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J. Biol. Chem., Vol. 280, Issue 9, 7469-7476, March 4, 2005

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A Novel Phosphatidylcholine-hydrolyzing Phospholipase C Induced by Phosphate Starvation in Arabidopsis^*

Yuki Nakamura, Koichiro Awai¶||, Tatsuru Masuda**, Yasushi Yoshioka, Ken-ichiro Takamiya, and Hiroyuki Ohta

From the Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, 4259-B-14 Nagatsuta-cho, Midori-ku, Yokohama, 226-8501, Japan, the ^¶Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan, 48824, and the Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, 464-8602, Japan

During phosphate starvation, it is known that phospholipids are degraded, and conversely, a nonphosphorus galactolipid digalactosyldiacylglycerol accumulates in the root plasma membrane of plants. We report a novel phospholipase C that hydrolyzes phosphatidylcholine and is greatly induced in response to phosphate deprivation in Arabidopsis. Since phosphatidylcholine-hydrolyzing activity by phospholipase C was highly up-regulated in phosphate-deprived plants, gene expression of some phospholipase C was expected to be induced during phosphate starvation. Based on amino acid sequence similarity to a bacterial phosphatidylcholine-hydrolyzing phospholipase C, six putative phospholipase Cs were identified in the Arabidopsis genome, one of which, NPC4, showed significant transcriptional activation upon phosphate limitation. Molecular cloning and functional expression of NPC4 confirmed that the NPC4 gene encoded a functional phosphatidylcholine-hydrolyzing phospholipase C that did not require Ca²⁺ for its activity. Subcellular localization analysis showed that NPC4 protein was highly enriched in the plasma membrane. Analyses of transferred DNA-tagged npc4 mutants revealed that disruption of NPC4 severely reduces the phosphatidylcholine-hydrolyzing phospholipase C activity in response to phosphate starvation. These results suggest that NPC4 plays an important role in the supply of both inorganic phosphate and diacylglycerol from membrane-localized phospholipids that would be used for phosphate supplementation and the replacement of polar lipids in the root plasma membrane during phosphate deprivation.

Received for publication, August 2, 2004 , and in revised form, December 21, 2004.

^* This work was supported in part by Ministry of Education, Sports, Science, and Culture of Japan Grant-in-aid for Scientific Research on Priority Areas 15380049. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Supported by the Grant of the 21st Century COE Program.

^|| Supported by JSPS Postdoctoral Fellowships for Research Abroad, the Ministry of Education, Sports, Science and Culture of Japan.

^** Present address: Dept. of General Systems Studies, Graduate School of Arts and Sciences, The University of Tokyo, 3-8-1 Komaba, Meguro, Tokyo 153-8902, Japan.

To whom correspondence should be addressed: Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, 4259-B-14 Nagatsuta-cho, Midori-ku, Yokohama, Kanagawa 226-8501, Japan. Tel.: 81-45-924-5736; Fax: 81-45-924-5823; E-mail: hohta{at}bio.titech.ac.jp.

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