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J. Biol. Chem., Vol. 279, Issue 8, 6874-6882, February 20, 2004

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Mitochondria Provide the Main Source of Cytosolic ATP for Activation of Outward-rectifying K⁺ Channels in Mesophyll Protoplast of Chlorophyll-deficient Mutant Rice (OsCHLH) Seedlings^*

Chang-Hyo Goh, Ki-Hong Jung¶, Stephen K. Roberts||, Martin R. McAinsh||, Alistair M. Hetherington||, Youn-il Park**, KyeHong Suh, Gynheung An¶, and Hong Gil Nam¶

From the Bionanotechnology Center, Department of Life Science, Pohang University of Science and Technology, the ^¶Division of Molecular and Life Science, Pohang University of Science and Technology, Kyungbuk 790-784, Korea, the ^||Department of Biological Sciences, University of Lancaster, Lancaster LA1 4YQ, United Kingdom, the ^**Department of Biology, Chungnam National University, Taejon 305-764, Korea, and the Division of Life Science, Daegu University, Daegu 712-714, Korea

The role of mitochondria in providing intracellular ATP that controls the activity of plasma membrane outward-rectifying K⁺ channels was evaluated. The OsCHLH rice mutant, which lacks chlorophyll in the thylakoids, was isolated by T-DNA gene trapping (Jung, K.-H., Hur, J., Ryu, C.-H., Choi, Y., Chung, Y.-Y., Miyao, A., Hirochika, H., and An, G. (2003) Plant Cell Physiol. 44, 463-472). The OsCHLH mutant is unable to fix CO₂ and exhibits reduced growth. Wild type and mutant plants exhibit similar rates of respiratory O₂ uptake in the dark, whereas the rate of photosynthetic O₂ evolution by the mutant was negligible during illumination. During dark respiration the wild type and mutant exhibited similar levels of cytoplasmic ATP. In the mutant oligomycin treatment (an inhibitor of mitochondrial F₁F₀-ATPase) drastically reduced ATP production. The fact that this was reversed by the addition of glucose suggested that the mutant produced ATP exclusively from mitochondria but not from chloroplasts. In whole cell patch clamp experiments, the activity of outward-rectifying K⁺ channels of rice mesophyll cells showed ATP-dependent currents, which were 1.5-fold greater in wild type than in mutant cells. Channels in both wild type and mutant cells were deactivated by the removal of cytosolic ATP, whereas in the presence of ATP the channels remained active. We conclude that mesophyll cells in the OsCHLH rice mutant derive ATP from mitochondrial respiration, and that this is critical for the normal function of plasma membrane outward-rectifying K⁺ channels.

Received for publication, August 15, 2003 , and in revised form, December 2, 2003.

^* This work was supported by a Korea and United Kingdom scientist exchange program (to C.-H. G.) and partly supported by Brain Korea 21 and Korean Research Foundation Grant 2003-005-C00011. 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.

To whom correspondence should be addressed. Tel.: 82-54-279-8283; Fax: 82-54-279-2199; E-mail: gohunse{at}postech.ac.kr.

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