Respective contributions of PGR5- and NDH-dependent cyclic electron flows around photosystem I for generating the proton gradient across the thylakoid membrane are ~30 and ~5%.
The proton concentration gradient across the thylakoid membrane (ΔpH) produced by photosynthetic electron transport is the driving force of ATP synthesis and non-photochemical quenching. Two types of electron transfer contribute to ΔpH formation: linear electron flow (LEF) and cyclic electron flow (CEF, divided into PGR5- and NDH-dependent pathways). However, the respective contributions of LEF and CEF to ΔpH formation are largely unknown. We employed fluorescence quenching analysis with the pH indicator 9-aminoacridine to directly monitor ΔpH formation in isolated chloroplasts of Arabidopsis mutants lacking PGR5- and/or NDH-dependent CEF. The results indicate that ΔpH formation is mostly due to LEF, with the contributions of PGR5- and NDH-dependent CEF estimated as only ~30 and ~5%, respectively.
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Cyclic electron flow
Proton concentration gradient across the inside and outside of the thylakoid membrane
Linear electron flow
Proton gradient regulation 5
Proton motive force
Armbruster U, Leonelli L, Correa Galvis V et al (2016) Regulation and levels of the thylakoid K+/H+ antiporter KEA3 shape the dynamic response of photosynthesis in fluctuating light. Plant Cell Physiol 57:1557–1567
Blankenship RE (2002) Molecular mechanisms of photosynthesis. Blackwell Science Ltd, Hoboken
Carraretto L, Formentin E, Teardo E et al (2013) A thylakoid-located two-pore K+ channel controls photosynthetic light utilization in Plants. Science 342:114–118
Dana S, Herdean A, Lundin B, Spetea C (2016) Retracted: each of the chloroplast potassium efflux antiporters affects photosynthesis and growth of fully developed Arabidopsis rosettes under short-day photoperiod. Physiol Plant 158:483–491
Heber U, Santarius KA (1970) Direct and indirect transfer of ATP and ADP across the chloroplast envelope. Z Naturforsch B 25:718–728
Herdean A, Teardo E, Nilsson AK et al (2016) A voltage-dependent chloride channel fine-tunes photosynthesis in plants. Nat Commun 7:11654
Johnson MP, Ruban AV (2011) Restoration of rapidly reversible photoprotective energy dissipation in the absence of PsbS protein by enhanced ΔpH. J Biol Chem 286:19973–19981
Johnson MP, Zia A, Ruban AV (2012) Elevated ΔpH restores rapidly reversible photoprotective energy dissipation in Arabidopsis chloroplasts deficient in lutein and xanthophyll cycle activity. Planta 235:193–204
Kalituho L, Beran KC, Jahns P (2007) The transiently generated nonphotochemical quenching of excitation energy in Arabidopsis leaves is modulated by zeaxanthin. Plant Physiol 143:1861–1870
Kaňa R, Kotabová E, Kopečná J et al (2016) Violaxanthin inhibits nonphotochemical quenching in light-harvesting antenna of Chromera velia. FEBS Lett 590:1076–1085
Kaushik D, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:53
Kotera E, Tasaka M, Shikanai T (2005) A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature 433:326–330
Kunz H-H, Gierth M, Herdean A et al (2014) Plastidial transporters KEA1, -2, and -3 are essential for chloroplast osmoregulation, integrity, and pH regulation in Arabidopsis. Proc Natl Acad Sci 111:7480–7485
Li XP, Björkman O, Shih C et al (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395
Li XP, Gilmore AM, Caffarri S et al (2004) Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J Biol Chem 279:22866–22874
Munekage Y, Hojo M, Meurer J et al (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110:361–371
Niyogi KK, Grossman AR, Bjorkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10:1121–1134
Okegawa Y, Long TA, Iwano M et al (2007) A balanced PGR5 level is required for chloroplast development and optimum operation of cyclic electron transport around photosystem I. Plant Cell Physiol 48:1462–1471
Ruban AV (2016) Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage. Plant Physiol 170:1903–1916
Schuldiner S, Rottenberg H, Avron M (1972) Determination of DpH in chloroplasts. Eur J Biochem 25:64–70
Seigneurin-Berny D, Salvi D, Joyard J et al (2008) Purification of intact chloroplasts from Arabidopsis and spinach leaves by isopycnic centrifugation. Curr Protoc Cell Biol 40:3.30.1–3.30.14
Shikanai T (2007) Cyclic electron transport around photosystem I: genetic approaches. Annu Rev Plant Biol 58:199–217
Shikanai T (2016) Regulatory network of proton motive force: contribution of cyclic electron transport around photosystem I. Photosynth Res 129:253–260
Shikanai T, Yamamoto H (2017) Contribution of cyclic and pseudo-cyclic electron transport to the formation of proton motive force in chloroplasts. Mol Plant 10:20–29
Song C-P, Guo Y, Qiu Q et al (2004) A probable Na+(K+)/H+ exchanger on the chloroplast envelope functions in pH homeostasis and chloroplast development in Arabidopsis thaliana. Proc Natl Acad Sci USA 101:10211–10216
Wang C, Yamamoto H, Shikanai T (2015) Role of cyclic electron transport around photosystem I in regulating proton motive force. Biochim Biophys Acta 1847:931–938
Wang C, Yamamoto H, Narumiya F et al (2017) Fine-tuned regulation of the K+/H+ antiporter KEA3 is required to optimize photosynthesis during induction. Plant J 89:540–553
Yamamoto H, Takahashi S, Badger M, Shikanai T (2016) Artificial remodeling of alternative electron flow by flavodiiron proteins in Arabidopsis. Nat Plants 2:16012
Yamori W (2016) Photosynthetic response to fluctuating environments and photoprotective strategies under abiotic stress. J Plant Res 129:379–395
We thank Professor Toshiharu Shikanai at Kyoto University for providing mutant seeds. This work was supported by a Grant-in-Aid for Scientific Research, KAKENHI (17H05719, 16K14694 and 16H03280) to SM.
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Kawashima, R., Sato, R., Harada, K. et al. Relative contributions of PGR5- and NDH-dependent photosystem I cyclic electron flow in the generation of a proton gradient in Arabidopsis chloroplasts. Planta 246, 1045–1050 (2017). https://doi.org/10.1007/s00425-017-2761-1
- Cyclic electron transfer
- Non-photochemical quenching