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J. Biol. Chem., Vol. 282, Issue 39, 29013-29021, September 28, 2007

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Plastidic Phosphatidic Acid Phosphatases Identified in a Distinct Subfamily of Lipid Phosphate Phosphatases with Prokaryotic Origin^*

Yuki Nakamura¹, Mami Tsuchiya, and Hiroyuki Ohta^¶2

From the Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, 4259-B-65 Nagatsuta-cho, Midori-ku, Yokohama 226-8501, Japan, the Center for Biological Resources and Informatics, Tokyo Institute of Technology, 4259-B-65 Nagatsuta-cho, Midori-ku, Yokohama 226-8501, Japan, and the ^¶Research Center for the Evolving Earth and Planets, Tokyo Institute of Technology, 4259-B-65 Nagatsuta-cho, Midori-ku, Yokohama 226-8501, Japan

Plastidic phosphatidic acid phosphatase (PAP) dephosphorylates phosphatidic acid to yield diacylglycerol, which is a precursor for galactolipids, a primary and indispensable component of photosynthetic membranes. Despite its functional importance, the molecular characteristics and phylogenetic origin of plastidic PAP were unknown because no potential homologs have been found. Here, we report the isolation and characterization of plastidic PAPs in Arabidopsis that belong to a distinct lipid phosphate phosphatase (LPP) subfamily with prokaryotic origin. Because no homolog of mammalian LPP was found in cyanobacteria, we sought an LPP ortholog in a more primitive organism, Chlorobium tepidum, and its homologs in cyanobacteria. Arabidopsis had five homologs of cyanobacterial LPP, three of which (LPP, LPP1, and LPP2) localized to chloroplasts. Complementation of yeast dpp1lpp1pah1 by plastidic LPPs rescued the relevant phenotype in vitro and in vivo, suggesting that they function as PAPs. Of the three LPPs, LPP activity best resembled the native activity. The three plastidic LPPs were differentially expressed both in green and nongreen tissues, with LPP expressed the highest in shoots. A knock-out mutant for LPP could not be obtained, although a lpp1lpp2 double knock-out showed no significant changes in lipid composition. However, lpp homozygous mutant was isolated only under ectopic overexpression of LPP, suggesting that loss of LPP may cause lethal effect on plant viability. Thus, in Arabidopsis, there are three isoforms of plastidic PAP that belong to a distinct subfamily of LPP, and LPP may be the primary plastidic PAP.

Received for publication, May 29, 2007 , and in revised form, July 24, 2007.

^* This work was supported in part by a Grand-in-aid for Scientific Research on Priority Areas 17051009 from Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan. 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.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. S1 and S2.

¹ Supported by a doctoral fellowship by Japan Society for the Promotion of Science.

² To whom correspondence should be addressed: Center for Biological Resources and Informatics, Tokyo Institute of Technology, 4259-B-65 Nagatsuta-cho, Midori-ku, Yokohama 226-8501, Japan. Tel.: 81-45-924-5736; Fax: 81-45-924-5823; E-mail: ohta.h.ab{at}m.titech.ac.jp.

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