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Published on May 5, 2006; 10.1104/pp.106.080457

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Received March 15, 2006
Returned for revision March 27, 2006
Accepted April 26, 2006

Illumination is necessary and sufficient to induce histone acetylation independent of transcriptional activity at the C4-specific phosphoenolpyruvate carboxylase promoter in maize

Sascha Offermann , Tanja Danker , Daniela Dreymüller , Rainer Kalamajka , Sonja Töpsch , Katrin Weyand , and Christoph Peterhänsel *

RWTH Aachen, Institute for Biology I, Worringer Weg 1, 52056 Aachen, Germany

* Corresponding author; email: cp{at}bio1.rwth-aachen.de.

Expression of the C4-specific phosphoenolpyruvate carboxylase (C4-PEPC) gene in maize (Zea mays L.) is regulated in a tissue-specific manner but affected by light and nutrient availability. We manipulated these stimuli in a combinatorial manner and analysed 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 a 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 irrespective of the transcriptional activity of the gene. Our data indicate that an understanding of the interplay between histone modifications and transcription requires the analysis of the signal integration on promoters in vivo.




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