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CELL BIOLOGY AND SIGNAL TRANSDUCTION

Role of the Rice Hexokinases OsHXK5 and OsHXK6 as Glucose Sensors^1,[C],[W]

Plant Metabolism Research Center and Graduate School of Biotechnology, Kyung Hee University, Yongin 446–701, Korea (J.-I.C., N.R., J.-S.E., D.-W.L., H.-B.K., Y.-K.K., M.-H.C., S.H.B., T.-R.H., J.-S.J.); Department of Biology, Chungnam National University, Daejeon 305–764, Korea (S.-W.J., Y.-I.P.); Department of Horticultural Biotechnology, Kyung Hee University, Yongin 446–701, Korea (Y.-H.L.); Department of Life Sciences, Pohang University of Science and Technology, Pohang 790–784, Korea (I.H.); and Department of Molecular Biology, Massachusetts General Hospital, Department of Genetics, Harvard Medical School, Boston, Massachusetts 02114 (J.S.)

The Arabidopsis (Arabidopsis thaliana) hexokinase 1 (AtHXK1) is recognized as an important glucose (Glc) sensor. However, the function of hexokinases as Glc sensors has not been clearly demonstrated in other plant species, including rice (Oryza sativa). To investigate the functions of rice hexokinase isoforms, we characterized OsHXK5 and OsHXK6, which are evolutionarily related to AtHXK1. Transient expression analyses using GFP fusion constructs revealed that OsHXK5 and OsHXK6 are associated with mitochondria. Interestingly, the OsHXK5mTP-GFP and OsHXK6mTP-GFP fusion proteins, which lack N-terminal mitochondrial targeting peptides, were present mainly in the nucleus with a small amount of the proteins seen in the cytosol. In addition, the OsHXK5NLS-GFP and OsHXK6NLS-GFP fusion proteins harboring nuclear localization signals were targeted predominantly in the nucleus, suggesting that these OsHXKs retain a dual-targeting ability to mitochondria and nuclei. In transient expression assays using promoter::luciferase fusion constructs, these two OsHXKs and their catalytically inactive alleles dramatically enhanced the Glc-dependent repression of the maize (Zea mays) Rubisco small subunit (RbcS) and rice -amylase genes in mesophyll protoplasts of maize and rice. Notably, the expression of OsHXK5, OsHXK6, or their mutant alleles complemented the Arabidopsis glucose insensitive2-1 mutant, thereby resulting in wild-type characteristics in seedling development, Glc-dependent gene expression, and plant growth. Furthermore, transgenic rice plants overexpressing OsHXK5 or OsHXK6 exhibited hypersensitive plant growth retardation and enhanced repression of the photosynthetic gene RbcS in response to Glc treatment. These results provide evidence that rice OsHXK5 and OsHXK6 can function as Glc sensors.

² These authors contributed equally to the article.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Jong-Seong Jeon (jjeon{at}khu.ac.kr).

^[C] Some figures in this article are displayed in color online but in black and white in the print edition.

^[W] The online version of this article contains Web-only data.

www.plantphysiol.org/cgi/doi/10.1104/pp.108.131227

^* Corresponding author; e-mail jjeon{at}khu.ac.kr.

Received October 16, 2008; accepted November 10, 2008; published November 14, 2008.

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