Hacking the thylakoid proton motive force for improved photosynthesis: modulating ion flux rates that control proton motive force partitioning into Delta psi and Delta pH
File(s)
Accepted version
Author(s)
Davis, GA
Rutherford, AW
Kramer, DM
Type
Journal Article
Abstract
There is considerable interest in improving plant productivity by altering the dynamic responses of photosynthesis in tune with natural conditions. This is exemplified by the ‘energy-dependent' form of non-photochemical quenching (qE), the formation and decay of which can be considerably slower than natural light fluctuations, limiting photochemical yield. In addition, we recently reported that rapidly fluctuating light can produce field recombination-induced photodamage (FRIP), where large spikes in electric field across the thylakoid membrane (Δψ) induce photosystem II recombination reactions that produce damaging singlet oxygen (1O2). Both qE and FRIP are directly linked to the thylakoid proton motive force (pmf), and in particular, the slow kinetics of partitioning pmf into its ΔpH and Δψ components. Using a series of computational simulations, we explored the possibility of ‘hacking' pmf partitioning as a target for improving photosynthesis. Under a range of illumination conditions, increasing the rate of counter-ion fluxes across the thylakoid membrane should lead to more rapid dissipation of Δψ and formation of ΔpH. This would result in increased rates for the formation and decay of qE while resulting in a more rapid decline in the amplitudes of Δψ-spikes and decreasing 1O2 production. These results suggest that ion fluxes may be a viable target for plant breeding or engineering. However, these changes also induce transient, but substantial mismatches in the ATP : NADPH output ratio as well as in the osmotic balance between the lumen and stroma, either of which may explain why evolution has not already accelerated thylakoid ion fluxes. Overall, though the model is simplified, it recapitulates many of the responses seen in vivo, while spotlighting critical aspects of the complex interactions between pmf components and photosynthetic processes. By making the programme available, we hope to enable the community of photosynthesis researchers to further explore and test specific hypotheses.
Date Issued
2017-09-26
Date Acceptance
2017-05-31
Citation
Philosophical Transactions of the Royal Society of London: Biological Sciences, 2017, 372 (1730)
ISSN
0962-8436
Publisher
Royal Society, The
Journal / Book Title
Philosophical Transactions of the Royal Society of London: Biological Sciences
Volume
372
Issue
1730
Copyright Statement
© 2017 The Author(s)
Published by the Royal Society. All rights reserved.
Published by the Royal Society. All rights reserved.
Subjects
Science & Technology
Life Sciences & Biomedicine
Biology
Life Sciences & Biomedicine - Other Topics
photosynthesis
proton motive force
bioenergetics
ATP synthase
non-photochemical quenching
photoinhibition
K+/H+ ANTIPORTER KEA3
PHOTOSYSTEM-II
FLUCTUATING LIGHT
CHARGE RECOMBINATION
PLANT PHOTOSYNTHESIS
FLAVODIIRON PROTEINS
ELECTRON-TRANSFER
REACTION CENTERS
WATER OXIDATION
ATP SYNTHESIS
Publication Status
Published
Article Number
20160381