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

• Published in: The Plant cell 2006-05, Vol.18 (5), p.1226-1238
• Main Authors: Huang, Jirong, Taylor, J. Philip, Chen, Jin-Gui, Uhrig, Joachim F, Schnell, Danny J, Nakagawa, Tsuyoshi, Korth, Kenneth L, Jones, Alan M
• Format: Article
• Language: English
• Subjects: Amino Acid Sequence; Arabidopsis - anatomy & histology; Arabidopsis - metabolism; Arabidopsis - ultrastructure; Arabidopsis Proteins - analysis; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Arabidopsis thaliana; Cell membranes; Energy transfer; Fluorescence; Glucose; Glucose - metabolism; Glucose - pharmacology; GTP-Binding Protein alpha Subunits - genetics; GTP-Binding Protein alpha Subunits - metabolism; Intracellular Membranes - metabolism; Membrane Proteins - analysis; Membrane Proteins - genetics; Membrane Proteins - metabolism; Membranes; Meristem - metabolism; Models, Biological; Molecular Sequence Data; Plant cells; Plant growth; Plant Roots - anatomy & histology; Plant Roots - growth & development; Plant Roots - metabolism; Plants; Plasma interactions; Plastids; Plastids - metabolism; Plastids - ultrastructure; Protein Interaction Mapping; Proteins; Seedlings; Sequence Alignment; Signal Transduction; Sugar; Sugars; Two-Hybrid System Techniques; Yeasts
• ISSN: 1040-4651; 1532-298X; 1532-298X
• DOI: 10.1105/tpc.105.037259

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 Gα 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.