The D-ring, not the A-ring, rotates in Synechococcus OS-B' phytochrome

Chen Song, Georgios Psakis, Jakub Kopycki, Christina Lang, Jörg Matysik, Jon Hughes

Research output: Contribution to journalArticle

21 Citations (Scopus)

Abstract

Phytochrome photoreceptors in plants and microorganisms switch photochromically between two states, controlling numerous important biological processes. Although this phototransformation is generally considered to involve rotation of ring D of the tetrapyrrole chromophore, Ulijasz etal. (Ulijasz, A. T., Cornilescu, G., Cornilescu, C. C, Zhang, J., Rivera, M., Markley, J. L., and Vierstra, R. D. (2010) Nature 463, 250-254) proposed that the A-ring rotates instead. Here, we apply magic angle spinning NMR to the two parent states following studies of the 23-kDa GAF (cGMP phosphodiesterase/adenylyl cyclase/FhlA) domain fragment of phytochrome from Synechococcus OS-B'. Major changes occur at the A-ring covalent linkage to the protein as well as at the protein residue contact of ring D. Conserved contacts associated with the A-ring nitrogen rule out an A-ring photoflip, whereas loss of contact of the D-ring nitrogen to the protein implies movement of ring D. Although none of the methine bridges showed a chemical shift change comparable with those characteristic of the D-ring photoflip in canonical phytochromes, denaturation experiments showed conclusively that the same occurs in Synechococcus OS-B' phytochrome upon photoconversion. The results are consistent with the D-ring being strongly tilted in both states and the C15=C16 double bond undergoing a Z/E isomerization upon light absorption. More subtle changes are associated with the A-ring linkage to the protein. Our findings thus disprove A-ring rotation and are discussed in relation to the position of the D-ring, photoisomerization, and photochromicity in the phytochrome family.

LanguageEnglish
Pages2552-2562
Number of pages11
JournalJournal of Biological Chemistry
Volume289
Issue number5
Early online date10 Dec 2013
DOIs
Publication statusPublished - 31 Jan 2014
Externally publishedYes

Fingerprint

Phytochrome B
Phytochrome
Synechococcus
Plant Photoreceptors
Proteins
Nitrogen
Tetrapyrroles
Biological Phenomena
Photoisomerization
Denaturation
Magic angle spinning
Phosphoric Diester Hydrolases
Chemical shift
Chromophores
Isomerization
Adenylyl Cyclases
Microorganisms
Light absorption
Switches
Nuclear magnetic resonance

Cite this

Song, Chen ; Psakis, Georgios ; Kopycki, Jakub ; Lang, Christina ; Matysik, Jörg ; Hughes, Jon. / The D-ring, not the A-ring, rotates in Synechococcus OS-B' phytochrome. In: Journal of Biological Chemistry. 2014 ; Vol. 289, No. 5. pp. 2552-2562.
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The D-ring, not the A-ring, rotates in Synechococcus OS-B' phytochrome. / Song, Chen; Psakis, Georgios; Kopycki, Jakub; Lang, Christina; Matysik, Jörg; Hughes, Jon.

In: Journal of Biological Chemistry, Vol. 289, No. 5, 31.01.2014, p. 2552-2562.

Research output: Contribution to journalArticle

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AU - Psakis, Georgios

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AU - Hughes, Jon

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AB - Phytochrome photoreceptors in plants and microorganisms switch photochromically between two states, controlling numerous important biological processes. Although this phototransformation is generally considered to involve rotation of ring D of the tetrapyrrole chromophore, Ulijasz etal. (Ulijasz, A. T., Cornilescu, G., Cornilescu, C. C, Zhang, J., Rivera, M., Markley, J. L., and Vierstra, R. D. (2010) Nature 463, 250-254) proposed that the A-ring rotates instead. Here, we apply magic angle spinning NMR to the two parent states following studies of the 23-kDa GAF (cGMP phosphodiesterase/adenylyl cyclase/FhlA) domain fragment of phytochrome from Synechococcus OS-B'. Major changes occur at the A-ring covalent linkage to the protein as well as at the protein residue contact of ring D. Conserved contacts associated with the A-ring nitrogen rule out an A-ring photoflip, whereas loss of contact of the D-ring nitrogen to the protein implies movement of ring D. Although none of the methine bridges showed a chemical shift change comparable with those characteristic of the D-ring photoflip in canonical phytochromes, denaturation experiments showed conclusively that the same occurs in Synechococcus OS-B' phytochrome upon photoconversion. The results are consistent with the D-ring being strongly tilted in both states and the C15=C16 double bond undergoing a Z/E isomerization upon light absorption. More subtle changes are associated with the A-ring linkage to the protein. Our findings thus disprove A-ring rotation and are discussed in relation to the position of the D-ring, photoisomerization, and photochromicity in the phytochrome family.

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