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Science 305 (5685): 855-858

Copyright © 2004 by the American Association for the Advancement of Science

A Plant Vacuolar Protease, VPE, Mediates Virus-Induced Hypersensitive Cell Death

Noriyuki Hatsugai,1,2,3 Miwa Kuroyanagi,1 Kenji Yamada,2,3 Tetsuo Meshi,4 Shinya Tsuda,5 Maki Kondo,2 Mikio Nishimura,2,3 Ikuko Hara-Nishimura1*

Abstract: Programmed cell death (PCD) in animals depends on caspase protease activity. Plants also exhibit PCD, for example as a response to pathogens, although a plant caspase remains elusive. Here we show that vacuolar processing enzyme (VPE) is a protease essential for a virus-induced hypersensitive response that involves PCD. VPE deficiency prevented virus-induced hypersensitive cell death in tobacco plants. VPE is structurally unrelated to caspases, although VPE has a caspase-1 activity. Thus, plants have evolved a regulated cellular suicide strategy that, unlike PCD of animals, is mediated by VPE and the cellular vacuole.

1 Graduate School of Science, Kyoto University, Sakyo-ku, Kyoto 606-8502, Japan.
2 Department of Cell Biology, National Institute for Basic Biology, Okazaki 444-8585, Japan.
3 School of Life Science, Graduate University for Advanced Studies, Okazaki 444-8585, Japan.
4 National Institute of Agrobiological Sciences, Tsukuba 305-8602, Japan.
5 National Agricultural Research Center, Tsukuba 305-8666, Japan.

* To whom correspondence should be addressed. E-mail: ihnishi{at}gr.bot.kyoto-u.ac.jp


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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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F. Quattrocchio, W. Verweij, A. Kroon, C. Spelt, J. Mol, and R. Koes (2006)
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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