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Plant Cell Advance Online Publication
Published on March 31, 2006; 10.1105/tpc.105.037259

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Received August 19, 2005
Returned for revision March 7, 2006
Accepted March 15, 2006

The Plastid Protein THYLAKOID FORMATION1 and the Plasma Membrane G-Protein GPA1 Interact in a Novel Sugar-Signaling Mechanism in Arabidopsis

Jirong Huang 1, J. Philip Taylor 1, Jin-Gui Chen 1, Joachim F. Uhrig 2, Danny J. Schnell 3, Tsuyoshi Nakagawa 4, Kenneth L. Korth 5, and Alan M. Jones 6*

1 Department of Biology, University of North Carolina, Chapel Hill, North Carolina 27599
2 Max Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany
3 Department of Biochemistry and Molecular Biology, University of Massachusetts, Amherst, Massachusetts 01003
4 Research Institute of Molecular Genetics, Shimane University, Matsue 690-8504, Japan
5 Department of Plant Pathology, University of Arkansas, Fayetteville, Arkansas 72701
6 Department of Biology, University of North Carolina, Chapel Hill, North Carolina 27599; Department of Pharmacology, University of North Carolina, Chapel Hill, North Carolina 27599

* To whom correspondence should be addressed. E-mail: alan_jones{at}unc.edu.

Mutations in genes encoding components of the heterotrimeric G-protein complex were previously shown to confer altered sensitivity to increased levels of D-glucose. This suggests that G-protein coupling may be a novel sugar-signaling mechanism in Arabidopsis thaliana. THYLAKOID FORMATION1 (THF1) is here demonstrated in vivo as a G{alpha} interaction partner that functions downstream of the plasma membrane-delimited heterotrimeric G-protein (GPA1) in a D-glucose signaling pathway. THF1 is a plastid protein localized to both the outer plastid membrane and the stroma. Contact between root plastidic THF1 and GPA1 at the plasma membrane occurs at sites where the plastid membrane abuts the plasma membrane, as demonstrated by Förster resonance energy transfer (FRET). A probable role for THF1 in sugar signaling is demonstrated by both biochemical and genetic evidence. Root growth in the thf1-1 null mutant is hypersensitive to exogenous D-glucose, and THF1-overexpressing roots are resistant to inhibition of growth rate by high D-glucose. Additionally, THF1 levels are rapidly degraded by D-glucose but not L-glucose. The interaction between THF1 and GPA1 has been confirmed by in vitro and in vivo coimmunoprecipitation, FRET analysis, and genetic epistasis and provides evidence of a sugar-signaling mechanism between plastids and the plasma membrane.






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