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PLANT CELL 18 (5): 1226-1238

Copyright © 2006 by the American Society of Plant Physiologists.

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

Jirong Huanga,1,2, J. Philip Taylora,1, Jin-Gui Chena,3, Joachim F. Uhrigb,4, Danny J. Schnellc, Tsuyoshi Nakagawad, Kenneth L. Korthe, and Alan M. Jonesa,f,5

a Department of Biology, University of North Carolina, Chapel Hill, North Carolina 27599
b Max Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany
c Department of Biochemistry and Molecular Biology, University of Massachusetts, Amherst, Massachusetts 01003
d Research Institute of Molecular Genetics, Shimane University, Matsue 690-8504, Japan
e Department of Plant Pathology, University of Arkansas, Fayetteville, Arkansas 72701
f Department of Pharmacology, University of North Carolina, Chapel Hill, North Carolina 27599

5 To whom correspondence should be addressed. E-mail alan_jones{at}unc.edu; fax 919-962-1625.

Abstract: 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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