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The structure of a complete phytochrome sensory module in the Pr ground state.

ABSTRACT: Phytochromes are red/far-red photochromic biliprotein photoreceptors, which in plants regulate seed germination, stem extension, flowering time, and many other light effects. However, the structure/functional basis of the phytochrome photoswitch is still unclear. Here, we report the ground state structure of the complete sensory module of Cph1 phytochrome from the cyanobacterium Synechocystis 6803. Although the phycocyanobilin (PCB) chromophore is attached to Cys-259 as expected, paralleling the situation in plant phytochromes but contrasting to that in bacteriophytochromes, the ZZZssa conformation does not correspond to that expected from Raman spectroscopy. We show that the PHY domain, previously considered unique to phytochromes, is structurally a member of the GAF (cGMP phosphodiesterase/adenylyl cyclase/FhlA) family. Indeed, the tandem-GAF dumbbell revealed for phytochrome sensory modules is remarkably similar to the regulatory domains of cyclic nucleotide (cNMP) phosphodiesterases and adenylyl cyclases. A unique feature of the phytochrome structure is a long, tongue-like protrusion from the PHY domain that seals the chromophore pocket and stabilizes the photoactivated far-red-absorbing state (Pfr). The tongue carries a conserved PRxSF motif, from which an arginine finger points into the chromophore pocket close to ring D forming a salt bridge with a conserved aspartate residue. The structure that we present provides a framework for light-driven signal transmission in phytochromes.

SUBMITTER: Essen LO

PROVIDER: S-EPMC2567182 | biostudies-literature | 2008 Sep

REPOSITORIES: biostudies-literature

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The structure of a complete phytochrome sensory module in the Pr ground state.

Essen Lars-Oliver LO Mailliet Jo J Hughes Jon J

Proceedings of the National Academy of Sciences of the United States of America 20080917 38

Phytochromes are red/far-red photochromic biliprotein photoreceptors, which in plants regulate seed germination, stem extension, flowering time, and many other light effects. However, the structure/functional basis of the phytochrome photoswitch is still unclear. Here, we report the ground state structure of the complete sensory module of Cph1 phytochrome from the cyanobacterium Synechocystis 6803. Although the phycocyanobilin (PCB) chromophore is attached to Cys-259 as expected, paralleling the ...[more]

PMID: 18799745

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Project description:We present structural information for oat phyA3 in the far-red-light-absorbing (Pfr) signaling state, to our knowledge the first three-dimensional (3D) information for a plant phytochrome as Pfr. Solid-state magic-angle spinning (MAS) NMR was used to detect interatomic contacts in the complete photosensory module [residues 1-595, including the NTE (N-terminal extension), PAS (Per/Arnt/Sim), GAF (cGMP phosphodiesterase/adenylyl cyclase/FhlA) and PHY (phytochrome-specific) domains but with the C-terminal PAS repeat and transmitter-like module deleted] auto-assembled in vitro with 13C- and 15N-labeled phycocyanobilin (PCB) chromophore. Thereafter, quantum mechanics/molecular mechanics (QM/MM) enabled us to refine 3D structural models constrained by the NMR data. We provide definitive atomic assignments for all carbon and nitrogen atoms of the chromophore, showing the Pfr chromophore geometry to be periplanar ZZEssa with the D -ring in a ?-facial disposition incompatible with many earlier notions regarding photoconversion yet supporting circular dichroism (CD) data. The Y268 side chain is shifted radically relative to published Pfr crystal structures in order to accommodate the ?-facial ring D . Our findings support a photoconversion sequence beginning with Pr photoactivation via an anticlockwise D -ring Za?Ea photoflip followed by significant shifts at the coupling of ring A to the protein, a B -ring propionate partner swap from R317 to R287, changes in the C -ring propionate hydrogen-bonding network, breakage of the D272-R552 salt bridge accompanied by sheet-to-helix refolding of the tongue region stabilized by Y326-D272-S554 hydrogen bonding, and binding of the NTE to the hydrophobic side of ring A . We discuss phyA photoconversion, including the possible roles of mesoscopic phase transitions and protonation dynamics in the chromophore pocket. We also discuss possible associations between structural changes and translocation and signaling processes within the cell.

Dataset Information

The structure of a complete phytochrome sensory module in the Pr ground state.

Publications

The structure of a complete phytochrome sensory module in the Pr ground state.

Similar Datasets

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