Genetic characterization of a flap1 null mutation in Arabidopsis npq4 and pgr5 plants suggests that the regulatory role of FLAP1 involves the control of proton homeostasis in chloroplasts

Abstract

Precise control of the proton concentration gradient across thylakoid membranes (ΔpH) is essential for photosynthesis and its regulation because the gradient contributes to the generation of the proton motive force used for ATP synthesis and also for the fast and reversible induction of non-photochemical quenching (NPQ) to avoid photoinhibition and photodamage. However, the regulatory mechanism(s) controlling ΔpH in response to fluctuating light has not been fully elucidated. We previously described a new NPQ-regulatory chloroplastic protein, Fluctuating-Light-Acclimation Protein1 (FLAP1), which is important for plant growth and modulation of ΔpH under fluctuating light conditions. For this report, we further characterized FLAP1 activity by individually crossing an Arabidopsis flap1 mutant with npq4 and pgr5 plants; npq4 is defective in PsbS-dependent NPQ, and pgr5 is defective in induction of steady-state proton motive force (pmf) and energy-dependent quenching (qE). Both npq4 and npq4 flap1 exhibited similar NPQ kinetics and other photosynthetic parameters under constant or fluctuating actinic light. Conversely, pgr5 flap1 had recovered NPQ, photosystem II quantum yield and growth under fluctuating light, each of which was impaired in pgr5. Together with other data, we propose that FLAP1 activity controls proton homeostasis under steady-state photosynthesis to manipulate luminal acidification levels appropriately to balance photoprotection and photochemical processes.

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Acknowledgements

We thank Professor Toshiharu Shikanai (Kyoto University, Japan) and Professor Krishna K. Niyogi (University of California, Berkeley, USA) for providing the pgr5 and npq4 mutant seeds used in this study.

Funding

This study was supported by a Grant-in-Aid for Scientific Research, KAKENHI (Grant Number 17H05719) to SM.

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Correspondence to Shinji Masuda.

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Trinh, M.D.L., Sato, R. & Masuda, S. Genetic characterization of a flap1 null mutation in Arabidopsis npq4 and pgr5 plants suggests that the regulatory role of FLAP1 involves the control of proton homeostasis in chloroplasts. Photosynth Res 139, 413–424 (2019). https://doi.org/10.1007/s11120-018-0575-z

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Keywords

  • FLAP1
  • Fluctuating light
  • Luminal acidification
  • Non-photochemical quenching
  • PGR5
  • Photosynthesis