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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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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Goss R, Lepetit B (2015) Biodiversity of NPQ. J Plant Physiol 172:13–32. https://doi.org/10.1016/j.jplph.2014.03.004
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
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
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
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
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
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
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
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
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
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
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
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
Minagawa J, Tokutsu R (2015) Dynamic regulation of photosynthesis in Chlamydomonas reinhardtii. Plant J 82:413–428. https://doi.org/10.1111/tpj.12805
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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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DOI: https://doi.org/10.1007/s10265-019-01138-2