ATP compartmentation in plastids and cytosol of Arabidopsis thaliana revealed by fluorescent protein sensing

Voon, Chia Pao; Guan, Xiaoqian; Sun, Yuzhe; Sahu, Abira; Chan, May Ngor; Gardeström, Per; Wagner, Stephan; Fuchs, Philippe; Nietzel, Thomas; Versaw, Wayne K.; Schwarzländer, Markus; Lim, Boon Leong

doi:10.1073/pnas.1711497115

Title: ATP compartmentation in plastids and cytosol of Arabidopsis thaliana revealed by fluorescent protein sensing

Journal Article · 22 October 2018 · Proceedings of the National Academy of Sciences of the United States of America

DOI: https://doi.org/10.1073/pnas.1711497115 · OSTI ID:1612065

Voon, Chia Pao ^[1]; Guan, Xiaoqian ^[2]; Sun, Yuzhe ^[2]; Sahu, Abira ^[3]; Chan, May Ngor ^[2]; Gardeström, Per ^[4]; Wagner, Stephan ^[5]; Fuchs, Philippe ^[5]; Nietzel, Thomas ^[5]; Versaw, Wayne K. ^[3];

^[5];

^[6]

Univ. of Hong Kong (China); DOE/OSTI
Univ. of Hong Kong (China)
Texas A & M Univ., College Station, TX (United States)
Umea Univ. (Sweden)
Rheinische Friedrich-Wilhelms-Univ., Bonn (Germany); Westfalische Wilhelms-Univ., Munster (Germany)
Univ. of Hong Kong (China); Chinese Univ. of Hong Kong (China)

Matching ATP:NADPH provision and consumption in the chloroplast is a prerequisite for efficient photosynthesis. In terms of ATP:NADPH ratio, the amount of ATP generated from the linear electron flow does not meet the demand of the Calvin–Benson–Bassham (CBB) cycle. Several different mechanisms to increase ATP availability have evolved, including cyclic electron flow in higher plants and the direct import of mitochondrial-derived ATP in diatoms. By imaging a fluorescent ATP sensor protein expressed in living Arabidopsis thaliana seedlings, we found that MgATP^2- concentrations were lower in the stroma of mature chloroplasts than in the cytosol, and exogenous ATP was able to enter chloroplasts isolated from 4- and 5-day-old seedlings, but not chloroplasts isolated from 10- or 20-day-old photosynthetic tissues. This observation is in line with the previous finding that the expression of chloroplast nucleotide transporters (NTTs) in Arabidopsis mesophyll is limited to very young seedlings. Employing a combination of photosynthetic and respiratory inhibitors with compartment-specific imaging of ATP, we corroborate the dependency of stromal ATP production on mitochondrial dissipation of photosynthetic reductant. Our data suggest that, during illumination, the provision and consumption of ATP:NADPH in chloroplasts can be balanced by exporting excess reductants rather than importing ATP from the cytosol.

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Research Organization:: Texas A & M Univ., College Station, TX (United States)

Sponsoring Organization:: Deutsche Forschungsgemeinschaft; Hong Kong Research Grants Council Area of Excellence Scheme; Hong Kong Special Administrative Region; Seed Funding Program for Basic Research; USDOE Office of Science (SC)

Grant/Contract Number:: SC0014037

OSTI ID:: 1612065

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 45 Vol. 115; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

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Imaging Cellular Inorganic Phosphate in Caenorhabditis elegans Using a Genetically Encoded FRET-Based Biosensor Banerjee, Swayoma; Versaw, Wayne K.; Garcia, L. Rene PLOS ONE, Vol. 10, Issue 10 https://doi.org/10.1371/journal.pone.0141128	journal	October 2015
A simple way to identify non-viable cells within living plant tissue using confocal microscopy Truernit, Elisabeth; Haseloff, Jim ETH Zurich https://doi.org/10.3929/ethz-b-000085314	text	January 2008
ATP sensing in living plant cells reveals tissue gradients and stress dynamics of energy physiology De Col, Valentina; Fuchs, Philippe; Nietzel, Thomas eLife, Vol. 6 https://doi.org/10.7554/eLife.26770	journal	July 2017

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59 BASIC BIOLOGICAL SCIENCES
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chloroplasts
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mitochondria
photosynthesis

Title: ATP compartmentation in plastids and cytosol of Arabidopsis thaliana revealed by fluorescent protein sensing

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