Limitations to photosynthesis by proton motive force-induced photosystem II photodamage
Geoffry A Davis,
Atsuko Kanazawa,
Mark Aurel Schöttler,
Kaori Kohzuma,
John E Froehlich,
A William Rutherford,
Mio Satoh-Cruz,
Deepika Minhas,
Stefanie Tietz,
Amit Dhingra,
David M Kramer
Affiliations
Geoffry A Davis
Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, United States; Graduate Program of Cell and Molecular Biology, Michigan State University, East Lansing, United States
Atsuko Kanazawa
Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, United States; Department of Chemistry, Michigan State University, East Lansing, United States
Mark Aurel Schöttler
Max-Planck-Institut für Molekulare Pflanzenphysiologie, Potsdam-Golm, Germany
Kaori Kohzuma
Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, United States
John E Froehlich
Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, United States
A William Rutherford
Department of Life Sciences, Imperial College London, London, United Kingdom
Mio Satoh-Cruz
Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, United States
Deepika Minhas
Department of Horticulture, Washington State University, Pullman, United States
Stefanie Tietz
Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, United States
Amit Dhingra
Department of Horticulture, Washington State University, Pullman, United States
Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, United States; Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, United States
The thylakoid proton motive force (pmf) generated during photosynthesis is the essential driving force for ATP production; it is also a central regulator of light capture and electron transfer. We investigated the effects of elevated pmf on photosynthesis in a library of Arabidopsis thaliana mutants with altered rates of thylakoid lumen proton efflux, leading to a range of steady-state pmf extents. We observed the expected pmf-dependent alterations in photosynthetic regulation, but also strong effects on the rate of photosystem II (PSII) photodamage. Detailed analyses indicate this effect is related to an elevated electric field (Δψ) component of the pmf, rather than lumen acidification, which in vivo increased PSII charge recombination rates, producing singlet oxygen and subsequent photodamage. The effects are seen even in wild type plants, especially under fluctuating illumination, suggesting that Δψ-induced photodamage represents a previously unrecognized limiting factor for plant productivity under dynamic environmental conditions seen in the field.