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SYSTEMS BIOLOGY, MOLECULAR BIOLOGY, AND GENE REGULATION

Illumination Is Necessary and Sufficient to Induce Histone Acetylation Independent of Transcriptional Activity at the C₄-Specific Phosphoenolpyruvate Carboxylase Promoter in Maize¹

RWTH Aachen University, Institute for Biology I, 52056 Aachen, Germany

Expression of the C₄-specific phosphoenolpyruvate carboxylase (C₄-PEPC) gene in maize (Zea mays) is regulated in a tissue-specific manner, but affected by light and nutrient availability. We manipulated these stimuli in a combinatorial manner and analyzed concomitant changes in histone acetylation of the nucleosomes associated with the C₄-PEPC gene in relation to transcriptional activity and steady-state mRNA levels. Whereas the transition from the lowest activity to an intermediate activity was observed in the absence of histone acetylation, the light-induced boost to full activity was associated with strong enhancement of the acetylation of both histones H3 and H4 limited to the gene region. Once activated by light, prolonged darkness was necessary to reduce both transcription and, in parallel, histone acetylation. Unexpectedly, histone acetylation was also induced in bundle sheath cells, although the transcriptional activity did not respond to illumination in this tissue. Furthermore, we were able to down-regulate the promoter by nitrogen depletion in the light without any decrease in the hyperacetylation of histone H4. When plants kept in prolonged darkness were nitrogen depleted and then exposed to light, transcription was not induced, but the promoter chromatin became hyperacetylated. We suggest a model where inhibition of a histone deacetylase in the light triggers H4 hyperacetylation at the C₄-PEPC gene promoter regardless of the transcriptional activity of the gene. Our data indicate that an understanding of the interplay between histone modification and transcription requires analysis of signal integration on promoters in vivo.

² These authors contributed equally to the paper.

³ Present address: Interdisziplinäres Zentrum für Klinische Forschung Biomat, Universitaetsklinikum Aachen, 52074 Aachen, Germany.

⁴ Present address: Institute of Life Sciences, Aalborg University, DK–9000 Aalborg, Denmark.

⁵ Present address: Institut für Zelluläre und Molekulare Botanik, Abteilung Molekulare Evolution, Kirschallee 1, 53115 Bonn, Germany.

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: Christoph Peterhänsel (cp{at}bio1.rwth-aachen.de).

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.106.080457.

^* Corresponding author; e-mail cp{at}bio1.rwth-aachen.de; fax 49–241–80622632.

Received March 15, 2006; returned for revision April 25, 2006; accepted April 26, 2006.

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