide; mRFP, monomeric red fluorescent protein.

8Present address: Department of Biological Science, Graduate School of Sciences, The University of Tokyo, Hongo 7-3-1, Bunkyo-ku, Tokyo, 113-0033 Japan.

(Received October 30, 2008; Accepted February 19, 2009)
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