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J. Biol. Chem., Vol. 283, Issue 1, 461-468, January 4, 2008

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Differential Degradation of Extraplastidic and Plastidic Lipids during Freezing and Post-freezing Recovery in Arabidopsis thaliana^*

Weiqi Li¹, Ruiping Wang, Maoyin Li, Lixia Li, Chuanming Wang^¶, Ruth Welti^||, and Xuemin Wang

From the Kunming Institute of Botany, Chinese Academy of Sciences, 132 Lanhei Road, Kunming 650204, China, the Department of Biology, University of Missouri and Donald Danforth Plant Science Center, St. Louis, Missouri 63121, the ^¶Department of Biology, Honghe University, Mengzi, Yunnan 661100, China, and the ^||Kansas Lipidomics Research Center, Division of Biology, Kansas State University, Manhattan, Kansas 66506

Changes in membrane lipid composition play important roles in plant adaptation to and survival after freezing. Plant response to cold and freezing involves three distinct phases: cold acclimation, freezing, and post-freezing recovery. Considerable progress has been made toward understanding lipid changes during cold acclimation and freezing, but little is known about lipid alteration during post-freezing recovery. We previously showed that phospholipase D (PLD) is involved in lipid hydrolysis and Arabidopsis thaliana freezing tolerance. This study was undertaken to determine how lipid species change during post-freezing recovery and to determine the effect of two PLDs, PLD1 and PLD, on lipid changes during post-freezing recovery. During post-freezing recovery, hydrolysis of plastidic lipids, monogalactosyldiacylglycerol and plastidic phosphatidylglycerol, is the most prominent change. In contrast, during freezing, hydrolysis of extraplastidic phospholipids, phosphatidylcholine and phosphatidylethanolamine, occurs. Suppression of PLD1 decreased phospholipid hydrolysis and phosphatidic acid production in both the freezing and post-freezing phases, whereas ablation of PLD increased lipid hydrolysis and phosphatidic acid production during post-freezing recovery. Thus, distinctly different changes in lipid hydrolysis occur in freezing and post-freezing recovery. The presence of PLD1 correlates with phospholipid hydrolysis in both freezing and post-freezing phases, whereas the presence of PLD correlates with reduced lipid hydrolysis during post-freezing recovery. These data suggest a negative role for PLD1 and a positive role for PLD in freezing tolerance.

Received for publication, August 13, 2007 , and in revised form, October 24, 2007.

^* The work was supported by grants from the United States Department of Agriculture, the Kansas State University (KSU) Plant Biotechnology Center, the National Basic Research Program of China (Grant 2006CB100100), Knowledge Innovation Program of CAS (KSCX2-YW-N-014), NSFC (30670474), NSF (MCB 0455318, IOS 0454866, DBI 0521587, and Kansas NSF EPSCoR award, EPS-0236913), with support from the State of Kansas through the Kansas Technology Enterprise Corporation and KSU, as well from United States Public Health Services Grant P20 RR016475 from the INBRE program of the National Center for Research Resources. 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 Table S1.

¹ To whom correspondence should be addressed. Tel.: 86-871-522-3025; Fax: 86-871-522-3018; E-mail: weiqili{at}mail.kib.ac.cn.

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