Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Matters Arising
  • Published:

Reply to: Is the debate over grana stacking formation finally solved?

Nature Plants volume 7, pages 279–281 (2021)Cite this article

Subjects

The Original Article was published on 11 March 2021

replying to M. M. Gudarzi et al. Nature Plants https://doi.org/10.1038/s41477-021-00880-7 (2021)

In plants, the photosynthetic pigment–protein complexes catalysing energy conversion are harboured in the thylakoid membrane system of chloroplasts. Recent breakthroughs in electron tomography1,2,3 reveal the sophisticated architecture of this unique membrane system with stacked grana as a structural hallmark. A long-standing question has been whether the combination of physicochemical forces alone can explain the strict stacking of grana with an intermembrane separation of 3–4 nm. In our 2017 Nature Plants paper4, we argued that the balance between attractive van der Waals (vdW) forces (FvdW) and repulsive electrostatic (Fel) and hydrostructural (Fhydro) forces could explain grana stacking, in contrast with previous reports. Our finding was challenged in the report by Gudarzi et al.5 This reply addresses this critique.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Net repulsive force between granal thylakoid membranes across the stromal gap.

References

  1. Bussi, Y. et al. Fundamental helical geometry consolidates the plant photosynthetic membrane. Proc. Natl Acad. Sci. USA 116, 22366–22375 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Daum, B., Nicastro, D., Il, J. A., McIntosh, J. R. & Kühlbrandt, W. Arrangement of Photosystem II and ATP synthase in chloroplast membranes of spinach and pea. Plant Cell 22, 1299–1312 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Austin, J. R. & Staehelin, L. A. Three-dimensional architecture of grana and stroma thylakoids of higher plants as determined by electron tomography. Plant Physiol. 155, 1601–1611 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Puthiyaveetil, S., van Oort, B. & Kirchhoff, H. Surface charge dynamics in photosynthetic membranes and the structural consequences. Nat. Plants 3, 17020 (2017).

    Article  CAS  PubMed  Google Scholar 

  5. Gudarzi, M. M., Aboutalebi, S. H. & Satalov, A. Is the debate over grana stacking formation finally solved? Nat. Plants https://doi.org/10.1038/s41477-021-00880-7 (2021).

  6. Sculley, M. J., Duniec, J. T., Thorne, S. W., Chow, W. S. & Boardman, N. K. The stacking of chloroplast thylakoids: quantitative analysis of the balance of forces between thylakoid membranes of chloroplasts, and the role of divalent cations. Arch. Biochem. Biophys. 201, 339–346 (1980).

    Article  CAS  PubMed  Google Scholar 

  7. Renger, T. et al. Thermally activated superradiance and intersystem crossing in the water-soluble chlorophyll binding protein. J. Phys. Chem. B 113, 9948–9957 (2009).

    Article  CAS  PubMed  Google Scholar 

  8. Müh, F. & Zouni, A. Extinction coefficients and critical solubilisation concentrations of photosystems I and II from Thermosynechococcus elongatus. Biochim. Biophys. Acta 1708, 219–228 (2005).

    Article  PubMed  Google Scholar 

  9. Renger, T. & Müh, F. Understanding photosynthetic light-harvesting: a bottom up theoretical approach. Phys. Chem. Chem. Phys. 15, 3348–3371 (2013).

    Article  CAS  PubMed  Google Scholar 

  10. Su, X. et al. Structure and assembly mechanism of plant C2S2M2-type PSII–LHCII supercomplex. Science 357, 815–820 (2017).

    Article  CAS  PubMed  Google Scholar 

  11. Kirchhoff, H. et al. Dynamic control of protein diffusion within the granal thylakoid lumen. Proc. Natl Acad. Sci. USA 108, 20248–20253 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by grants to H.K. from the National Science Foundation (NSF-MCB-1616982 and 1953570), the US Department of Energy (DE-SC 0017160) and the US Department of Agriculture (ARC grant WNP00775), to S.P. from DOE (DE-SC0020639) and USDA-NIFA (Hatch: 1013608) as well as to F.M. by the Austrian Science Fund (FWF) in conjunction with the district of Upper Austria (P 33154-B and P 33155-NBL) and the Linz Institute of Technology (LIT-2019-8-SEE-120). B.v.O. was supported by the Novo Nordisk Foundation project ‘Harnessing the Energy of the Sun for Biomass Conversion’ (NNF16OC0021832).

Author information

Author notes

  1. Bart van Oort

    Present address: Physical Chemistry and Soft Matter, Wageningen University, Wageningen, the Netherlands

Authors and Affiliations

  1. Institute for Theoretical Physics, Department of Theoretical Biophysics, Johannes Kepler University Linz, Linz, Austria

    Frank Müh

  2. Biophysics of Photosynthesis, Department of Physics and Astronomy, Faculty of Science, Vrije Universiteit Amsterdam, Amsterdam, the Netherlands

    Bart van Oort

  3. Department of Biochemistry and Center for Plant Biology, Purdue University, West Lafayette, IN, USA

    Sujith Puthiyaveetil

  4. Institute of Biological Chemistry, Washington State University, Pullman, WA, USA

    Helmut Kirchhoff

Authors
  1. Frank Müh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bart van Oort
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sujith Puthiyaveetil
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Helmut Kirchhoff
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

F.M. and H.K. performed calculations. F.M., B.v.O., S.P. and H.K. designed the study and wrote the manuscript.

Corresponding authors

Correspondence to Frank Müh or Helmut Kirchhoff.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Tables 1 and 2.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Müh, F., van Oort, B., Puthiyaveetil, S. et al. Reply to: Is the debate over grana stacking formation finally solved?. Nat. Plants 7, 279–281 (2021). https://doi.org/10.1038/s41477-021-00881-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41477-021-00881-6

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing