Skip to main content

Structural organization, thermal stability, and excitation energy utilization of pea thylakoid membranes adapted to low light conditions

Abstract

While the morphological changes in the leaves of low light adapted higher plants are well established, the architecture and lateral arrangement of the thylakoid membrane from plants grown under low light conditions are still not well explored. In the present work we compare the structural organization and thermal stability of thylakoid membranes isolated from pea plants adapted to moderate and low light conditions, and relate the observed structural changes to the functional capacity of the photosynthetic apparatus. In line with earlier reports we confirm that low light induces decrease in the chlorophyll a/b ratio and enlargement of grana membrane regions. Importantly, for the first time we demonstrate a significant thermal instability of low-light thylakoids that are reflected in lower heat needed to disassemble the lateral order of the photosynthetic complexes, as well as for the destabilization of the trimers and monomers of the major light-harvesting complex of photosystem II. Data suggest that this important regulatory complex might adopt different conformation at moderate and low light, which is caused by its specific lateral arrangement within the membrane and might be essential for its regulatory role. In functional terms low light decreases the photochemical activity of thylakoids due to partial photosystem II centers inactivation and impaired electron transport towards photosystem I without inhibiting the photosystems’ functionality, which suggests that the established structural changes play a part in the photosynthetic apparatus operation.

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

Fig. 1
Fig. 2
Fig. 3

References

  1. Albanese P, Manfredi M, Meneghesso A, Marengo E, Saracco G, Barber J, Morosinotto T, Pagliano C (2016) Dynamic reorganization of photosystem II supercomplexes in response to variations in light intensities. Biochim Biophys Acta Bioenerg 1857:1651–1660. https://doi.org/10.1016/j.bbabio.2016.06.011

    CAS  Article  Google Scholar 

  2. Anderson JM, Chow WS, Goodchild DJ (1988) Thylakoid membrane organisation in sun/shade acclimation. Funct Plant Biol 15:11–26. https://doi.org/10.1071/PP9880011

    Article  Google Scholar 

  3. Apostolova EA, Dobrikova AG, Ivanova PI, Petkanchin IB, Taneva SG (2006) Relationship between the organization of the PSII supercomplex and the functions of the photosynthetic apparatus. J Photochem Photobiol B 83:114–122. https://doi.org/10.1016/j.jphotobiol.2005.12.012

    CAS  Article  PubMed  Google Scholar 

  4. Arnon D (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15. https://doi.org/10.1104/pp.24.1.1

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. Bailey S, Walters RG, Jansson S, Horton P (2001) Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses. Planta 213:794–801. https://doi.org/10.1007/s004250100556

    CAS  Article  PubMed  Google Scholar 

  6. Ballottari M, Dall’Osto L, Morosinotto T, Bassi R (2007) Contrasting behavior of higher plant photosystem I and II antenna systems during acclimation. J Biol Chem 282:8947–8958. https://doi.org/10.1074/jbc.M606417200

    CAS  Article  PubMed  Google Scholar 

  7. Brooks A, Portis AR, Sharkey TD (1988) Effects of irradiance and methyl viologen treatment on ATP, ADP, and activation of ribulose bisphosphate carboxylase in spinach leaves. Plant Physiol 88:850–853

    CAS  Article  Google Scholar 

  8. Chow WS, Thorne SW, Duniec JT, Sculley MJ, Boardman NK (1980) The stacking of chloroplast thylakoids: effects of cation screening and binding, studied by the digitonin method. Arch Biochem Biophys 201:347–355. https://doi.org/10.1016/0003-9861(80)90520-2

    CAS  Article  PubMed  Google Scholar 

  9. Chow WS, Hope AB, Anderson JM (1991) Further studies on quantifying photosystem II in vivo by flash-induced oxygen yield from leaf discs. Funct Plant Biol 18:397–410

    CAS  Article  Google Scholar 

  10. Dankov K, Dobrikova A, Bogos B, Gombos Z, Apostolova E (2009) The role of anionic lipids in LHCII organization and in photoinhibition of photosynthetic apparatus. Compt Rend Acad Bulg Sci 62(8):941–948

    CAS  Google Scholar 

  11. Dankov KG, Dobrikova AG, Ughy B, Bogos B, Gombos Z, Apostolova EL (2011) LHCII organization and thylakoid lipids affect the sensitivity of the photosynthetic apparatus to high-light treatment. Plant Physiol Biochem 49:629–635. https://doi.org/10.1016/j.plaphy.2011.02.019

    CAS  Article  PubMed  Google Scholar 

  12. Dobrikova AG, Várkonyi Z, Krumova SB, Kovács L, Kostov GK, Todinova SJ, Busheva MC, Taneva SG, Garab G (2003) Structural rearrangements in chloroplast thylakoid membranes revealed by differential scanning calorimetry and circular dichroism spectroscopy. Thermo-optic effect. Biochemistry 42:11272–11280. https://doi.org/10.1021/bi034899j

    CAS  Article  PubMed  Google Scholar 

  13. Garab G, van Amerongen H (2009) Linear dichroism and circular dichroism in photosynthesis research. Photosynth Res 101:135–146. https://doi.org/10.1007/s11120-009-9424-4

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. Garab G, Wells S, Finzi L, Bustamante C (1988) Helically organized macroaggregates of pigment-protein complexes in chloroplasts: evidence from circular intensity differential scattering. Biochemistry 27:5839–5843

    CAS  Article  Google Scholar 

  15. Goltsev VN, Kalaji HM, Paunov M, Bąba W, Horaczek T, Mojski J, Kociel H, Allakhverdiev SI (2016) Variable chlorophyll fluorescence and its use for assessing physiological condition of plant photosynthetic apparatus. Russ J Plant Physiol 63:869–893. https://doi.org/10.1134/S1021443716050058

    CAS  Article  Google Scholar 

  16. Horton P (2012) Optimization of light harvesting and photoprotection: molecular mechanisms and physiological consequences. Philos Trans R Soc B 367:3455–3465. https://doi.org/10.1098/rstb.2012.0069

    CAS  Article  Google Scholar 

  17. Ivanova PI, Dobrikova AG, Taneva SG, Apostolova EL (2008) Sensitivity of the photosynthetic apparatus to UV-A radiation: role of light-harvesting complex II–photosystem II supercomplex organization. Radiat Environ Biophys 47:169–177. https://doi.org/10.1007/s00411-007-0139-7

    CAS  Article  PubMed  Google Scholar 

  18. Janik E, Bednarska J, Sowinski K, Luchowski R, Zubik M, Grudzinski W, Gruszecki WI (2017) Light-induced formation of dimeric LHCII. Photosynth Res 132:265–276. https://doi.org/10.1007/s11120-017-0387-6

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. Johnson MP, Goral TK, Ruban AV (2011) Photoprotective energy dissipation involves the reorganization of photosystem II light-harvesting complexes in the grana membranes of spinach chloroplasts. Plant Cell 23:1468–1479. https://doi.org/10.1105/tpc.110.081646

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. Kirchhoff H, Haase W, Wegner S, Danielsson R, Ackermann R, Albertsson PA (2007) Low-light-induced formation of semicrystalline photosystem II arrays in higher plant chloroplasts. Biochemistry 46:11169–11176. https://doi.org/10.1021/bi700748y

    CAS  Article  PubMed  Google Scholar 

  21. Kouřil R, Wientjes E, Bultema JB, Croce R, Boekema EJ (2013) High-light vs. low-light: effect of light acclimation on photosystem II composition and organization in Arabidopsis thaliana. Biochim Biophys Acta Bioenerg 1827:411–419. https://doi.org/10.1016/j.bbabio.2012.12.003

    CAS  Article  Google Scholar 

  22. Leong TY, Anderson JM (1984) Adaptation of the thylakoid membranes of pea chloroplasts to light intensities. I. Study on the distribution of chlorophyll-protein complexes. Photosynth Res 5:105–115. https://doi.org/10.1007/BF00028524

    CAS  Article  PubMed  Google Scholar 

  23. Lichtenthaler HK, Kuhn G, Prenzel U, Buschmann C, Meier D (1982a) Adaptation of chloroplast-ultrastructure and of chlorophyll-protein levels to high-light and low-light growth conditions. Z Naturforsch C 37:464–475. https://doi.org/10.1515/znc-1982-5-619

    Article  Google Scholar 

  24. Lichtenthaler HK, Kuhn G, Prenzel U, Meier D (1982b) Chlorophyll-protein levels and degree of thylakoid stacking in radish chloroplasts from high-light, low-light and bentazon-treated plants. Physiol Plant 56:183–188. https://doi.org/10.1111/j.1399-3054.1982.tb00322.x

    CAS  Article  Google Scholar 

  25. Melis A, Harvey GW (1981) Regulation of photosystem stoichiometry, chlorophyll a and chlorophyll b content and relation to chloroplast ultrastructure. Biochim Biophys Acta Bioenerg 637:138–145. https://doi.org/10.1016/0005-2728(81)90219-X

    CAS  Article  Google Scholar 

  26. Minagawa J (2011) State transitions—the molecular remodeling of photosynthetic supercomplexes that controls energy flow in the chloroplast. Biochim Biophys Acta Bioenerg 1807:897–905. https://doi.org/10.1016/j.bbabio.2010.11.005

    CAS  Article  Google Scholar 

  27. Murchie EH, Horton P (1997) Acclimation of photosynthesis to irradiance and spectral quality in British plant species: chlorophyll content, photosynthetic capacity and habitat preference. Plant Cell Environ 20:438–448. https://doi.org/10.1046/j.1365-3040.1997.d01-95.x

    Article  Google Scholar 

  28. Oguchi R, Hikosaka K, Hirose T (2003) Does the photosynthetic light-acclimation need change in leaf anatomy? Plant Cell Environ 26:505–512. https://doi.org/10.1046/j.1365-3040.2003.00981.x

    Article  Google Scholar 

  29. Park IIY, Chow WS, Anderson JM (1997) Antenna size dependency of photoinactivation of photosystem II in light-acclimated pea leaves. Plant Physiol 115:151–157. https://doi.org/10.1104/pp.115.1.151

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. Petrova N, Todinova S, Paunov M, Kovács L, Taneva S, Krumova S (2018) Thylakoid membrane unstacking increases LHCII thermal stability and lipid phase fluidity. J Bioenerg Biomembr 50:425–435. https://doi.org/10.1007/s10863-018-9783-7

    CAS  Article  PubMed  Google Scholar 

  31. Ruban AV (2016) Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage. Plant Physiol 170:1903–1916. https://doi.org/10.1104/pp.15.01935

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. Sims DA, Pearcy RW (1992) Response of leaf anatomy and photosynthetic capacity in Alocasia macrorrhiza (Araceae) to a transfer from low to high light. Am J Bot 79:449–455. https://doi.org/10.2307/2445158

    Article  Google Scholar 

  33. Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence, vol 19. Advances in photosynthesis and respiration. Springer, Dordrecht, pp 321–362

    Chapter  Google Scholar 

  34. Tóth TN, Rai N, Solymosi K, Zsiros O, Schröder WP, Garab G, van Amerongen H, Horton P, Kovács L (2016) Fingerprinting the macro-organisation of pigment–protein complexes in plant thylakoid membranes in vivo by circular-dichroism spectroscopy. Biochim Biophys Acta Bioenerg 1857:1479–1489. https://doi.org/10.1016/j.bbabio.2016.04.287

    CAS  Article  Google Scholar 

Download references

Acknowledgements

This work is supported by Grant Number DFNP 17-138 (N.P.), Program for career development of young scientists and PhD students in Bulgarian Academy of Sciences 2017 and partially by Bulgarian Ministry of Education and Science under the National Research Programme “Young scientists and postdoctoral students” approved by DCM # 577/17.08.2018 (NP). The authors are grateful to Assoc. Prof. Anelia Dobrikova for her help with oxygen evolution experiments.

Funding

This study was funded by Program for career development of young scientists and PhD students in Bulgarian Academy of Sciences 2017 (Grant Number DFNP 17-138, NP) and partially supported by Bulgarian Ministry of Education and Science under the National Research Programme “Young scientists and postdoctoral students” approved by DCM # 577/17.08.2018 (NP).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Sashka Krumova.

Additional information

Publisher's Note

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

Communicated by J. Kovacik.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Petrova, N., Stoichev, S., Paunov, M. et al. Structural organization, thermal stability, and excitation energy utilization of pea thylakoid membranes adapted to low light conditions. Acta Physiol Plant 41, 188 (2019). https://doi.org/10.1007/s11738-019-2979-6

Download citation

Keywords

  • Low light adaptation
  • Thylakoid membrane
  • Photosynthesis
  • Thermal stability