Skip to main content
Log in

Relative contributions of PGR5- and NDH-dependent photosystem I cyclic electron flow in the generation of a proton gradient in Arabidopsis chloroplasts

  • Short Communication
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Abbreviations

CEF:

Cyclic electron flow

ΔpH:

Proton concentration gradient across the inside and outside of the thylakoid membrane

Δψ:

Membrane potential

LEF:

Linear electron flow

NDH:

NAD(P)H dehydrogenase

NPQ:

Non-photochemical quenching

PGR5:

Proton gradient regulation 5

PMF:

Proton motive force

PSI:

Photosystem I

PSII:

Photosystem II

9-AA:

9-Aminoacridine

References

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Blankenship RE (2002) Molecular mechanisms of photosynthesis. Blackwell Science Ltd, Hoboken

    Book  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Heber U, Santarius KA (1970) Direct and indirect transfer of ATP and ADP across the chloroplast envelope. Z Naturforsch B 25:718–728

    CAS  PubMed  Google Scholar 

  • Herdean A, Teardo E, Nilsson AK et al (2016) A voltage-dependent chloride channel fine-tunes photosynthesis in plants. Nat Commun 7:11654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Kotera E, Tasaka M, Shikanai T (2005) A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature 433:326–330

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li XP, Björkman O, Shih C et al (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ruban AV (2016) Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage. Plant Physiol 170:1903–1916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schuldiner S, Rottenberg H, Avron M (1972) Determination of DpH in chloroplasts. Eur J Biochem 25:64–70

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Shikanai T (2007) Cyclic electron transport around photosystem I: genetic approaches. Annu Rev Plant Biol 58:199–217

    Article  CAS  PubMed  Google Scholar 

  • Shikanai T (2016) Regulatory network of proton motive force: contribution of cyclic electron transport around photosystem I. Photosynth Res 129:253–260

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto H, Takahashi S, Badger M, Shikanai T (2016) Artificial remodeling of alternative electron flow by flavodiiron proteins in Arabidopsis. Nat Plants 2:16012

    Article  CAS  PubMed  Google Scholar 

  • Yamori W (2016) Photosynthetic response to fluctuating environments and photoprotective strategies under abiotic stress. J Plant Res 129:379–395

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shinji Masuda.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 74 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-017-2761-1

Keywords

Navigation