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J. Biol. Chem., Vol. 282, Issue 16, 12298-12309, April 20, 2007

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High Resolution Structure of Deinococcus Bacteriophytochrome Yields New Insights into Phytochrome Architecture and Evolution^*

Jeremiah R. Wagner, Junrui Zhang, Joseph S. Brunzelle, Richard D. Vierstra¹, and Katrina T. Forest^¶2

From the Departments of Genetics and ^¶Bacteriology, University of Wisconsin, Madison, Wisconsin 53706 and the Life Sciences Collaborative Access Team, Northwestern University, Argonne, Illinois 60439

Phytochromes are red/far red light photochromic photoreceptors that direct many photosensory behaviors in the bacterial, fungal, and plant kingdoms. They consist of an N-terminal domain that covalently binds a bilin chromophore and a C-terminal region that transmits the light signal, often through a histidine kinase relay. Using x-ray crystallography, we recently solved the first three-dimensional structure of a phytochrome, using the chromophore-binding domain of Deinococcus radiodurans bacterial phytochrome assembled with its chromophore, biliverdin IX. Now, by engineering the crystallization interface, we have achieved a significantly higher resolution model. This 1.45Å resolution structure helps identify an extensive buried surface between crystal symmetry mates that may promote dimerization in vivo. It also reveals that upon ligation of the C3² carbon of biliverdin to Cys²⁴, the chromophore A-ring assumes a chiral center at C2, thus becoming 2(R),3(E)-phytochromobilin, a chemistry more similar to that proposed for the attached chromophores of cyanobacterial and plant phytochromes than previously appreciated. The evolution of bacterial phytochromes to those found in cyanobacteria and higher plants must have involved greater fitness using more reduced bilins, such as phycocyanobilin, combined with a switch of the attachment site from a cysteine near the N terminus to one conserved within the cGMP phosphodiesterase/adenyl cyclase/FhlA domain. From analysis of site-directed mutants in the D. radiodurans phytochrome, we show that this bilin preference was partially driven by the change in binding site, which ultimately may have helped photosynthetic organisms optimize shade detection. Collectively, these three-dimensional structural results better clarify bilin/protein interactions and help explain how higher plant phytochromes evolved from prokaryotic progenitors.

Received for publication, December 26, 2006 , and in revised form, February 20, 2007.

The atomic coordinates and structure factors (code 2O9B and 2O9C) have been deposited in the Protein Data Bank, Research Collaboratory for Structural Bioinformatics, Rutgers University, New Brunswick, NJ (http://www.rcsb.org/).

^* This work was supported by National Science Foundation Grant MCB-0424062 (to R. D. V. and K. T. F.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Fig. 1.

¹ To whom correspondence may be addressed: Dept. of Genetics, 425-G Henry Mall, University of Wisconsin, Madison, WI 53706. Tel.: 608-262-8215; Fax: 608-262-2976; E-mail: vierstra{at}wisc.edu.

² To whom correspondence may be addressed: Dept. of Bacteriology, University of Wisconsin, Madison, WI 53706. Tel.: 608-265-3566; Fax: 608-262-9865; E-mail: forest{at}bact.wisc.edu.

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