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J. Biol. Chem., Vol. 280, Issue 28, 26137-26142, July 15, 2005

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5-Formyltetrahydrofolate Is an Inhibitory but Well Tolerated Metabolite in Arabidopsis Leaves^*

Aymeric Goyer, Eva Collakova¶, Rocío Díaz de la Garza, Eoin P. Quinlivan||, Jerry Williamson||, Jesse F. Gregory, III||, Yair Shachar-Hill¶, and Andrew D. Hanson**

From the Horticultural Sciences Department and ^||Food Science and Human Nutrition Departments, University of Florida, Gainesville, Florida 32611 and the ^¶Department of Plant Biology, Michigan State University, East Lansing, Michigan 48824

5-Formyltetrahydrofolate (5-CHO-THF) is formed via a second catalytic activity of serine hydroxymethyltransferase (SHMT) and strongly inhibits SHMT and other folate-dependent enzymes in vitro. The only enzyme known to metabolize 5-CHO-THF is 5-CHO-THF cycloligase (5-FCL), which catalyzes its conversion to 5,10-methenyltetrahydrofolate. Because 5-FCL is mitochondrial in plants and mitochondrial SHMT is central to photorespiration, we examined the impact of an insertional mutation in the Arabidopsis 5-FCL gene (At5g13050) under photorespiratory (30 and 370 µmol of CO₂ mol^–1) and non-photorespiratory (3200 µmol of CO₂ mol^–1) conditions. The mutation had only mild visible effects at 370 µmol of CO₂ mol^–1, reducing growth rate by 20% and delaying flowering by 1 week. However, the mutation doubled leaf 5-CHO-THF level under all conditions and, under photorespiratory conditions, quadrupled the pool of 10-formyl-/5,10-methenyltetrahydrofolates (which could not be distinguished analytically). At 370 µmol of CO₂ mol^–1, the mitochondrial 5-CHO-THF pool was 8-fold larger in the mutant and contained most of the 5-CHO-THF in the leaf. In contrast, the buildup of 10-formyl-/5,10-methenyltetrahydrofolates was extramitochondrial. In photorespiratory conditions, leaf glycine levels were up to 46-fold higher in the mutant than in the wild type. Furthermore, when leaves were supplied with 5-CHO-THF, glycine accumulated in both wild type and mutant. These data establish that 5-CHO-THF can inhibit SHMT in vivo and thereby influence glycine pool size. However, the near-normal growth of the mutant shows that even exceptionally high 5-CHO-THF levels do not much affect fluxes through SHMT or any other folate-dependent reaction, i.e. that 5-CHO-THF is well tolerated in plants.

Received for publication, March 21, 2005 , and in revised form, May 5, 2005.

^* This work was supported in part by the Florida Agricultural Experimental Station, by an endowment from the C. V. Griffin, Sr. Foundation, and by Grants MCB-0114117 and MCB-0129944 from the National Science Foundation and approved for publication as Journal Series No. R-10807. 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.

These authors contributed equally to this study.

^** To whom correspondence should be addressed: Horticultural Sciences Dept., University of Florida, Gainesville, FL 32611. Tel.: 352-392-1928 (ext. 334); Fax: 352-392-5653; E-mail: adha{at}mail.ifas.ufl.edu.

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