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CELL BIOLOGY AND SIGNAL TRANSDUCTION

Coordination of Plastid Protein Import and Nuclear Gene Expression by Plastid-to-Nucleus Retrograde Signaling^1,[W],[OA]

The 21st Century Centers of Excellence Program, Cryobiofrontier Research Center, Iwate University, Morioka, Iwate 020–8550, Japan (T.K., K.N., T.I.); Iwate Biotechnology Research Center, Kitakami, Iwate 024–0003, Japan (H.M., R.T.); and Department of Environmental Biology, Faculty of Bioscience, Nagahama Institute of Bioscience and Technology, Nagahama, Shiga 526–0829, Japan (F.-S.C.)

Expression of nuclear-encoded plastid proteins and import of those proteins into plastids are indispensable for plastid biogenesis. One possible cellular mechanism that coordinates these two essential processes is retrograde signaling from plastids to the nucleus. However, the molecular details of how this signaling occurs remain elusive. Using the plastid protein import2 mutant of Arabidopsis (Arabidopsis thaliana), which lacks the atToc159 protein import receptor, we demonstrate that the expression of photosynthesis-related nuclear genes is tightly coordinated with their import into plastids. Down-regulation of photosynthesis-related nuclear genes is also observed in mutants lacking other components of the plastid protein import apparatus. Genetic studies indicate that the coordination of plastid protein import and nuclear gene expression is independent of proposed plastid signaling pathways such as the accumulation of Mg-protoporphyrin IX and the activity of ABA INSENSITIVE4 (ABI4). Instead, it may involve GUN1 and the transcription factor AtGLK. The expression level of AtGLK1 is tightly correlated with the expression of photosynthesis-related nuclear genes in mutants defective in plastid protein import. Furthermore, the activity of GUN1 appears to down-regulate the expression of AtGLK1 when plastids are dysfunctional. Based on these data, we suggest that defects in plastid protein import generate a signal that represses photosynthesis-related nuclear genes through repression of AtGLK1 expression but not through activation of ABI4.

² Present address: National Institute of Vegetable and Tea Science, 360 Kusawa, Ano, Tsu, Mie 514–2392, Japan.

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: Takehito Inaba (tinaba{at}iwate-u.ac.jp).

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

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www.plantphysiol.org/cgi/doi/10.1104/pp.109.145987

^* Corresponding author; e-mail tinaba{at}iwate-u.ac.jp.

Received August 10, 2009; accepted August 30, 2009; published September 2, 2009.