Formation of a PSI–PSII megacomplex containing LHCSR and PsbS in the moss Physcomitrella patens

Abstract

Mosses are one of the earliest land plants that diverged from fresh-water green algae. They are considered to have acquired a higher capacity for thermal energy dissipation to cope with dynamically changing solar irradiance by utilizing both the “algal-type” light-harvesting complex stress-related (LHCSR)-dependent and the “plant-type” PsbS-dependent mechanisms. It is hypothesized that the formation of photosystem (PS) I and II megacomplex is another mechanism to protect photosynthetic machinery from strong irradiance. Herein, we describe the analysis of the PSI–PSII megacomplex from the model moss, Physcomitrella patens, which was resolved using large-pore clear-native polyacrylamide gel electrophoresis (lpCN-PAGE). The similarity in the migration distance of the Physcomitrella PSI–PSII megacomplex to the Arabidopsis megacomplex shown during lpCN-PAGE suggested that the Physcomitrella PSI–PSII and Arabidopsis megacomplexes have similar structures. Time-resolved chlorophyll fluorescence measurements show that excitation energy was rapidly and efficiently transferred from PSII to PSI, providing evidence of an ordered association of the two photosystems. We also found that LHCSR and PsbS co-migrated with the Physcomitrella PSI–PSII megacomplex. The megacomplex showed pH-dependent chlorophyll fluorescence quenching, which may have been induced by LHCSR and/or PsbS proteins with the collaboration of zeaxanthin. We discuss the mechanism that regulates the energy distribution balance between two photosystems in Physcomitrella.

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References

  1. Alboresi A, Gerotto C, Giacometti GM, Bassi R, Morosinotto T (2010) Physcomitrella patens mutants affected on heat dissipation clarify the evolution of photoprotection mechanisms upon land colonization. Proc Natl Acad Sci USA 107:11128–11133. https://doi.org/10.1073/pnas.1002873107

    CAS  Article  PubMed  Google Scholar 

  2. Allahverdiyeva Y, Suorsa M, Tikkanen M, Aro EM (2015) Photoprotection of photosystems in fluctuating light intensities. J Exp Bot 66:2427–2436. https://doi.org/10.1093/jxb/eru463

    CAS  Article  PubMed  Google Scholar 

  3. Allorent G, Lefebvre-Legendre L, Chappuis R, Kuntz M, Truong TB, Niyogi KK, Ulm R, Goldschmidt-Clermont M (2016) UV-B photoreceptor-mediated protection of the photosynthetic machinery in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 113:14864–14869. https://doi.org/10.1073/pnas.1607695114

    CAS  Article  PubMed  Google Scholar 

  4. Ballottari M, Alcocer MJ, D’Andrea C, Viola D, Ahn TK, Petrozza A, Polli D, Fleming GR, Cerullo G, Bassi R (2014) Regulation of photosystem I light-harvesting by zeaxanthin. Proc Natl Acad Sci USA 111:E2431–E2438. https://doi.org/10.1073/pnas.1404377111

    CAS  Article  PubMed  Google Scholar 

  5. Bellafiore S, Barneche F, Peltier G, Rochaix JD (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433:892–895. https://doi.org/10.1038/nature03286

    CAS  Article  PubMed  Google Scholar 

  6. Benson SL, Maheswaran P, Ware MA, Hunter CN, Horton P, Jansson S, Ruban AV, Johnson MP (2015) An intact light-harvesting complex I antenna system is required for complete state transitions in Arabidopsis. Nat Plant 1:15176. https://doi.org/10.1038/nplants.2015.176

    CAS  Article  Google Scholar 

  7. Bonente G, Ballottari M, Truong TB, Morosinotto T, Ahn TK, Fleming GR, Niyogi KK, Bassi R (2011) Analysis of LhcSR3, a protein essential for feedback de-excitation in the green alga Chlamydomonas reinhardtii. PLOS Biol 9:e1000577. https://doi.org/10.1371/journal.pbio.1000577

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. Bos I, Bland KM, Tian LJ, Croce R, Frankel LK, van Amerongen H, Bricker TM, Wientjes E (2017) Multiple LHCII antennae can transfer energy efficiently to a single photosystem I. Biochim Biophys Acta 1858:371–378. https://doi.org/10.1016/j.bbabio.2017.02.012

    CAS  Article  Google Scholar 

  9. Busch A, Petersen J, Webber-Birungi MT, Powikrowska M, Lassen LM, Naumann-Busch B, Nielsen AZ, Ye J, Boekema EJ, Jensen ON, Lunde C, Jensen PE (2013) Composition and structure of photosystem I in the moss Physcomitrella patens. J Exp Bot 64:2689–2699. https://doi.org/10.1093/jxb/ert126

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. Correa-Galvis V, Poschmann G, Melzer M, Stühler K, Jahns P (2016a) PsbS interactions involved in the activation of energy dissipation in Arabidopsis. Nat Plants 2:15225. https://doi.org/10.1038/nplants.2015.225

    CAS  Article  PubMed  Google Scholar 

  11. Correa-Galvis V, Redekop P, Guan K, Griess A, Truong TB, Wakao S, Niyogi KK, Jahns P (2016b) Photosystem II subunit PsbS is involved in the induction of LHCSR protein-dependent energy dissipation in Chlamydomonas reinhardtii. J Biol Chem 291:17478–17487. https://doi.org/10.1074/jbc.M116.737312

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. Croce R, van Amerongen H (2013) Light-harvesting in photosystem I. Photosynth Res 116:153–166. https://doi.org/10.1007/s11120-013-9838-x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. Dinc E, Tian L, Roy LM, Roth R, Goodenough U, Croce R (2016) LHCSR1 induces a fast and reversible pH-dependent fluorescence quenching in LHCII in Chlamydomonas reinhardtii cells. Proc Natl Acad Sci USA 113(27):7673–7678. https://doi.org/10.1073/pnas.1605380113

    CAS  Article  PubMed  Google Scholar 

  14. Ferroni L, Suorsa M, Aro EM, Baldisserotto C, Pancaldi S (2016) Light acclimation in the lycophyte Selaginella martensii depends on changes in the number of photosystems and on the flexibility of the light-harvesting complex II antenna association with both photosystems. New Phytol 211:554–568. https://doi.org/10.1111/nph.13939

    CAS  Article  PubMed  Google Scholar 

  15. Ferroni L, Cucuzza S, Angeleri M, Aro EM, Pagliano C, Giovanardi M, Baldisserotto C, Pancaldi S (2018) In the lycophyte Selaginella martensii is the “extra-qT” related to energy spillover? Insights into photoprotection in ancestral vascular plants. Enrion Exp Bot 154:110–122. https://doi.org/10.1016/j.envexpbot.2017.10.023

    CAS  Article  Google Scholar 

  16. Gerotto C, Alboresi A, Giacometti GM, Bassi R, Morosinotto T (2011) Role of PSBS and LHCSR in Physcomitrella patens acclimation to high light and low temperature. Plant Cell Environ 34:922–932. https://doi.org/10.1111/j.1365-3040.2011.02294.x

    CAS  Article  PubMed  Google Scholar 

  17. Giovanardi M, Poggioli M, Ferroni L, Lespinasse M, Baldisserotto C, Aro EM, Pancaldi S (2017) Higher packing of thylakoid complexes ensures a preserved photosystem II activity in mixotrophic Neochloris oleoabundans. Algal Res 25:322–332. https://doi.org/10.1016/j.algal.2017.05.020

    Article  Google Scholar 

  18. Goss R, Lepetit B (2015) Biodiversity of NPQ. J Plant Physiol 172:13–32. https://doi.org/10.1016/j.jplph.2014.03.004

    CAS  Article  PubMed  Google Scholar 

  19. Iwai M, Yokono M (2017) Light-harvesting antenna complexes in the moss Physcomitrella patens: implications for the evolutionary transition from green algae to land plants. Curr Opin Plant Biol 37:94–101. https://doi.org/10.1016/j.pbi.2017.04.002

    CAS  Article  PubMed  Google Scholar 

  20. Iwai M, Yokono M, Inada N, Minagawa J (2010) Live-cell imaging of photosystem II antenna dissociation during state transitions. Proc Natl Acad Sci USA 107:2337–2342. https://doi.org/10.1073/pnas.0908808107

    Article  PubMed  Google Scholar 

  21. Iwai M, Yokono M, Kono M, Noguchi K, Akimoto S, Nakano A (2015) Light-harvesting complex Lhcb9 confers a green alga-type photosystem I supercomplex to the moss Physcomitrella patens. Nat Plants 1:14008. https://doi.org/10.1038/nplants.2014.8

    CAS  Article  PubMed  Google Scholar 

  22. Iwai M, Grob P, Iavarone AT, Nogales E, Niyogi KK (2018) A unique supramolecular organization of photosystem I in the moss Physcomitrella patens. Nat Plants 4:904–909. https://doi.org/10.1038/s41477-018-0271-1

    CAS  Article  PubMed  Google Scholar 

  23. Järvi S, Suorsa M, Paakkarinen V, Aro EM (2011) Optimized native gel systems for separation of thylakoid protein complexes: novel super- and mega-complexes. Biochem J 439:207–214. https://doi.org/10.1042/BJ20102155

    CAS  Article  PubMed  Google Scholar 

  24. Kondo T, Pinnola A, Chen WJ, Dall’Osto L, Bassi R, Schlau-Cohen GS (2017) Single-molecule spectroscopy of LHCSR1 protein dynamics identifies two distinct states responsible for multi-timescale photosynthetic photoprotection. Nat Chem 9:772–778. https://doi.org/10.1038/nchem.2818

    CAS  Article  PubMed  Google Scholar 

  25. Kosuge K, Tokutsu R, Kim E, Akimoto S, Yokono M, Ueno Y, Minagawa J (2018) LHCSR1-dependent fluorescence quenching is mediated by excitation energy transfer from LHCII to photosystem I in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 115:3722–3727. https://doi.org/10.1073/pnas.1720574115

    CAS  Article  PubMed  Google Scholar 

  26. Kunugi M, Satoh S, Ihara K, Shibata K, Yamagishi Y, Kogame K, Obokata J, Takabayashi A, Tanaka A (2016) Evolution of green plants accompanied changes in light-harvesting systems. Plant Cell Physiol 57:1231–1243. https://doi.org/10.1093/pcp/pcw071

    CAS  Article  PubMed  Google Scholar 

  27. Mazor Y, Borovikova A, Nelson N (2015) The structure of plant photosystem I super-complex at 2.8 A resolution. Elife 4:e07433. https://doi.org/10.7554/eLife.07433

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  28. Melkozernov AN, Blankenship RE (2005) Structural and functional organization of the peripheral light-harvesting system in photosystem I. Photosynth Res 85:33–50. https://doi.org/10.1007/s11120-004-6474-5

    CAS  Article  PubMed  Google Scholar 

  29. Melkozernov AN, Kargul J, Lin S, Barber J, Blankenship RE (2004) Energy coupling in the PSI–LHCI supercomplex from the green alga Chlamydomonas reinhardtii. J Phys Chem B 108:10547–10555. https://doi.org/10.1021/jp049375n

    CAS  Article  Google Scholar 

  30. Mimuro M, Yokono M, Akimoto S (2010) Variations in photosystem I properties in the primordial cyanobacterium Gloeobacter violaceus PCC 7421. Photochem Photobiol 86:62–69. https://doi.org/10.1111/j.1751-1097.2009.00619.x

    CAS  Article  PubMed  Google Scholar 

  31. Minagawa J, Tokutsu R (2015) Dynamic regulation of photosynthesis in Chlamydomonas reinhardtii. Plant J 82:413–428. https://doi.org/10.1111/tpj.12805

    CAS  Article  PubMed  Google Scholar 

  32. Nishiyama T, Hiwatashi Y, Sakakibara I, Kato M, Hasebe M (2000) Tagged mutagenesis and gene-trap in the moss, Physcomitrella patens by shuttle mutagenesis. DNA Res 7:9–17. https://doi.org/10.1093/dnares/7.1.9

    CAS  Article  PubMed  Google Scholar 

  33. Niyogi KK, Truong TB (2013) Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis. Curr Opin Plant Biol 16:307–314. https://doi.org/10.1016/j.pbi.2013.03.011

    CAS  Article  PubMed  Google Scholar 

  34. Peers G, Truong TB, Ostendorf E, Busch A, Elrad D, Grossman AR, Hippler M, Niyogi KK (2009) An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462:518–521. https://doi.org/10.1038/nature08587

    CAS  Article  PubMed  Google Scholar 

  35. Pesaresi P, Hertle A, Pribil M, Kleine T, Wagner R, Strissel H, Ihnatowicz A, Bonardi V, Scharfenberg M, Schneider A, Pfannschmidt T, Leister D (2009) Arabidopsis STN7 kinase provides a link between short- and long-term photosynthetic acclimation. Plant Cell 21:2402–2423. https://doi.org/10.1105/tpc.108.064964

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. Petroutsos D, Tokutsu R, Maruyama S, Flori S, Greiner A, Magneschi L, Cusant L, Kottke T, Mittag M, Hegemann P, Finazzi G, Minagawa J (2016) A blue-light photoreceptor mediates the feedback regulation of photosynthesis. Nature 537:563–566. https://doi.org/10.1038/nature19358

    CAS  Article  PubMed  Google Scholar 

  37. Pinnola A, Dall’Osto L, Gerotto C, Morosinotto T, Bassi R, Alboresi A (2013) Zeaxanthin binds to light-harvesting complex stress-related protein to enhance nonphotochemical quenching in Physcomitrella patens. Plant Cell 25:3519–3534. https://doi.org/10.1105/tpc.113.114538

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. Pinnola A, Cazzaniga S, Alboresi A, Nevo R, Levin-Zaidman S, Reich Z, Bassi R (2015) Light-harvesting complex stress-related proteins catalyze excess energy dissipation in both photosystems of Physcomitrella patens. Plant Cell 27:3213–3227. https://doi.org/10.1105/tpc.15.00443

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. Pinnola A, Ballottari M, Bargigia I, Alcocer M, D’Andrea C, Cerullo G, Bassi R (2017) Functional modulation of LHCSR1 protein from Physcomitrella patens by zeaxanthin binding and low pH. Sci Rep 7:11158. https://doi.org/10.1038/s41598-017-11101-7

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. Popot JL, Althoff T, Bagnard D, Baneres JL, Bazzacco P, Billon-Denis E, Catoire LJ, Champeil P, Charvolin D, Cocco MJ, Cremel G, Dahmane T, de la Maza LM, Ebel C, Gabel F, Giusti F, Gohon Y, Goormaghtigh E, Guittet E, Kleinschmidt JH, Kuhlbrandt W, Le Bon C, Martinez KL, Picard M, Pucci B, Sachs JN, Tribet C, van Heijenoort C, Wien F, Zito F, Zoonens M (2011) Amphipols from A to Z. Annu Rev Biophys 40:379–408. https://doi.org/10.1146/annurev-biophys-042910-155219

    CAS  Article  PubMed  Google Scholar 

  41. Ruban AV (2015) Evolution under the sun: optimizing light harvesting in photosynthesis. J Exp Bot 66:7–23. https://doi.org/10.1093/jxb/eru400

    CAS  Article  PubMed  Google Scholar 

  42. 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 

  43. Sacharz J, Giovagnetti V, Ungerer P, Mastroianni G, Ruban AV (2017) The xanthophyll cycle affects reversible interactions between PsbS and light-harvesting complex II to control non-photochemical quenching. Nat Plants 3:16225. https://doi.org/10.1038/nplants.2016.225

    CAS  Article  PubMed  Google Scholar 

  44. Schlodder E, Hussels M, Çetin M, Karapetyan NV, Brecht M (2011) Fluorescence of the various red antenna states in photosystem I complexes from cyanobacteria is affected differently by the redox state of P700. Biochim Biophys Acta 1807:1423–1431. https://doi.org/10.1016/j.bbabio.2011.06.018

    CAS  Article  PubMed  Google Scholar 

  45. Shubin VV, Bezsmertnaya IN, Karapetyan NV (1995) Efficient energy-transfer from the long-wavelength antenna chlorophylls to P700 in photosystem-I complexes from Spirulina platensis. J Photochem Photobiol B 30:153–160. https://doi.org/10.1016/1011-1344(95)07173-Y

    CAS  Article  Google Scholar 

  46. Strecker V, Wumaier Z, Wittig I, Schägger H (2010) Large pore gels to separate mega protein complexes larger than 10 MDa by blue native electrophoresis: isolation of putative respiratory strings or patches. Proteomics 10:3379–3387. https://doi.org/10.1002/pmic.201000343

    CAS  Article  PubMed  Google Scholar 

  47. Suorsa M, Rantala M, Danielsson R, Jarvi S, Paakkarinen V, Schroder WP, Styring S, Mamedov F, Aro EM (2014) Dark-adapted spinach thylakoid protein heterogeneity offers insights into the photosystem II repair cycle. Biochim Biophys Acta 1837:1463–1471. https://doi.org/10.1016/j.bbabio.2013.11.014

    CAS  Article  PubMed  Google Scholar 

  48. Suorsa M, Rantala M, Mamedov F, Lespinasse M, Trotta A, Grieco M, Vuorio E, Tikkanen M, Jarvi S, Aro EM (2015) Light acclimation involves dynamic re-organization of the pigment-protein megacomplexes in non-appressed thylakoid domains. Plant J 84:360–373. https://doi.org/10.1111/tpj.13004

    CAS  Article  PubMed  Google Scholar 

  49. Tilbrook K, Dubois M, Crocco CD, Yin R, Chappuis R, Allorent G, Schmid-Siegert E, Goldschmidt-Clermont M, Ulm R (2016) UV-B perception and acclimation in Chlamydomonas reinhardtii. Plant Cell 28:966–983. https://doi.org/10.1105/tpc.15.00287

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. Tokutsu R, Minagawa J (2013) Energy-dissipative supercomplex of photosystem II associated with LHCSR3 in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 110:10016–10021. https://doi.org/10.1073/pnas.1222606110

    Article  PubMed  Google Scholar 

  51. Tokutsu R, Fujimura-Kamada K, Yamasaki T, Matsuo T, Minagawa J (2019) Isolation of photoprotective signal transduction mutants by systematic bioluminescence screening in Chlamydomonas reinhardtii. Sci Rep 9:2820. https://doi.org/10.1038/s41598-019-39785-z

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  52. Ueno Y, Aikawa S, Kondo A, Akimoto S (2018) Adaptation of light-harvesting functions of unicellular green algae to different light qualities. Photosynth Res 139:145–154. https://doi.org/10.1007/s11120-018-0523-y

    CAS  Article  PubMed  Google Scholar 

  53. Umetani I, Kunugi M, Yokono M, Takabayashi A, Tanaka A (2018) Evidence of the supercomplex organization of photosystem II and light-harvesting complexes in Nannochloropsis granulata. Photosynth Res 136:49–61. https://doi.org/10.1007/s11120-017-0438-z

    CAS  Article  PubMed  Google Scholar 

  54. Van Grondelle R (1985) Excitation-energy transfer, trapping and annihilation in photosynthetic systems. Biochim Biophys Acta 811:147–195. https://doi.org/10.1016/0304-4173(85)90017-5

    Article  Google Scholar 

  55. Vasil’ev S, Irrgang KD, Schrotter T, Bergmann A, Eichler HJ, Renger G (1997) Quenching of chlorophyll a fluorescence in the aggregates of LHCII: steady-state fluorescence and picosecond relaxation kinetics. Biochemistry 36:7503–7512. https://doi.org/10.1021/bi9625253

    Article  PubMed  Google Scholar 

  56. Watanabe A, Kim E, Burton-Smith RN, Tokutsu R, Minagawa J (2019) Amphipol-assisted purification method for the highly active and stable photosystem II supercomplex of Chlamydomonas reinhardtii. FEBS Lett 593:1072–1079. https://doi.org/10.1002/1873-3468.13394

    CAS  Article  PubMed  Google Scholar 

  57. Wobbe L, Bassi R, Kruse O (2016) Multi-level light capture control in plants and green algae. Trends Plant Sci 21:55–68. https://doi.org/10.1016/j.tplants.2015.10.004

    CAS  Article  PubMed  Google Scholar 

  58. Xu DQ, Chen Y, Chen GY (2015) Light-harvesting regulation from leaf to molecule with the emphasis on rapid changes in antenna size. Photosynth Res 124:137–158. https://doi.org/10.1007/s11120-015-0115-z

    CAS  Article  PubMed  Google Scholar 

  59. Yokono M, Akimoto S (2018) Energy transfer and distribution in photosystem super/megacomplexes of plants. Curr Opin Biotechnol 54:50–56. https://doi.org/10.1016/j.copbio.2018.01.001

    CAS  Article  PubMed  Google Scholar 

  60. Yokono M, Takabayashi A, Akimoto S, Tanaka A (2015) A megacomplex composed of both photosystem reaction centres in higher plants. Nat Commun. https://doi.org/10.1038/ncomms7675

    Article  PubMed  Google Scholar 

  61. Yokono M, Umetani I, Takabayashi A, Akimoto S, Tanaka A (2018) Regulation of excitation energy in Nannochloropsis photosystem II. Photosynth Res 139:155–161. https://doi.org/10.1007/s11120-018-0510-3

    CAS  Article  PubMed  Google Scholar 

  62. Yokono M, Takabayashi A, Kishimoto J, Fujita T, Iwai M, Murakami A, Akimoto S, Tanaka A (2019) The PSI–PSII megacomplex in green plants. Plant Cell Phyiol accepted. https://doi.org/10.1093/pcp/pcz026

    Article  Google Scholar 

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Acknowledgements

This work was supported by JSPS (Japan Society for the Promotion of Science) KAKENHI Grant numbers 23770035 to A. Takabayashi, 16H06553 to S. Akimoto, and 16H06554 to R. Tanaka.

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Furukawa, R., Aso, M., Fujita, T. et al. Formation of a PSI–PSII megacomplex containing LHCSR and PsbS in the moss Physcomitrella patens. J Plant Res 132, 867–880 (2019). https://doi.org/10.1007/s10265-019-01138-2

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Keywords

  • Physcomitrella
  • PSI–PSII megacomplex
  • LHCSR
  • CN-PAGE