Structure‐based control of the rate limitation of photosynthetic electron transport

Ness, Jillian; Naurin, Sejuti; Effinger, Katherine; Stadnytskyi, Valentyn; Ibrahim, Iskander M.; Puthiyaveetil, Sujith; Cramer, William A.

doi:10.1002/1873-3468.13484

Title: Structure‐based control of the rate limitation of photosynthetic electron transport

Abstract

The 2.5 Å structure of the cytochrome (cyt) b ₆ f complex provides a basis for control of the rate‐limiting electron transfer step of oxygenic photosynthesis associated with the plastoquinol/quinone exchange pathway. Here, a structural change was made at a site containing two proline residues which border the intra‐cyt pathway for plastoquinol/quinone exchange. The proline side chains confer a larger aperture for passage of plastoquinol/quinone. Change of these prolines to alanine in the cyanobacterium Synechococcus sp. PCC 7002 results in attenuation of this rate‐limiting step, observed by a two‐fold reduction in the rate of cell growth, O ₂ evolution, and plastoquinol‐mediated reduction of cyt f . This study demonstrates modification by site‐directed mutagenesis of photosynthetic energy transduction based on rational application of information in the atomic structure.

Authors:

Ness, Jillian ^[1]; Naurin, Sejuti ^[1]; Effinger, Katherine ^[2]; Stadnytskyi, Valentyn ^[3];

^[2]; Puthiyaveetil, Sujith ^[2]; Cramer, William A. ^[1]

Department of Biological Sciences Purdue University West Lafayette IN USA
Department of Biochemistry Purdue University West Lafayette IN USA
Laboratory of Chemical Physics NIDDK/NIH Bethesda MD USA

Publication Date:: 2019-07-08

Sponsoring Org.:: USDOE

OSTI Identifier:: 1542522

Grant/Contract Number:: DE‐SC0018238

Resource Type:: Publisher's Accepted Manuscript

Journal Name:: FEBS Letters

Additional Journal Information:: Journal Name: FEBS Letters Journal Volume: 593 Journal Issue: 16; Journal ID: ISSN 0014-5793

Publisher:: Wiley Blackwell (John Wiley & Sons)

Country of Publication:: Netherlands

Language:: English

Citation Formats


                    Ness, Jillian, Naurin, Sejuti, Effinger, Katherine, Stadnytskyi, Valentyn, Ibrahim, Iskander M., Puthiyaveetil, Sujith, and Cramer, William A.. Structure‐based control of the rate limitation of photosynthetic electron transport.  Netherlands: N. p., 2019. 
Web.  doi:10.1002/1873-3468.13484.

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                    Ness, Jillian, Naurin, Sejuti, Effinger, Katherine, Stadnytskyi, Valentyn, Ibrahim, Iskander M., Puthiyaveetil, Sujith, & Cramer, William A.. Structure‐based control of the rate limitation of photosynthetic electron transport.  Netherlands.  https://doi.org/10.1002/1873-3468.13484

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                    Ness, Jillian, Naurin, Sejuti, Effinger, Katherine, Stadnytskyi, Valentyn, Ibrahim, Iskander M., Puthiyaveetil, Sujith, and Cramer, William A.. Mon .  
"Structure‐based control of the rate limitation of photosynthetic electron transport".  Netherlands.  https://doi.org/10.1002/1873-3468.13484.

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@article{osti_1542522,

  title        = {Structure‐based control of the rate limitation of photosynthetic electron transport},

  author       = {Ness, Jillian and Naurin, Sejuti and Effinger, Katherine and Stadnytskyi, Valentyn and Ibrahim, Iskander M. and Puthiyaveetil, Sujith and Cramer, William A.},

  abstractNote = {The 2.5 Å structure of the cytochrome (cyt) b 6 f complex provides a basis for control of the rate‐limiting electron transfer step of oxygenic photosynthesis associated with the plastoquinol/quinone exchange pathway. Here, a structural change was made at a site containing two proline residues which border the intra‐cyt pathway for plastoquinol/quinone exchange. The proline side chains confer a larger aperture for passage of plastoquinol/quinone. Change of these prolines to alanine in the cyanobacterium Synechococcus sp. PCC 7002 results in attenuation of this rate‐limiting step, observed by a two‐fold reduction in the rate of cell growth, O 2 evolution, and plastoquinol‐mediated reduction of cyt f . This study demonstrates modification by site‐directed mutagenesis of photosynthetic energy transduction based on rational application of information in the atomic structure.},

  doi          = {10.1002/1873-3468.13484},

  journal      = {FEBS Letters},

  number       = 16,

  volume       = 593,

  place        = {Netherlands},

  year         = {2019},

  month        = {7}

}

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Title: Structure‐based control of the rate limitation of photosynthetic electron transport

Abstract

Citation Formats

An Algorithm for Least-Squares Estimation of Nonlinear Parameters journal, June 1963

Plastoquinone as a common link between photosynthesis and respiration in a blue-green alga journal, January 1980

Light-saturated photosynthesis — Limitation by electron transport or carbon fixation? journal, May 1987

Quantifying impacts of enhancing photosynthesis on crop yield journal, April 2019

On rate limitations of electron transfer in the photosynthetic cytochrome b6f complex journal, January 2012

Milestones in chloroplast genetic engineering: an environmentally friendly era in biotechnology journal, February 2002

Role of Domain Swapping in the Hetero-Oligomeric Cytochrome b 6 f Lipoprotein Complex journal, May 2015

Internal Lipid Architecture of the Hetero-Oligomeric Cytochrome b6f Complex journal, July 2014

Quantitative Treatment of the Function of Plastoquinone in Photosynthesis journal, December 1969

Traffic within the Cytochrome b6f Lipoprotein Complex: Gating of the Quinone Portal journal, October 2014

Structure of the Cytochrome b6f Complex of Oxygenic Photosynthesis: Tuning the Cavity journal, November 2003

Reconstruction of the chloroplast noncyclic electron transport pathway from water to NADP with three integral protein complexes journal, September 1982

Expression of the Escherichia coli lacZ gene on a plasmid vector in a cyanobacterium journal, November 1985

Identification of the Basic Residues of Cytochrome f Responsible for Electrostatic Docking Interactions with Plastocyanin in Vitro: Relevance to the Electron Transfer Reaction in Vivo † journal, October 1998

Structure of the Cytochrome b6f Complex: Quinone Analogue Inhibitors as Ligands of Heme cn journal, June 2007

Pathways for proton release during ubihydroquinone oxidation by the bc1 complex journal, August 1999

Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega journal, January 2011

Function-Directed Mutagenesis of the Cytochrome b 6 f Complex in Chlamydomonas reinhardtii : Involvement of the cd Loop of Cytochrome b 6 in Quinol Binding to the Q o Site † journal, March 1997

On the question of interheme electron transfer in the chloroplast cytochrome b6 in situ journal, November 1989

Improving Photosynthetic Efficiency for Greater Yield journal, June 2010

Functional Insensitivity of the Cytochrome b 6 f Complex to Structure Changes in the Hinge Region of the Rieske Iron-Sulfur Protein journal, April 2003

Crystal structure of chloroplast cytochrome freveals a novel cytochrome fold and unexpected heme ligation journal, February 1994

SOME NEW STRUCTURAL ASPECTS AND OLD CONTROVERSIES CONCERNING THE CYTOCHROME b 6 f COMPLEX OF OXYGENIC PHOTOSYNTHESIS journal, June 1996

Localization of electron transport inhibition in plastoquinone reactions journal, June 1982

Characterization and Crystallization of the Lumen Side Domain of the Chloroplast Rieske Iron-Sulfur Protein journal, December 1996

Transmembrane Traffic in the Cytochrome b 6 f Complex journal, June 2006

Photochemistry beyond the red limit in chlorophyll f–containing photosystems journal, June 2018

Localization of a site of energy coupling between plastoquinone and cytochrome f in the electron-transport chain of spinach chloroplasts journal, March 1972

Comparing Photosynthetic and Photovoltaic Efficiencies and Recognizing the Potential for Improvement journal, May 2011

Shifting hydrogen bonds may produce flexible transmembrane helices journal, May 2012

An atypical haem in the cytochrome b6f complex journal, November 2003

An Algorithm for Least-Squares Estimation of Nonlinear Parameters
journal, June 1963

Plastoquinone as a common link between photosynthesis and respiration in a blue-green alga
journal, January 1980

Light-saturated photosynthesis — Limitation by electron transport or carbon fixation?
journal, May 1987

Quantifying impacts of enhancing photosynthesis on crop yield
journal, April 2019

On rate limitations of electron transfer in the photosynthetic cytochrome b6f complex
journal, January 2012

Milestones in chloroplast genetic engineering: an environmentally friendly era in biotechnology
journal, February 2002

Role of Domain Swapping in the Hetero-Oligomeric Cytochrome b ₆ f Lipoprotein Complex
journal, May 2015

Internal Lipid Architecture of the Hetero-Oligomeric Cytochrome b6f Complex
journal, July 2014

Quantitative Treatment of the Function of Plastoquinone in Photosynthesis
journal, December 1969

Traffic within the Cytochrome b6f Lipoprotein Complex: Gating of the Quinone Portal
journal, October 2014

Structure of the Cytochrome b6f Complex of Oxygenic Photosynthesis: Tuning the Cavity
journal, November 2003

Reconstruction of the chloroplast noncyclic electron transport pathway from water to NADP with three integral protein complexes
journal, September 1982

Expression of the Escherichia coli lacZ gene on a plasmid vector in a cyanobacterium
journal, November 1985

Identification of the Basic Residues of Cytochrome f Responsible for Electrostatic Docking Interactions with Plastocyanin in Vitro: Relevance to the Electron Transfer Reaction in Vivo ^†
journal, October 1998

Structure of the Cytochrome b6f Complex: Quinone Analogue Inhibitors as Ligands of Heme cn
journal, June 2007

Pathways for proton release during ubihydroquinone oxidation by the bc1 complex
journal, August 1999

Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega
journal, January 2011

Function-Directed Mutagenesis of the Cytochrome b ₆ f Complex in Chlamydomonas reinhardtii : Involvement of the cd Loop of Cytochrome b ₆ in Quinol Binding to the Q _o Site ^†
journal, March 1997

On the question of interheme electron transfer in the chloroplast cytochrome b6 in situ
journal, November 1989

Improving Photosynthetic Efficiency for Greater Yield
journal, June 2010

Functional Insensitivity of the Cytochrome b ₆ f Complex to Structure Changes in the Hinge Region of the Rieske Iron-Sulfur Protein
journal, April 2003

Crystal structure of chloroplast cytochrome freveals a novel cytochrome fold and unexpected heme ligation
journal, February 1994

SOME NEW STRUCTURAL ASPECTS AND OLD CONTROVERSIES CONCERNING THE CYTOCHROME b ₆ f COMPLEX OF OXYGENIC PHOTOSYNTHESIS
journal, June 1996

Localization of electron transport inhibition in plastoquinone reactions
journal, June 1982

Characterization and Crystallization of the Lumen Side Domain of the Chloroplast Rieske Iron-Sulfur Protein
journal, December 1996

Transmembrane Traffic in the Cytochrome b ₆ f Complex
journal, June 2006

Photochemistry beyond the red limit in chlorophyll f–containing photosystems
journal, June 2018

Localization of a site of energy coupling between plastoquinone and cytochrome f in the electron-transport chain of spinach chloroplasts
journal, March 1972

Comparing Photosynthetic and Photovoltaic Efficiencies and Recognizing the Potential for Improvement
journal, May 2011

Shifting hydrogen bonds may produce flexible transmembrane helices
journal, May 2012

An atypical haem in the cytochrome b6f complex
journal, November 2003