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Plant and Cell Physiology Advance Access originally published online on August 18, 2007
Plant and Cell Physiology 2007 48(10):1414-1425; doi:10.1093/pcp/pcm109
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© The Author 2007. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oxfordjournals.org

Elicitor-Induced Cytoskeletal Rearrangement Relates to Vacuolar Dynamics and Execution of Cell Death: In Vivo Imaging of Hypersensitive Cell Death in Tobacco BY-2 Cells

Takumi Higaki1,2,5, Tatsuaki Goh2,5,6, Teruyuki Hayashi2,3, Natsumaro Kutsuna1, Yasuhiro Kadota2,7, Seiichiro Hasezawa1, Toshio Sano1 and Kazuyuki Kuchitsu2,3,4,*

1Department of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwanoha Kashiwa, Chiba, 277-8562 Japan
2Department of Applied Biological Science, Tokyo University of Science, 2641 Yamazaki, Noda, Chiba, 278-8510 Japan
3Research Center for Health Science of Nanoparticles, Tokyo University of Science, 2641 Yamazaki, Noda, Chiba, 278-8510 Japan
4Genome & Drug Research Center, Tokyo University of Science, 2641 Yamazaki, Noda, Chiba, 278-8510 Japan

*Corresponding author: E-mail, kuchitsu{at}rs.noda.tus.ac.jp; Fax, +81-4-7123-9767.


  Abstract

Disintegration of the vacuolar membrane (VM) has been proposed to be a crucial event in various types of programmed cell death (PCD) in plants. However, its regulatory mechanisms are mostly unknown. To obtain new insights on the regulation of VM disintegration during hypersensitive cell death, we investigated the structural dynamics and permeability of the VM, as well as cytoskeletal reorganization during PCD in tobacco BY-2 cells induced by a proteinaceous elicitor, cryptogein. From sequential observations, we have identified the following remarkable events during PCD. Stage 1: bulb-like VM structures appear within the vacuolar lumen and the cortical microtubules are disrupted, while the cortical actin microfilaments are bundled. Simultaneously, transvacuolar strands including endoplasmic microtubules and actin microfilaments are gradually disrupted and the nucleus moves from the center to the periphery of the cell. Stage 2: cortical actin microfilament bundles and complex bulb-like VM structures disappear. The structure of the large central vacuole becomes simpler, and small spherical vacuoles appear. Stage 3: the VM is disintegrated and a fluorescent dye, BCECF, leaks out of the vacuoles just prior to PCD. Application of an actin polymerization inhibitor facilitates both the disappearance of bulb-like vacuolar membrane structures and induction of cell death. These results suggest that the elicitor-induced reorganization of actin microfilaments is involved in the regulation of hypersensitive cell death via modification of the vacuolar structure to induce VM disintegration.

Keywords: Actin microfilament - Green fluorescent protein - Hypersensitive cell death - Tobacco BY-2 cells - Transvacuolar strand - Vacuole

Abbreviations: ABD, actin-binding domain; BA, bistheonellide A; BCECF-AM, 2',7'-bis-(2-carboxyethyl)-5-(and-6)-carboxyfluorescein acetoxymethyl ester; DIC, differential interference contrast; GFP, green fluorescent protein; MF, actin microfilament; PCD, programmed cell death; PM, plasma membrane; TVS, transvacuolar strand; VM, vacuolar membrane.

5These authors equally contributed to this work.

6Present address: Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-0033 Japan.

7Present address: RIKEN Plant Science Center, 1-7-22 Suehiro-cho, Tsurumi-ku, Kanagawa, 230-0045 Japan.

(Received May 20, 2007; Accepted August 13, 2007)
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