The Chloroplast Tat Pathway Utilizes the Transmembrane Electric Potential as an Energy Source

doi:https://doi.org/10.1529/biophysj.106.098731

Title: The Chloroplast Tat Pathway Utilizes the Transmembrane Electric Potential as an Energy Source

Abstract

Here, the thylakoid membrane, located inside the chloroplast, requires proteins transported across it for plastid biogenesis and functional photosynthetic electron transport. The chloroplast Tat translocator found on thylakoids transports proteins from the plastid stroma to the thylakoid lumen. Previous studies have shown that the chloroplast Tat pathway is independent of NTP hydrolysis as an energy source and instead depends on the thylakoid transmembrane proton gradient to power protein translocation. Because of its localization on the same membrane as the proton motive force-dependent F ₀F ₁ ATPase, we believed that the chloroplast Tat pathway also made use of the thylakoid electric potential for transporting substrates. By adjusting the rate of photosynthetic proton pumping and by utilizing ionophores, we show that the chloroplast Tat pathway can also utilize the transmembrane electric potential for protein transport. Our findings indicate that the chloroplast Tat pathway is likely dependent on the total protonmotive force (PMF) as an energy source. As a protonmotive-dependent device, certain predictions can be made about structural features expected to be found in the Tat translocon, specifically, the presence of a proton well, a device in the membrane that converts electrical potential into chemical potential.

Authors:

Braun, Nikolai A. ^[1]; Davis, Andrew W. ^[1]; Theg, Steven M. ^[1]

Univ. of California, Davis, CA (United States). Dept. of Plant Biology

Publication Date:: 2009-01-06

Research Org.:: Univ. of California, Davis, CA (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Chemical Sciences, Geosciences & Biosciences Division

OSTI Identifier:: 1490449

Grant/Contract Number:: FG02-03ER15405

Resource Type:: Journal Article: Accepted Manuscript

Journal Name:: Biophysical Journal

Additional Journal Information:: Journal Volume: 93; Journal Issue: 6; Journal ID: ISSN 0006-3495

Publisher:: Elsevier

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES

Citation Formats


                    Braun, Nikolai A., Davis, Andrew W., and Theg, Steven M. The Chloroplast Tat Pathway Utilizes the Transmembrane Electric Potential as an Energy Source.  United States: N. p., 2009. 
        Web.  doi:10.1529/biophysj.106.098731.

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                    Braun, Nikolai A., Davis, Andrew W., & Theg, Steven M. The Chloroplast Tat Pathway Utilizes the Transmembrane Electric Potential as an Energy Source.  United States.  https://doi.org/10.1529/biophysj.106.098731

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                    Braun, Nikolai A., Davis, Andrew W., and Theg, Steven M. Tue .  
        "The Chloroplast Tat Pathway Utilizes the Transmembrane Electric Potential as an Energy Source".  United States.  https://doi.org/10.1529/biophysj.106.098731.  https://www.osti.gov/servlets/purl/1490449.

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@article{osti_1490449,

  title        = {The Chloroplast Tat Pathway Utilizes the Transmembrane Electric Potential as an Energy Source},

  author       = {Braun, Nikolai A. and Davis, Andrew W. and Theg, Steven M.},

  abstractNote = {Here, the thylakoid membrane, located inside the chloroplast, requires proteins transported across it for plastid biogenesis and functional photosynthetic electron transport. The chloroplast Tat translocator found on thylakoids transports proteins from the plastid stroma to the thylakoid lumen. Previous studies have shown that the chloroplast Tat pathway is independent of NTP hydrolysis as an energy source and instead depends on the thylakoid transmembrane proton gradient to power protein translocation. Because of its localization on the same membrane as the proton motive force-dependent F0F1 ATPase, we believed that the chloroplast Tat pathway also made use of the thylakoid electric potential for transporting substrates. By adjusting the rate of photosynthetic proton pumping and by utilizing ionophores, we show that the chloroplast Tat pathway can also utilize the transmembrane electric potential for protein transport. Our findings indicate that the chloroplast Tat pathway is likely dependent on the total protonmotive force (PMF) as an energy source. As a protonmotive-dependent device, certain predictions can be made about structural features expected to be found in the Tat translocon, specifically, the presence of a proton well, a device in the membrane that converts electrical potential into chemical potential.},

  doi          = {10.1529/biophysj.106.098731},

  url          = {https://www.osti.gov/biblio/1490449},
  journal      = {Biophysical Journal},

  issn         = {0006-3495},

  number       = 6,

  volume       = 93,

  place        = {United States},

  year         = {2009},

  month        = {1}

}

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Journal Article:

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Accepted Manuscript (DOE)

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https://doi.org/10.1529/biophysj.106.098731

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Cited by: 40 works

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Figures / Tables:

Figure 1: Valinomycin decreases the rate of cpTat transport at low values of ΔpH. ( A) The import data of four ionophore treatments replicated nine times are shown, as well as triplicates of 10% substrate loading standards used for quantification purposes interspersed with a nonradioactive molecular weight marker ( emptymore » lanes). The average percentage transport of each treatment as well as the standard errors and t-tests are presented graphically ( B). The two pairs of columns labeled Control and Nigericin show the percentage transport of iOE17 Tat substrate under highlight conditions in the absence and presence of 300 nM of nigericin. Light shaded bars are untreated reactions, and solid bars are reactions that contain 1 μM valinomycin.

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Works referencing / citing this record:

Twin-arginine-dependent translocation of folded proteins
journal, April 2012

Fröbel, Julia; Rose, Patrick; Müller, Matthias
Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 367, Issue 1592
https://doi.org/10.1098/rstb.2011.0202

Twin-arginine-dependent translocation of folded proteins
journal, April 2012

Fröbel, Julia; Rose, Patrick; Müller, Matthias
Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 367, Issue 1592
https://doi.org/10.1098/rstb.2011.0202

Transport of Folded Proteins by the Tat System
journal, August 2019

Frain, Kelly M.; Robinson, Colin; van Dijl, Jan Maarten
The Protein Journal, Vol. 38, Issue 4
https://doi.org/10.1007/s10930-019-09859-y

Routing of thylakoid lumen proteins by the chloroplast twin arginine transport pathway
journal, August 2018

New, Christopher Paul; Ma, Qianqian; Dabney-Smith, Carole
Photosynthesis Research, Vol. 138, Issue 3
https://doi.org/10.1007/s11120-018-0567-z

The twin-arginine transport system: moving folded proteins across membranes
journal, October 2007

Sargent, F.
Biochemical Society Transactions, Vol. 35, Issue 5
https://doi.org/10.1042/bst0350835

The Chloroplast Tat Pathway Transports Substrates in the Dark
journal, January 2008

Braun, Nikolai A.; Theg, Steven M.
Journal of Biological Chemistry, Vol. 283, Issue 14
https://doi.org/10.1074/jbc.m708948200

The Tat protein transport system: intriguing questions and conundrums
journal, May 2018

Hamsanathan, Shruthi; Musser, Siegfried M.
FEMS Microbiology Letters, Vol. 365, Issue 12
https://doi.org/10.1093/femsle/fny123

Figures / Tables found in this record:

Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.

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Title: The Chloroplast Tat Pathway Utilizes the Transmembrane Electric Potential as an Energy Source

Abstract

Citation Formats

Figures / Tables:

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