Probing functional and optical cross-sections of PSII in leaves during state transitions using fast repetition rate light induced fluorescence transients
Barry Osmond
A B C , Wah Soon Chow B , Barry J. Pogson B and Sharon A. Robinson A
+ Author Affiliations
- Author Affiliations
A Centre for Sustainable Ecosystem Solutions, School of Biological Sciences, University of Wollongong, Northfields Avenue, Wollongong, NSW 2522, Australia.
B Division of Plant Sciences, Research School of Biology, The Australian National University, 46 Sullivan’s Creek Road, Acton, ACT 2601, Australia.
C Corresponding author. Email: osmond.barry@gmail.com
Functional Plant Biology 46(6) 567-583 https://doi.org/10.1071/FP18054
Submitted: 8 March 2018 Accepted: 7 February 2019 Published: 4 March 2019
Abstract
Plants adjust the relative sizes of PSII and PSI antennae in response to the spectral composition of weak light favouring either photosystem by processes known as state transitions (ST), attributed to a discrete antenna migration involving phosphorylation of light-harvesting chlorophyll-protein complexes in PSII. Here for the first time we monitored the extent and dynamics of ST in leaves from estimates of optical absorption cross-section (relative PSII antenna size; aPSII). These estimates were obtained from in situ measurements of functional absorption cross-section (σPSII) and maximum photochemical efficiency of PSII (φPSII); i.e. aPSII = σPSII/φPSII (Kolber et al. 1998) and other parameters from a light induced fluorescence transient (LIFT) device (Osmond et al. 2017). The fast repetition rate (FRR) QA flash protocol of this instrument monitors chlorophyll fluorescence yields with reduced QA irrespective of the redox state of plastoquinone (PQ), as well as during strong ~1 s white light pulses that fully reduce the PQ pool. Fitting this transient with the FRR model monitors kinetics of PSII → PQ, PQ → PSI, and the redox state of the PQ pool in the ‘PQ pool control loop’ that underpins ST, with a time resolution of a few seconds. All LIFT/FRR criteria confirmed the absence of ST in antenna mutant chlorina-f2 of barley and asLhcb2–12 of Arabidopsis, as well as STN7 kinase mutants stn7 and stn7/8. In contrast, wild-type barley and Arabidopsis genotypes Col, npq1, npq4, OEpsbs, pgr5 bkg and pgr5, showed normal ST. However, the extent of ST (and by implication the size of the phosphorylated LHCII pool participating in ST) deduced from changes in aʹPSII and other parameters with reduced QA range up to 35%. Estimates from strong WL pulses in the same assay were only ~10%. The larger estimates of ST from the QA flash are discussed in the context of contemporary dynamic structural models of ST involving formation and participation of PSII and PSI megacomplexes in an ‘energetically connected lake’ of phosphorylated LHCII trimers (Grieco et al. 2015). Despite the absence of ST, asLhcb2-12 displays normal wild-type modulation of electron transport rate (ETR) and the PQ pool during ST assays, reflecting compensatory changes in antenna LHCIIs in this genotype. Impaired LHCII phosphorylation in stn7 and stn7/8 accelerates ETR from PSII →PQ, over-reducing the PQ pool and abolishing the yield difference between the QA flash and WL pulse, with implications for photochemical and thermal phases of the O-J-I-P transient.
Additional keywords: apparent antenna size, Arabidopsis mutants, barley mutants, chlorophyll fluorescence, electron transfer rates, PQ pool redox status.
References
Allen JF (2002) Plastoquinone redox control of chloroplast thylakoid protein phosphorylation and distribution of excitation energy between photosystems: discovery, background, implications. Photosynthesis Research 73, 139–148.| Plastoquinone redox control of chloroplast thylakoid protein phosphorylation and distribution of excitation energy between photosystems: discovery, background, implications.Crossref | GoogleScholarGoogle Scholar | 16245115PubMed |
Allen JF (2017) Why we need to know the structure of phosphorylated chloroplast light-harvesting complex II. Physiologia Plantarum 161, 28–44.
| Why we need to know the structure of phosphorylated chloroplast light-harvesting complex II.Crossref | GoogleScholarGoogle Scholar | 28393369PubMed |
Allen JF, Melis A (1988) The rate of P-700 photoxidation under continuous illumination is independent of State 1–State 2 transitions in the green alga Scenedesmus obliquus. Biochimica et Biophysica Acta 933, 95–106.
| The rate of P-700 photoxidation under continuous illumination is independent of State 1–State 2 transitions in the green alga Scenedesmus obliquus.Crossref | GoogleScholarGoogle Scholar |
Allen JF, Bennett J, Steinbeck KE, Arntzen CJ (1981) Chloroplast protein photophosphorylation couples plastoquinone redox state to distribution of excitation energy between photosystems. Nature 291, 25–29.
| Chloroplast protein photophosphorylation couples plastoquinone redox state to distribution of excitation energy between photosystems.Crossref | GoogleScholarGoogle Scholar |
Andersson J, Wentworth M, Walters RG, Howard CA, Ruban AV, Horton P, Jansson S (2003) Absence of the Lhcb1 and Lhcb2 proteins of the light-harvesting complex of photosystem II – effects on photosynthesis, grana stacking and fitness. The Plant Journal 35, 350–361.
| Absence of the Lhcb1 and Lhcb2 proteins of the light-harvesting complex of photosystem II – effects on photosynthesis, grana stacking and fitness.Crossref | GoogleScholarGoogle Scholar | 12887586PubMed |
Behrenfeld MJ, Kolber ZS (1999) Widespread iron limitation of phytoplankton photosynthesis in the South Pacific Ocean. Science 283, 840–843.
| Widespread iron limitation of phytoplankton photosynthesis in the South Pacific Ocean.Crossref | GoogleScholarGoogle Scholar | 9933166PubMed |
Bellafiore S, Barneche F, Peltier G, Rochaix J-D (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433, 892–895.
| State transitions and light adaptation require chloroplast thylakoid protein kinase STN7.Crossref | GoogleScholarGoogle Scholar | 15729347PubMed |
Bennett J, Steinback KE, Arntzen CJ (1980) Chloroplast phosphoproteins – regulation of excitation-energy transfer by phosphorylation of thylakoid membrane polypeptides. Proceedings of the National Academy of Sciences of the United States of America 77, 5253–5257.
| Chloroplast phosphoproteins – regulation of excitation-energy transfer by phosphorylation of thylakoid membrane polypeptides.Crossref | GoogleScholarGoogle Scholar | 6933557PubMed |
Bonardi V, Pesaresi P, Becker T, Schleiff E, Wagner R, Pfannschmidt T, Jahns P, Leister D (2005) Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases. Nature 437, 1179–1182.
| Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases.Crossref | GoogleScholarGoogle Scholar | 16237446PubMed |
Bonaventura C, Meyers J (1969) Fluorescence and oxygen evolution from Chlorella pyrenoidosa. Biochimica et Biophysica Acta 189, 366–383.
| Fluorescence and oxygen evolution from Chlorella pyrenoidosa.Crossref | GoogleScholarGoogle Scholar | 5370012PubMed |
Bos I, Bland KM, Tian L, Croce R, Frankel LK, van Amerongen H, Bricker TM, Wientjes E (2017) Multiple LHCII antennae can transfer energy efficiently to a single photosystem I. Biochimica et Biophysica Acta 1858, 371–378.
| Multiple LHCII antennae can transfer energy efficiently to a single photosystem I.Crossref | GoogleScholarGoogle Scholar | 28237494PubMed |
Bossmann B, Knoetzel J, Jansson S (1997) Screening chlorina mutants of barley (H. vulgare L.) with antibodies against light-harvesting proteins of PSI and PSII: absence of specific antenna proteins. Photosynthesis Research 52, 127–136.
| Screening chlorina mutants of barley (H. vulgare L.) with antibodies against light-harvesting proteins of PSI and PSII: absence of specific antenna proteins.Crossref | GoogleScholarGoogle Scholar |
Chow WS, Telfer A, Chapman DJ, Barber J (1981) State 1–State 2 transition in leaves and its association with ATP-induced chlorophyll fluorescence quenching. Biochimica et Biophysica Acta 638, 60–68.
| State 1–State 2 transition in leaves and its association with ATP-induced chlorophyll fluorescence quenching.Crossref | GoogleScholarGoogle Scholar |
Delosme R, Olive J, Wollman FA (1996) Changes in light energy distribution upon state transitions: an in vivo photoacoustic study of the wildtype and photosynthesis mutants from Chlamydomonas reinhardtii. Biochimica et Biophysica Acta 1273, 153–158.
Dietzel L, Bräutigam K, Steiner S, Schüffler K, Lepetit B, Grimm B, Schöttler MA, Pfannschmidt T (2011) Photosystem II supercomplex remodelling serves as an entry mechanism for state transitions in Arabidopsis. The Plant Cell 23, 2964–2977.
| Photosystem II supercomplex remodelling serves as an entry mechanism for state transitions in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 21880991PubMed |
Falkowski PG, Kolber Z (1995) Variations in chlorophyll fluorescence yields in phytoplankton in the world oceans. Australian Journal of Plant Physiology 22, 341–355.
Galka P, Santabarbara S, Khuong TTH, Degand H, Morosomme P, Jennings RC, Boekema EJ, Caffarri S (2012) Functional analyses of the plant photosystem I-light-harvesting complex II supercomplex reveal that light-harvesting complex II loosely bound to photosystem II is a very efficient antenna for photosystem I in State II. The Plant Cell 24, 2963–2978.
| Functional analyses of the plant photosystem I-light-harvesting complex II supercomplex reveal that light-harvesting complex II loosely bound to photosystem II is a very efficient antenna for photosystem I in State II.Crossref | GoogleScholarGoogle Scholar | 22822202PubMed |
Grieco M, Suorsa M, Paakkarinen V, Kangajarvi S, Aro E-M (2012) Steady-state phosphorylation of light-harvesting complex II proteins preserves photosystem I underfluctuating white light. Plant Physiology 160, 1896–1910.
| Steady-state phosphorylation of light-harvesting complex II proteins preserves photosystem I underfluctuating white light.Crossref | GoogleScholarGoogle Scholar | 23033142PubMed |
Grieco M, Suorsa M, Jajoo A, Tikkanen M (2015) Light-harvesting II antenna trimers connect energetically the entire photosynthetic machinery – including both photosystems II and I. Biochimica et Biophysica Acta 1847, 607–619.
| Light-harvesting II antenna trimers connect energetically the entire photosynthetic machinery – including both photosystems II and I.Crossref | GoogleScholarGoogle Scholar | 25843550PubMed |
Haldrup A, Jensen PE, Lunde C, Scheller HV (2001) Balance of power: a view of the mechanisms of photosynthetic state transitions. Trends in Plant Science 6, 301–305.
| Balance of power: a view of the mechanisms of photosynthetic state transitions.Crossref | GoogleScholarGoogle Scholar | 11435168PubMed |
Harrison MA, Nemson JA, Melis A (1993) Assembly and composition of the chlorophyll a-b light-harvesting complex of barley (Hordeum vulgare L.): immunochemical analysis of chlorophyll b-less and chlorophyll b-deficient mutants. Photosynthesis Research 38, 141–151.
| Assembly and composition of the chlorophyll a-b light-harvesting complex of barley (Hordeum vulgare L.): immunochemical analysis of chlorophyll b-less and chlorophyll b-deficient mutants.Crossref | GoogleScholarGoogle Scholar | 24317910PubMed |
Highkin HR (1950) Chlorophyll studies on barley mutants. Plant Physiology 25, 294–306.
| Chlorophyll studies on barley mutants.Crossref | GoogleScholarGoogle Scholar | 16654291PubMed |
Hirth M, Dietzel L, Steiner S, Ludwig R, Weidenbach H, Pfalz J, Pfannschmidt T (2013) Photosynthetic acclimation responses of maize seedlings grown under artificial laboratory light gradients mimicking natural canopy conditions. Frontiers in Plant Science 4, 334
| Photosynthetic acclimation responses of maize seedlings grown under artificial laboratory light gradients mimicking natural canopy conditions.Crossref | GoogleScholarGoogle Scholar | 24062753PubMed |
Hogewoning SW, Wientjes E, Douwstra P, Trouwborst G, van Ieperen W, Croce R, Harbinson J (2012) Photosynthetic quantum yield dynamics; from photosystems to leaves. The Plant Cell 24, 1921–1935.
| Photosynthetic quantum yield dynamics; from photosystems to leaves.Crossref | GoogleScholarGoogle Scholar | 22623496PubMed |
Horton P (1983) Control of chloroplast electron transport by phosphorylation of thylakoid proteins. FEBS Letters 152, 47–52.
| Control of chloroplast electron transport by phosphorylation of thylakoid proteins.Crossref | GoogleScholarGoogle Scholar |
Iwai M, Yokono M, Minagawa J (2008) Molecular remodeling of photosystem II during state transitions in Chlamydomonas reinhardtii. The Plant Cell 20, 2177–2189.
| Molecular remodeling of photosystem II during state transitions in Chlamydomonas reinhardtii.Crossref | GoogleScholarGoogle Scholar | 18757554PubMed |
Iwai M, Yokono M, Minagawa J (2010) Live-cell imaging of photosystem II antenna dissociation during state transitions. Proceedings of the National Academy of Sciences of the United States of America 107, 2337–2342.
| Live-cell imaging of photosystem II antenna dissociation during state transitions.Crossref | GoogleScholarGoogle Scholar | 20080575PubMed |
Järvi S, Suorsa M, Paakkarinen V, Aro E-M (2011) Optimized native gel systems for separation of thylakoid protein complexes: novel super- and mega-complexes. The Biochemical Journal 439, 207–214.
| Optimized native gel systems for separation of thylakoid protein complexes: novel super- and mega-complexes.Crossref | GoogleScholarGoogle Scholar | 21707535PubMed |
Keller B, Vass I, Matsubara S, Paul K, Jedmowski C, Pieruschka R, Nedbal L, Rascher U, Muller O (2018) Maximum fluorescence yield and electron transport kinetics determined by light-induced fluorescence transients (LIFT) for photosynthesis phenotyping. Photosynthesis Research
| Maximum fluorescence yield and electron transport kinetics determined by light-induced fluorescence transients (LIFT) for photosynthesis phenotyping.Crossref | GoogleScholarGoogle Scholar | 30357678PubMed |
Kim E, Ahn TK, Kumazaki S (2015) Changes in antenna sizes of photosystems during state transitions in granal and stroma-exposed thylakoid membrane of intact chloroplasts in Arabidopsis mesophyll protoplasts. Plant & Cell Physiology 56, 759–768.
| Changes in antenna sizes of photosystems during state transitions in granal and stroma-exposed thylakoid membrane of intact chloroplasts in Arabidopsis mesophyll protoplasts.Crossref | GoogleScholarGoogle Scholar |
Kolber Z, Falkowski PG (1993) Use of active fluorescence to estimate phytoplankton photosynthesis in situ. Limnology and Oceanography 38, 1646–1665.
| Use of active fluorescence to estimate phytoplankton photosynthesis in situ.Crossref | GoogleScholarGoogle Scholar |
Kolber Z, Prasil O, Falkowski PG (1998) Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. Biochimica et Biophysica Acta 1367, 88–106.
| Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols.Crossref | GoogleScholarGoogle Scholar | 9784616PubMed |
Kolber Z, Klimov D, Ananyev G, Rascher U, Berry J, Osmond B (2005) Measuring photosynthetic parameters at a distance: laser induced fluorescence transient (LIFT) method for remote measurements of PSII in terrestrial vegetation. Photosynthesis Research 84, 121–129.
| Measuring photosynthetic parameters at a distance: laser induced fluorescence transient (LIFT) method for remote measurements of PSII in terrestrial vegetation.Crossref | GoogleScholarGoogle Scholar | 16049764PubMed |
Laisk A, Oja V (2018) Kinetics of photosystem II electron transport: a mathematical analysis based on chlorophyll fluorescence induction. Photosynthesis Research 136, 63–82.
| Kinetics of photosystem II electron transport: a mathematical analysis based on chlorophyll fluorescence induction.Crossref | GoogleScholarGoogle Scholar | 28936722PubMed |
Laisk A, Oja V, Eichelmann H, Dall’Osto L (2014) Action spectra of photosystem II and I and quantum yield of photosynthesis in leaves in State 1. Biochimica et Biophysica Acta 1837, 315–325.
| Action spectra of photosystem II and I and quantum yield of photosynthesis in leaves in State 1.Crossref | GoogleScholarGoogle Scholar | 24333386PubMed |
Ley AC, Mauzerall D (1982) Absolute absorption cross sections for photosystem II and the minimum quantum requirement for photosynthesis in Chlorella vulgaris. Biochimica et Biophysica Acta 680, 95–106.
| Absolute absorption cross sections for photosystem II and the minimum quantum requirement for photosynthesis in Chlorella vulgaris.Crossref | GoogleScholarGoogle Scholar |
Li X-P, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403, 391–395.
| A pigment-binding protein essential for regulation of photosynthetic light harvesting.Crossref | GoogleScholarGoogle Scholar | 10667783PubMed |
Li X-P, Müller-Moulɹ P, Gilmore AM, Niyogi KK (2002) PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proceedings of the National Academy of Sciences of the United States of America 99, 15222–15227.
| PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition.Crossref | GoogleScholarGoogle Scholar | 12417767PubMed |
Matsubara S, Chow WS (2004) Populations of photoinactivated photosystem II reaction centers characterized by chlorophyll a fluorescence lifetime in vivo. Proceedings of the National Academy of Sciences of the United States of America 101, 18234–18239.
| Populations of photoinactivated photosystem II reaction centers characterized by chlorophyll a fluorescence lifetime in vivo.Crossref | GoogleScholarGoogle Scholar | 15601775PubMed |
Mekala NR, Suorsa M, Rantala M, Aro E-M, Tikkanen M (2015) Plants actively avoid state transitions upon changes in light intensity: role of light-harvesting complex II protein dephosphorylation in high light. Plant Physiology 168, 721–734.
| Plants actively avoid state transitions upon changes in light intensity: role of light-harvesting complex II protein dephosphorylation in high light.Crossref | GoogleScholarGoogle Scholar | 25902812PubMed |
Minagawa J (2011) State transitions-the molecular remodeling of photosynthetic supercomplexes that controls energy flow in the chloroplast. Biochimica et Biophysica Acta 1807, 897–905.
| State transitions-the molecular remodeling of photosynthetic supercomplexes that controls energy flow in the chloroplast.Crossref | GoogleScholarGoogle Scholar | 21108925PubMed |
Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M, Shikanai T (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110, 361–371.
| PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 12176323PubMed |
Murata N (1969) Control of excitation transfer in photosynthesis I. Light-induced change of chlorophyll a fluorescence in Porphyridium cruenatum. Biochimica et Biophysica Acta 172, 242–251.
| Control of excitation transfer in photosynthesis I. Light-induced change of chlorophyll a fluorescence in Porphyridium cruenatum.Crossref | GoogleScholarGoogle Scholar | 5775694PubMed |
Murata N (2009) The discovery of state transitions in photosynthesis 40 years ago. Photosynthesis Research 99, 155–160.
| The discovery of state transitions in photosynthesis 40 years ago.Crossref | GoogleScholarGoogle Scholar | 19037742PubMed |
Nawrocki WJ, Santabarbara S, Mosebach L, Wollman F-A, Rappaport F (2016) State transitions redistribute rather than dissipate energy between two photosystems in Chlamydomonas. Nature Plants 2, 16031
| State transitions redistribute rather than dissipate energy between two photosystems in Chlamydomonas.Crossref | GoogleScholarGoogle Scholar | 27249564PubMed |
Niyogi KK, Grossman AR, Björkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in regulation of photosynthetic energy conversion. The Plant Cell 10, 1121–1134.
| Arabidopsis mutants define a central role for the xanthophyll cycle in regulation of photosynthetic energy conversion.Crossref | GoogleScholarGoogle Scholar | 9668132PubMed |
Osmond B, Chow WS, Wyber R, Zavaleta A, Keller B, Pogson BJ, Robinson SA (2017) Relative functional and optical absorption cross sections of PSII and other photosynthetic parameters monitored in situ, at a distance with a time resolution of a few seconds, using a prototype light induced fluorescence transient (LIFT) device. Functional Plant Biology 44, 985–1006.
| Relative functional and optical absorption cross sections of PSII and other photosynthetic parameters monitored in situ, at a distance with a time resolution of a few seconds, using a prototype light induced fluorescence transient (LIFT) device.Crossref | GoogleScholarGoogle Scholar |
Pesaresi P, Hertle A, Pribil M, Kleine T, Wagner R, Strissel H, Ihnatowicz A, Bonardi V, Scharfenberg M, Schneider T, Pfannschmidt T, Leister D (2009) Arabidopsis STN7 kinase provides a link between short- and long-term photosynthetic acclimation. The Plant Cell 21, 2402–2423.
| Arabidopsis STN7 kinase provides a link between short- and long-term photosynthetic acclimation.Crossref | GoogleScholarGoogle Scholar | 19706797PubMed |
Pfündel E (2007) ‘JUNIOR-PAM chlorophyll fluorometer operators guide.’ (H Walz GmbH: Effeltrich, Germany)
Prášil O, Kolber ZS, Falkowski PG (2018) Control of the maximum chlorophyll fluorescence yield by the Q B binding site. Photosynthetica 56, 150–162.
| Control of the maximum chlorophyll fluorescence yield by the Q B binding site.Crossref | GoogleScholarGoogle Scholar |
Rantala S, Tikkanen M (2018) Phosphorylation-induced lateral rearrangements of thylakoid protein complexes upon light acclimation. Plant Direct 2, e00039
| Phosphorylation-induced lateral rearrangements of thylakoid protein complexes upon light acclimation.Crossref | GoogleScholarGoogle Scholar |
Rantala M, Tikkanen M, Aro E-M (2017) Proteomic characterization of hierarchical megacomplex formation in Arabidopsis thylakoid membrane. The Plant Journal 92, 951–962.
| Proteomic characterization of hierarchical megacomplex formation in Arabidopsis thylakoid membrane.Crossref | GoogleScholarGoogle Scholar | 28980426PubMed |
Rochaix J-D (2014) Regulation and dynamics of the light-harvesting system. Annual Review of Plant Biology 65, 287–309.
| Regulation and dynamics of the light-harvesting system.Crossref | GoogleScholarGoogle Scholar | 24471838PubMed |
Ruban AV, Johnson MP (2009) Dynamics of higher plant photosystem cross-section associated with state transitions. Photosynthesis Research 99, 173–183.
| Dynamics of higher plant photosystem cross-section associated with state transitions.Crossref | GoogleScholarGoogle Scholar | 19037743PubMed |
Ruban AV, Wentworth M, Yakushevska AE, Keegstra W, Lee PJ, Dekker JP, Jansson S, Boekema E, Horton P (2003) Plants lacking the main light-harvesting complex retain photosystem II macro-organisation. Nature 421, 648–652.
| Plants lacking the main light-harvesting complex retain photosystem II macro-organisation.Crossref | GoogleScholarGoogle Scholar | 12571599PubMed |
Ruban AV, Solovieva S, Lee PJ, Iiloaia C, Wentworth M, Ganeteg U, Klimmek F, Chow WS, Anderson JM, Jansson S, Horton P (2006) Plasticity in the composition of the light-harvesting antenna of higher plants preserves structural integrity and biological function. Journal of Biological Chemistry 281, 14981–14990.
| Plasticity in the composition of the light-harvesting antenna of higher plants preserves structural integrity and biological function.Crossref | GoogleScholarGoogle Scholar | 16551629PubMed |
Schansker G, Tóth SZ, Holzwarth AR, Garab G (2014) Chlorophyll a fluorescence: beyond the limits of the QA model. Photosynthesis Research 120, 43–58.
| Chlorophyll a fluorescence: beyond the limits of the QA model.Crossref | GoogleScholarGoogle Scholar | 23456268PubMed |
Stirbet A, Govindjee (2012) Chlorophyll a fluorescence induction: a personal perspective of the thermal phase. Photosynthesis Research 113, 15–61.
| Chlorophyll a fluorescence induction: a personal perspective of the thermal phase.Crossref | GoogleScholarGoogle Scholar | 22810945PubMed |
Suggett DJ, MacIntyre HL, Geider RJ (2004) Evaluation of optical determinations of light absorption of photosystem II in phytoplankton. Limnology and Oceanography, Methods 2, 316–332.
| Evaluation of optical determinations of light absorption of photosystem II in phytoplankton.Crossref | GoogleScholarGoogle Scholar |
Suorsa M, Rantala M, Mamedov F, Lespinasse M, Trotta A, Grieco M, Vuorio E, Tikkanen M, Jävi S, Aro E-M (2015) Light acclimation involves dynamic re-organisation of the pigment-protein megacomplexes in non-appressed thylakoid domains. The Plant Journal 84, 360–373.
| Light acclimation involves dynamic re-organisation of the pigment-protein megacomplexes in non-appressed thylakoid domains.Crossref | GoogleScholarGoogle Scholar | 26332430PubMed |
Tikkanen M, Aro E-M (2014) Integrative regulatory network of plant thylakoid energy transduction. Trends in Plant Science 19, 10–17.
| Integrative regulatory network of plant thylakoid energy transduction.Crossref | GoogleScholarGoogle Scholar | 24120261PubMed |
Tikkanen M, Nurmi M, Suorsa M, Danielsson R, Mamedov F, Styring S, Aro E-M (2008) Phosphorylation-dependent regulation of excitation energy distribution between two photosystems in higher plants. Biochimica et Biophysica Acta 1777, 425–432.
| Phosphorylation-dependent regulation of excitation energy distribution between two photosystems in higher plants.Crossref | GoogleScholarGoogle Scholar | 18331820PubMed |
Tikkanen M, Grieco M, Kangasjärvi S, Aro EM (2010) Thylakoid protein phosphorylation in higher plant chloroplasts optimises electron transfer under fluctuating light. Plant Physiology 152, 723–735.
| Thylakoid protein phosphorylation in higher plant chloroplasts optimises electron transfer under fluctuating light.Crossref | GoogleScholarGoogle Scholar | 19965965PubMed |
Tikkanen M, Grieco M, Aro E-M (2011) Novel insights into light-harvesting complex II phosphorylation and ‘state transitions’. Trends in Plant Science 16, 126–131.
| Novel insights into light-harvesting complex II phosphorylation and ‘state transitions’.Crossref | GoogleScholarGoogle Scholar | 21183394PubMed |
Ünlü C, Drop B, Croce R, van Amerongen H (2014) State transitions in Chlamydomonas reinhardtii strongly modulate the functional size of photosystem II but not of photosystem I. Proceedings of the National Academy of Sciences of the United States of America 111, 3460–3465.
| State transitions in Chlamydomonas reinhardtii strongly modulate the functional size of photosystem II but not of photosystem I.Crossref | GoogleScholarGoogle Scholar | 24550508PubMed |
Wang RT, Myers J (1974) On the state 1–state 2 phenomenon in photosynthesis. Biochimica et Biophysica Acta 347, 134–140.
| On the state 1–state 2 phenomenon in photosynthesis.Crossref | GoogleScholarGoogle Scholar | 4433555PubMed |
Wientjes E, van Amerongen H, Croce R (2013a) LHCII is an antenna of both photosystems after long term acclimation. Biochimica et Biophysica Acta 1827, 420–426.
| LHCII is an antenna of both photosystems after long term acclimation.Crossref | GoogleScholarGoogle Scholar | 23298812PubMed |
Wientjes E, van Amerongen H, Croce R (2013b) Quantum yield of changes in photosystem II: effect of changes in antenna size upon light acclimation. The Journal of Physical Chemistry B 117, 11200–11208.
| Quantum yield of changes in photosystem II: effect of changes in antenna size upon light acclimation.Crossref | GoogleScholarGoogle Scholar | 23534376PubMed |
Wyber RA, Malenovsky Z, Ashcroft MB, Osmond B, Robinson SA (2017) Do daily and seasonal trends in leaf solar induced fluorescence reflect changes in photosynthesis, growth or light exposure? Remote Sensing 9, 1–19.
Wyber RA, Osmond B, Ashcroft MB, Malenovsky Z, Robinson SA (2018) Remote monitoring of dynamic canopy photosynthesis with high time resolution light-induced fluorescence transients. Tree Physiology 38, 1302–1318.
| Remote monitoring of dynamic canopy photosynthesis with high time resolution light-induced fluorescence transients.Crossref | GoogleScholarGoogle Scholar |
Yokono M, Takabayashi A, Akimoto S, Tanaka A (2015) A megacomplex composed of both photosystem reaction centres in higher plants. Nature Communications 6, 6675
| A megacomplex composed of both photosystem reaction centres in higher plants.Crossref | GoogleScholarGoogle Scholar | 25809225PubMed |
