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BIOENERGETICS AND PHOTOSYNTHESIS

Plastid Regulation of Lhcb1 Transcription in the Chlorophyte Alga Dunaliella tertiolecta¹

Environmental Biophysics and Molecular Ecology Program, Institute of Marine and Coastal Sciences, New Brunswick, New Jersey 08901–8521(Y-B.C., M.K., P.G.F.); and Department of Biology, University of New Brunswick, Fredericton, New Brunswick, Canada E3B 6E1 (D.G.D.)

We identify four novel DNA-binding complexes in the nuclear-encoded Lhcb1 promoter of the chlorophyte alga Dunaliella tertiolecta that are regulated by photosynthetic pathways in the plastid. The binding activities of three of the complexes were positively correlated with time-dependent changes in Lhcb1 transcript abundance, implicating their roles as transcriptional enhancers in a retrograde signal transduction pathway. Using a combination of inhibitors, uncouplers, and antimycin A, and by following the kinetic pattern of gene regulation, we infer two different sensors in the signal transduction pathway. On short time scales of 0.5 to about 4 h, the transthylakoid membrane potential appears to be a critical determinant of gene expression, whereas on time scales of 8 h or longer, the redox state of the plastoquinone pool becomes increasingly more important. The differentiation of these two types of signals was observed in parallel effects on gene transcription and on the patterns of DNA-binding activities in the Lhcb1 promoter. These signals appear to be transduced at the nuclear level via a coordinated ensemble of DNA-binding complexes located between –367 and –188 bp from the start codon of the gene. The regulation of these elements allows the cell to up- or down-regulate the expression on Lhcb1 in response to changes in irradiance.

² Present address: Institute of Microbiology, Laboratory of Photosynthesis, Opatovicky mlyn, 379 81 Trebon, Czech Republic.

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.038919.

^* Corresponding author; e-mail falko{at}imcs.rutgers.edu; fax 732–932–4083.

Received January 10, 2004; returned for revision June 28, 2004; accepted August 3, 2004.

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