Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

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

Barry Osmond A B D , Wah Soon Chow B , Rhys Wyber A , Alonso Zavafer B , Beat Keller C , 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, Australian National University, Acton, ACT 2601, Australia.

C Institute of Bio- and Geosciences, IBG-2: Plant Sciences, Forschungszentrum Jülich GmbH, 52425 Jülich, Germany.

D Corresponding author. Email: osmond.barry@gmail.com

Functional Plant Biology 44(10) 985-1006 https://doi.org/10.1071/FP17024
Submitted: 23 January 2017  Accepted: 12 June 2017   Published: 21 July 2017

Abstract

The prototype light-induced fluorescence transient (LIFT) instrument provides continuous, minimally intrusive, high time resolution (~2 s) assessment of photosynthetic performance in terrestrial plants from up to 2 m. It induces a chlorophyll fluorescence transient by a series of short flashes in a saturation sequence (180 ~1μs flashlets in <380 μs) to achieve near-full reduction of the primary acceptor QA, followed by a relaxation sequence (RQA; 90 flashlets at exponentially increasing intervals over ~30 ms) to observe kinetics of QA re-oxidation. When fitted by the fast repetition rate (FRR) model (Kolber et al. 1998) the QA flash of LIFT/FRR gives smaller values for FmQA from dark adapted leaves than FmPAM from pulse amplitude modulated (PAM) assays. The ratio FmQA/FmPAM resembles the ratio of fluorescence yield at the J/P phases of the classical O-J-I-P transient and we conclude that the difference simply is due to the levels of PQ pool reduction induced by the two techniques. In a strong PAM-analogous WL pulse in the dark monitored by the QA flash of LIFT/FRR φPSIIWLφPSIIPAM. The QA flash also tracks PQ pool reduction as well as the associated responses of ETR QA → PQ and PQ → PSI, the relative functional (σPSII) and optical absorption (aPSII) cross-sections of PSII in situ with a time resolution of ~2 s as they relax after the pulse. It is impractical to deliver strong WL pulses at a distance in the field but a longer PQ flash from LIFT/FRR also achieves full reduction of PQ pool and delivers φPSIIPQφPSIIPAM to obtain PAM-equivalent estimates of ETR and NPQ at a distance. In situ values of σPSII and aPSII from the QA flash with smaller antenna barley (chlorina-f2) and Arabidopsis mutants (asLhcb212, ch13 Lhcb5) are proportionally similar to those previously reported from in vitro assays. These direct measurements are further validated by changes in antenna size in response to growth irradiance. We illustrate how the QA flash facilitates our understanding of photosynthetic regulation during sun flecks in natural environments at a distance, with a time resolution of a few seconds.

Additional keywords: Arabidopsis mutants, avocado, barley mutants, electron transfer rates, NPQ, O-J-I-P transient.


References

Adams WW, Demmig-Adams B, Logan BA, Barker DH, Osmond CB (1999) Rapid change in xanthophyll cycle-dependent energy dissipation and photosystem II efficiency in two vines: Stephania japonica and Smilax australis, growing in the understorey of an open Eucalyptus forest. Plant, Cell & Environment 22, 125–136.
Rapid change in xanthophyll cycle-dependent energy dissipation and photosystem II efficiency in two vines: Stephania japonica and Smilax australis, growing in the understorey of an open Eucalyptus forest.CrossRef | 1:CAS:528:DyaK1MXislaqu7o%3D&md5=ef0c0f4edb6cd4efa7ae921a60c4f770CAS |

Ananyev G, Kolber ZS, Klimov D, Falkowski PG, Berry JA, Rascher U, Martin R, Osmond B (2005) Remote sensing of heterogeneity in photosynthetic efficiency, electron transport and dissipation of excess light in Populus deltoides stands under ambient and elevated CO2 concentrations, and in a tropical forest canopy, using a new laser-induced fluorescence transient (LIFT) device. Global Change Biology 11, 1195–1206.
Remote sensing of heterogeneity in photosynthetic efficiency, electron transport and dissipation of excess light in Populus deltoides stands under ambient and elevated CO2 concentrations, and in a tropical forest canopy, using a new laser-induced fluorescence transient (LIFT) device.CrossRef |

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 | 1:CAS:528:DC%2BD3sXnsVCjs7o%3D&md5=8932b94d97026400dcd01f23de36beedCAS |

Apostol S, Briantais JM, Moise N, Cerovic Z, Moya I (2001) Photoinactivation of the photosynthetic electron transport chain by accumulation of over-saturating light pulses given to dark adapted pea leaves. Photosynthesis Research 67, 215–227.
Photoinactivation of the photosynthetic electron transport chain by accumulation of over-saturating light pulses given to dark adapted pea leaves.CrossRef | 1:CAS:528:DC%2BD3MXlsVemsb0%3D&md5=116a37e14189d1aa8c948628cd77ace3CAS |

Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annual Review of Plant Biology 59, 89–113.
Chlorophyll fluorescence: a probe of photosynthesis in vivo.CrossRef | 1:CAS:528:DC%2BD1cXntFaqsL8%3D&md5=2e931356ff6efeac700a0aa61c516f11CAS |

Ballottari M, Dall’Osto L, Morosinotto T, Bassi R (2007) Contrasting behaviour of higher plant photosystem I and II antenna systems during acclimation. The Journal of Biological Chemistry 282, 8947–8958.
Contrasting behaviour of higher plant photosystem I and II antenna systems during acclimation.CrossRef | 1:CAS:528:DC%2BD2sXivV2msbc%3D&md5=9b14a595dd60bfe04c86a6f27fa81f5aCAS |

Belgio E, Kapitonova E, Chemliov J, Duffy CDP, Ungerer P, Valkunasw L, Ruban AV (2014) Economic photoprotection in photosystem II that retains a complete light-harvesting system with slow energy traps. Nature Communications 5, 4433
Economic photoprotection in photosystem II that retains a complete light-harvesting system with slow energy traps.CrossRef | 1:CAS:528:DC%2BC2cXitVaksLjE&md5=e5b6918cb6b873827a7618d8d954a15eCAS |

Bilger W, Björkman O (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes fluorescence and photosynthesis in leaves of Hedra canariensis. Photosynthesis Research 25, 173–185.
Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes fluorescence and photosynthesis in leaves of Hedra canariensis.CrossRef | 1:CAS:528:DyaK3cXmtVymsbs%3D&md5=b46e638919aa989323367dd49512e865CAS |

Björkman O, Boardman NK, Anderson JM, Thorne SW, Goodchild DJ, Pyliotis NA (1972) Effect of light intensity during growth of Atriplex patula on the capacity of photosynthetic reactions, chloroplast components and structure. Carnegie Institution of Washington Year Book 71, 115–135.

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 | 1:CAS:528:DC%2BD2MXhtFahtL%2FN&md5=3a02e48a4b890452144e81b26fcebda0CAS |

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 | 1:CAS:528:DyaK2sXmtFSktL0%3D&md5=5b6b18990d5aaf9e9c58ca0460f03facCAS |

Bradbury M, Baker NR (1981) Analysis of the slow phase of the in vivo chlorophyll fluorescence induction curve. Changes in the redox state of photosystem II electron acceptors and fluorescence emission from photosystem I. Biochimica et Biophysica Acta 635, 542–551.
Analysis of the slow phase of the in vivo chlorophyll fluorescence induction curve. Changes in the redox state of photosystem II electron acceptors and fluorescence emission from photosystem I.CrossRef | 1:CAS:528:DyaL3MXitVGlsr8%3D&md5=10748520fd4a4860f846c1bda28491dfCAS |

Briantais J-M, Vernotte C, Picaud M, Krause GH (1979) A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts. Biochimica et Biophysica Acta 548, 128–138.
A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts.CrossRef | 1:CAS:528:DyaE1MXlvV2qtrs%3D&md5=e9257688735a402fb06c5feb3749cd8fCAS |

Cerovic ZG, Goulas Y, Gorbunov M, Briantais J-M, Camenen L, Moya I (1996) Fluorosensing of water stress in plants; yield of chlorophyll fluorescence measured simultaneously and at a distance with a τ-LIDAR and a modified PAM-fluorimeter in maize, sugar-beet and Kalanchoe. Remote Sensing of Environment 58, 311–321.
Fluorosensing of water stress in plants; yield of chlorophyll fluorescence measured simultaneously and at a distance with a τ-LIDAR and a modified PAM-fluorimeter in maize, sugar-beet and Kalanchoe.CrossRef |

Chappelle EW, Wood FM, McMurtrey JE, Newcomb WW (1984) Laser-induced fluorescence of green plants. 1: A technique for the remote detection of plant stress and species differentiation. Applied Optics 23, 134–138.
Laser-induced fluorescence of green plants. 1: A technique for the remote detection of plant stress and species differentiation.CrossRef | 1:CAS:528:DyaL2cXmsVertg%3D%3D&md5=fafd6d7160e81546ee0f63b533ee88f8CAS |

Chow WS, Anderson JM (1987) Photosynthetic responses of Pisum sativum to an increase in irradiance in growth I. Photosynthetic activities. Australian Journal of Plant Physiology 14, 1–8.
Photosynthetic responses of Pisum sativum to an increase in irradiance in growth I. Photosynthetic activities.CrossRef | 1:CAS:528:DyaL2sXhvFejt78%3D&md5=296ba632511e3f61d9cc5a3acdca7a12CAS |

Cleland RE, Melis A (1987) Probing the events of photoinhibition by altering electron-transport activity and light-harvesting capacity in chloroplast thylakoids. Plant, Cell & Environment 10, 747–752.

Duysens LNM, Sweers HE (1963) Mechanisms of two photochemical reactions in algae as studied by means of fluorescence. In ‘Studies on microalgae and photosynthetic bacteria’. (Eds Japanese Society of Plant Physiologists) pp. 353–372. (University of Tokyo Press: Tokyo)

Falkowski PG, Kolber Z (1995) Variations in chlorophyll fluorescence yields in phytoplankton in world oceans. Australian Journal of Plant Physiology 22, 341–355.
Variations in chlorophyll fluorescence yields in phytoplankton in world oceans.CrossRef |

Flexas J, Briantis J-M, Cerovic Z, Medrano H, Moya I (2000) Steady-state and maximum chlorophyll fluorescence responses to water stress in grapevine leaves: a new remote sensing system. Remote Sensing of Environment 73, 283–297.
Steady-state and maximum chlorophyll fluorescence responses to water stress in grapevine leaves: a new remote sensing system.CrossRef |

Förster B, Osmond CB, Pogson BJ (2011) Lutein from de-epoxidation of lutein epoxide replaces zeaxanthin to sustain enhanced capacity for non-photochemical chlorophyll fluorescence quenching in avocado shade leaves in the dark. Plant Physiology 156, 393–403.
Lutein from de-epoxidation of lutein epoxide replaces zeaxanthin to sustain enhanced capacity for non-photochemical chlorophyll fluorescence quenching in avocado shade leaves in the dark.CrossRef |

Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87–92.
The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence.CrossRef | 1:CAS:528:DyaL1MXhsFWntL4%3D&md5=ca3f55cdd9fa28062542f823d0b95a3aCAS |

Goltsev V, Zaharieva I, Chernev P, Strasser RJ (2009) Delayed fluorescence in photosynthesis. Photosynthesis Research 101, 217–232.
Delayed fluorescence in photosynthesis.CrossRef | 1:CAS:528:DC%2BD1MXhtFaqt7zN&md5=f6d7aa90caafdf9383c94a73898e01beCAS |

Goral TK, Johnson MP, Duffy CDP, Brain APR, Ruban AV, Mullineaux CP (2012) Light harvesting antenna composition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis. The Plant Journal 69, 289–301.
Light harvesting antenna composition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis.CrossRef | 1:CAS:528:DC%2BC38XhsFyntr4%3D&md5=6f0de9f6af6c2c7508195cc1470e1e30CAS |

Gorbunov MY, Kolber ZS, Falkowski PG (2000) Measurement of photosynthetic parameters in benthic organisms in situ using a SCUBA-based fast repetition rate fluorometer. Limnology and Oceanography 45, 242–245.
Measurement of photosynthetic parameters in benthic organisms in situ using a SCUBA-based fast repetition rate fluorometer.CrossRef |

Govindjee (1995) Sixty three years since Kautsky. Australian Journal of Plant Physiology 22, 131–160.
Sixty three years since Kautsky.CrossRef | 1:CAS:528:DyaK2MXmt1Oju7Y%3D&md5=b3c3b9972bbafaa8c6516c5e27f532b9CAS |

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 | 1:CAS:528:DyaK2cXhsF2is78%3D&md5=b44da69f2708dc9d32fa3023429bf5e9CAS |

Highkin HR (1950) Chlorophyll studies on barley mutants. Plant Physiology 25, 294–306.
Chlorophyll studies on barley mutants.CrossRef | 1:CAS:528:DyaG3cXjtlOktQ%3D%3D&md5=b64f463fe982c1f6215d0e098303ae0dCAS |

Jacquemoud S, Ustin SL, Verdebout J, Schmuk G, Andreoli G, Hosgood B (1996) Estimating leaf biochemistry using the PROSPECT leaf optical properties model. Remote Sensing of Environment 56, 194–202.
Estimating leaf biochemistry using the PROSPECT leaf optical properties model.CrossRef |

Jia HS, Förster B, Chow WS, Pogson BJ, Osmond CB (2013) Decreased photochemical efficiency of photosystem II following sunlight exposure of shade-grown leaves of avocado (Persea americana Mill.): because of, or in spite of, two kinetically distinct xanthophyll cycles? Plant Physiology 161, 836–852.
Decreased photochemical efficiency of photosystem II following sunlight exposure of shade-grown leaves of avocado (Persea americana Mill.): because of, or in spite of, two kinetically distinct xanthophyll cycles?CrossRef | 1:CAS:528:DC%2BC3sXmvFKqsL4%3D&md5=03fee5d80ebe173e60e16cca6e88b314CAS |

Kalaji HM, Schansker G, Brestic M, Bussotti F, Calatayud A, Ferroni L, Goltsev V, Guidi L, Jajoo A, Li P, et al. (2017) Frequently asked questions about fluorescence, the sequel. Photosynthesis Research 132, 13–66.
Frequently asked questions about fluorescence, the sequel.CrossRef | 1:CAS:528:DC%2BC28XhvVShsr%2FI&md5=dd260bd5e3e3310d5fa605c4aaa1b2bfCAS |

Kautsky H, Hirsch A (1931) Neue Versuche zur Kohlensäureassimilation. Naturwissenschaften 19, 964
Neue Versuche zur Kohlensäureassimilation.CrossRef | 1:CAS:528:DyaA38XhsFaguw%3D%3D&md5=4d0618c55935177fd90d1e447e5b6ee9CAS |

Kim E-H, Li X-P, Razeghifard R, Anderson JM, Niyogi KK, Pogson BJ, Chow WS (2009) The multiple roles of light-harvesting chlorophyll a/b-protein complexes define structure and optimize function of Arabidopsis chloroplasts: a study using two chlorophyll b-less mutants. Biochimica et Biophysica Acta 1787, 973–984.
The multiple roles of light-harvesting chlorophyll a/b-protein complexes define structure and optimize function of Arabidopsis chloroplasts: a study using two chlorophyll b-less mutants.CrossRef | 1:CAS:528:DC%2BD1MXnsFKru7k%3D&md5=31683c450c9b0aeba3f52cb13f8496d6CAS |

Kirschbaum MUF, Pearcy RW (1988a) Gas exchange analysis of the relative importance of stomatal and biochemical factors in photosynthetic induction in Alocasia macrorrhiza. Plant Physiology 86, 782–785.
Gas exchange analysis of the relative importance of stomatal and biochemical factors in photosynthetic induction in Alocasia macrorrhiza.CrossRef | 1:CAS:528:DyaL1cXitVWqtrY%3D&md5=d740f5c0e8ae4ea4c83f0abfa9737fd7CAS |

Kirschbaum MUF, Pearcy RW (1988b) Concurrent measurements of O2 and CO2 exchange during lightflecks in Alocasia macrorrhiza (L.) G. Don. Planta 174, 527–533.
Concurrent measurements of O2 and CO2 exchange during lightflecks in Alocasia macrorrhiza (L.) G. Don.CrossRef | 1:CAS:528:DyaL1cXkvV2qsLk%3D&md5=0832658b3ca0ddf169037f53000d7a9dCAS |

Klughammer C, Schreiber U (2015) Apparent PS II absorption cross-section and estimation of mean PAR in optically thin and dense suspensions of Chlorella. Photosynthesis Research 123, 77–92.
Apparent PS II absorption cross-section and estimation of mean PAR in optically thin and dense suspensions of Chlorella.CrossRef | 1:CAS:528:DC%2BC2cXhsFCisbvP&md5=cc10eb3211e1acf56d1a3f11c1d04b59CAS |

Kolber ZS, 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 | 1:CAS:528:DyaK2cXlvVKgurk%3D&md5=ec0094ba4d59123c2838e1c7923af076CAS |

Kolber Z, Zehr J, Falkowski PG (1988) Effects of growth irradiance and nitrogen limitation on photosynthetic energy conservation in photosystem II. Plant Physiology 88, 923–929.
Effects of growth irradiance and nitrogen limitation on photosynthetic energy conservation in photosystem II.CrossRef | 1:CAS:528:DyaL1MXkvV2j&md5=b4bb090b27bd25e48f88490f735cfc64CAS |

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 - Bioenergetics 1367, 88–106.
Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols.CrossRef | 1:CAS:528:DyaK1cXmslOgsrg%3D&md5=aeeab1996d48f3626141ddad0d1fa62bCAS |

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 | 1:CAS:528:DC%2BD2MXms1yitrs%3D&md5=2a5010b344c822dea253e552ad6675b8CAS |

Kouřil R, Wientjes E, Bultema JB, Croce R, Boekema EJ (2013) High-light vs. low-light acclimation on photosystem II composition and organization in Arabidopsis thaliana. Biochimica et Biophysica Acta 1827, 411–419.
High-light vs. low-light acclimation on photosystem II composition and organization in Arabidopsis thaliana.CrossRef |

Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annual Review of Plant Physiology and Plant Molecular Biology 42, 313–349.
Chlorophyll fluorescence and photosynthesis: the basics.CrossRef | 1:CAS:528:DyaK3MXltFSmsrc%3D&md5=df054e10a7abad6863ea4db172fdc469CAS |

Laisk A, Oja V (1998) Dynamics of leaf photosynthesis: rapid-response measurements and their interpretation. CSIRO Publishing: Melbourne)

Lavorel J, Etienne A-L (1977) In vivo chlorophyll fluorescence. In ‘Primary processes in photosynthesis’. (Ed. J Barber) pp. 203–268. (Elsevier/North Holland Biomedical Press: Amsterdam)

Leigh LS, Burgess T, Marino DVB, Wei YD (1999) Tropical forest biome of Biosphere 2: structure, composition and results of the first 2 years of operation. Ecological Engineering 13, 65–93.
Tropical forest biome of Biosphere 2: structure, composition and results of the first 2 years of operation.CrossRef |

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 | 1:CAS:528:DyaL38XhsF2msbo%3D&md5=092087cc1b01f170a25f2f342a92d44bCAS |

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 | 1:CAS:528:DC%2BD38Xpt1yqtbY%3D&md5=b35cf220c703d503407720b2e7f6f76bCAS |

MacAlister EC, Myers J (1940) The time course of photosynthesis and fluorescence measured simultaneously. Smithsonian Institution Miscellaneous Collection 99, 1–37.

Malkin S, Fork DC (1981) Photosynthetic units of sun and shade plants. Plant Physiology 67, 580–583.
Photosynthetic units of sun and shade plants.CrossRef | 1:CAS:528:DyaL3MXhsFelsL0%3D&md5=fe7021cea44e8c6efd9ee4bd6497d3acCAS |

Matsubara S, Morosinotto T, Osmond CB, Bassi R (2007) Short- and long-term operation of the lutein-epoxide cycle in light-harvesting antenna complexes. Plant Physiology 144, 926–941.
Short- and long-term operation of the lutein-epoxide cycle in light-harvesting antenna complexes.CrossRef | 1:CAS:528:DC%2BD2sXmvValt7k%3D&md5=8f2d21fb7cfd72c6d72f6802bcbdef2dCAS |

Matsubara S, Chen Y-C, Caliandro R, Govindjee , Clegg RM (2011) Photosystem II fluorescence lifetime imaging in avocado leaves: contributions of the lutein epoxide and violaxanthin cycles to fluorescence quenching. Journal of Photochemistry and Photobiology. B, Biology 104, 271–284.
Photosystem II fluorescence lifetime imaging in avocado leaves: contributions of the lutein epoxide and violaxanthin cycles to fluorescence quenching.CrossRef | 1:CAS:528:DC%2BC3MXntFWjsLg%3D&md5=d2a78b1294a99cdf4ac0c314244f1e07CAS |

Matsubara S, Förster B, Waterman M, Robinson SA, Pogson BJ, Gunning B, Osmond B (2012) From ecophysiology to phenomics: some implications of photoprotection and shade-sun acclimation in situ for dynamics of thylakoids in vitro. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 367, 3503–3514.
From ecophysiology to phenomics: some implications of photoprotection and shade-sun acclimation in situ for dynamics of thylakoids in vitro.CrossRef | 1:CAS:528:DC%2BC3sXosVaktw%3D%3D&md5=4dd87cb034f4a7ef737678f0102a24beCAS |

Maxwell K, Johnson GN (2000) Chlorophyll fluorescence – a practical guide. Journal of Experimental Botany 51, 659–668.

Melis A, Anderson JM (1983) Structural and functional organization of the photosystems in spinach chloroplasts. Antenna size, relative electron-transport capacity and chlorophyll composition. Biochimica et Biophysica Acta 724, 473–484.
Structural and functional organization of the photosystems in spinach chloroplasts. Antenna size, relative electron-transport capacity and chlorophyll composition.CrossRef | 1:CAS:528:DyaL3sXlvFWqs7s%3D&md5=09bbb9aa64125867143eee27ed688e4eCAS |

Melrose DC, Oviatt CA, O’Reilly JE, Berman MS (2006) Comparisons of fast repetition rate fluorescence estimated primary production and 14C uptake by phytoplankton. Marine Ecology Progress Series 311, 37–46.
Comparisons of fast repetition rate fluorescence estimated primary production and 14C uptake by phytoplankton.CrossRef |

Mishra Y, Jänkänpää HJ, Kiss AZ, Funk C, Schröeder WP, Jansson S (2012) Arabidopsis plants grown in the field and climate chambers differ significantly in leaf morphology and photosystem components. BMC Plant Biology 12, 6
Arabidopsis plants grown in the field and climate chambers differ significantly in leaf morphology and photosystem components.CrossRef | 1:CAS:528:DC%2BC38XkvVyjsLc%3D&md5=49a1bf9befd31080d4a72de2dbf611c6CAS |

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 | 1:CAS:528:DC%2BD38Xmtl2rs78%3D&md5=01a7372b2203b50eda07bae81d851684CAS |

Nichol CJ, Pieruschka R, Takayama K, Förster B, Kolber Z, Rascher U, Grace J, Robinson SA, Pogson B, Osmond B (2012) Canopy conundrums: building on the Biosphere 2 experience to scale measurements of inner and outer canopy photoprotection from the leaf to the landscape. Functional Plant Biology 39, 1–24.
Canopy conundrums: building on the Biosphere 2 experience to scale measurements of inner and outer canopy photoprotection from the leaf to the landscape.CrossRef |

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 | 1:CAS:528:DyaK1cXkvFejt7w%3D&md5=581f58a5077ae91b342d6caaf5d8bb53CAS |

Oguchi R, Hikosaka K, Hirose T (2005) Leaf anatomy as a constraint for photosynthetic acclimation: differential responses in leaf anatomy to increasing growth irradiance among three deciduous species. Plant, Cell & Environment 28, 916–927.
Leaf anatomy as a constraint for photosynthetic acclimation: differential responses in leaf anatomy to increasing growth irradiance among three deciduous species.CrossRef |

Ounis A, Evian S, Flexas J, Tosti S, Moya A (2001) Adaptation of a PAM-fluorometer for remote sensing of chlorophyll fluorescence. Photosynthesis Research 68, 113–120.
Adaptation of a PAM-fluorometer for remote sensing of chlorophyll fluorescence.CrossRef | 1:CAS:528:DC%2BD3MXnslGkur8%3D&md5=c6b599a06b9f22ab64bd1013c7360d3aCAS |

Oxborough K, Moore CM, Suggett DJ, Lawson T, Chan HG, Geider RJ (2012) Direct estimation of functional PSII reaction centre concentration and PSII electron flux on a volume basis: a new approach to the analysis of fast repetition rate fluorometry (FRR) data. Limnology and Oceanography, Methods 10, 142–154.
Direct estimation of functional PSII reaction centre concentration and PSII electron flux on a volume basis: a new approach to the analysis of fast repetition rate fluorometry (FRR) data.CrossRef |

Papageorgiou G, Govindjee (1968) Light-induced changes in the fluorescence yield of chlorophyll a in vivo. II Chlorella pyrenoidosa. Biophysical Journal 8, 1316–1328.
Light-induced changes in the fluorescence yield of chlorophyll a in vivo. II Chlorella pyrenoidosa.CrossRef | 1:CAS:528:DyaF1MXksFWnug%3D%3D&md5=cf67a7bc786d9bb6fc527a47dd2d82d2CAS |

Pearcy RW (1990) Sunflecks and photosynthesis in plant canopies. Annual Review of Plant Physiology and Plant Molecular Biology 41, 421–453.
Sunflecks and photosynthesis in plant canopies.CrossRef | 1:CAS:528:DyaK3cXksFGku78%3D&md5=e8b94a0fe76dba981a87db46e098d82eCAS |

Pearcy RW, Way DA (2012) Two decades of sunfleck research: looking back to move forward. Tree Physiology 32, 1059–1061.
Two decades of sunfleck research: looking back to move forward.CrossRef |

Pieruschka R, Klimov D, Kolber ZS, Berry JA (2010) Monitoring of cold and light stress impact on photosynthesis by using the laser induced fluorescence transient (LIFT) approach. Functional Plant Biology 37, 395–402.
Monitoring of cold and light stress impact on photosynthesis by using the laser induced fluorescence transient (LIFT) approach.CrossRef |

Pieruschka R, Albrecht H, Muller O, Berry JA, Klimov D, Kolber ZS, Malenovsky Z, Rascher U (2014) Daily and seasonal dynamics of remotely sensed photosynthetic efficiency in tree canopies. Tree Physiology 34, 674–685.
Daily and seasonal dynamics of remotely sensed photosynthetic efficiency in tree canopies.CrossRef |

Porcar-Castell A, Pfündel E, Korhonen JFJ, Juurola E (2008) A new monitoring PAM fluorometer (MONI-PAM) to study the short-and long-term acclimation of photosystem II in field conditions. Photosynthesis Research 96, 173–179.
A new monitoring PAM fluorometer (MONI-PAM) to study the short-and long-term acclimation of photosystem II in field conditions.CrossRef | 1:CAS:528:DC%2BD1cXksVKks7w%3D&md5=3add26e09ed3144ad369539eca7b9e8aCAS |

Rascher U, Bobich EG, Lin G-H, Walter A, Morris T, Naumann M, Nichol CJ, Pierce D, Bil K, Kudeyarov V, Berry JA (2004) Functional diversity of photosynthesis during drought in model tropical rainforest the contributions of leaf area, photosynthetic electron transport and stomatal conductance to reduction in net ecosystem carbon exchange. Plant, Cell & Environment 27, 1239–1256.
Functional diversity of photosynthesis during drought in model tropical rainforest the contributions of leaf area, photosynthetic electron transport and stomatal conductance to reduction in net ecosystem carbon exchange.CrossRef | 1:CAS:528:DC%2BD2cXhtVSksb7N&md5=560f1c5e9f47a7c9fecdf5f80ea87535CAS |

Schansker G, Tórh 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 | 1:CAS:528:DC%2BC2cXkslertLw%3D&md5=1f302a71bcb00c9f133426d10a6c43c2CAS |

Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynthesis Research 10, 51–62.
Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer.CrossRef | 1:CAS:528:DyaL2sXktlGrsbY%3D&md5=216e6e8bb6bdb5b23a58def8c5ac4a74CAS |

Schreiber U, Klughammer C, Kolbowski J (2012) Assessment of wavelength-dependent parameters of photosynthetic electron transport with a new type of multi-color PAM chlorophyll fluorometer. Photosynthesis Research 113, 127–144.
Assessment of wavelength-dependent parameters of photosynthetic electron transport with a new type of multi-color PAM chlorophyll fluorometer.CrossRef | 1:CAS:528:DC%2BC38Xht1KmtbfJ&md5=8eebdde2477b8dd62ebcc3d62ae214c3CAS |

Smith WK, Berry ZC (2013) Sunflecks? Tree Physiology 32, 1062–1065.

Stirbet A, Govindjee (2012) Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the J–I–P rise. Photosynthesis Research 113, 15–61.
Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the J–I–P rise.CrossRef | 1:CAS:528:DC%2BC38Xht1Kmur%2FL&md5=d0a5fdbb9726f474c2925133104222cfCAS |

Strasser RJ, Srivastava A, Govindjee (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochemistry and Photobiology 61, 32–42.
Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria.CrossRef | 1:CAS:528:DyaK2MXjtFWmtr0%3D&md5=f9bf678fdb637606a444fb540c0f25d4CAS |

Strasser RJ, Tsimilli-Michael M, Qiang S, Goltsev V (2010) Simultaneous in vivo recording of prompt and delayed fluorescence and 820 nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochimica et Biophysica Acta 1797, 1313–1326.
Simultaneous in vivo recording of prompt and delayed fluorescence and 820 nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis.CrossRef | 1:CAS:528:DC%2BC3cXnvV2qsr0%3D&md5=f37daba4b11fbe8135186c4dfe13c5ccCAS |

Suggett DJ, Oxborough K, Baker NR, MacIntyre HL, Kanna TM, Geider RJ (2003) Fast repetition rate and pulse amplitude modulation chlorophyll a fluorescence measurements for assessment of photosynthetic electron transport in marine phytoplankton. European Journal of Phycology 38, 371–384.
Fast repetition rate and pulse amplitude modulation chlorophyll a fluorescence measurements for assessment of photosynthetic electron transport in marine phytoplankton.CrossRef |

Suggett DJ, MacIntyre HL, Kana TM, Geider RJ (2009) Comparing electron transport with gas exchange: parameterising exchange rates between alternative photosynthetic currencies for eukaryotic phytoplankton. Aquatic Microbial Ecology 56, 147–162.
Comparing electron transport with gas exchange: parameterising exchange rates between alternative photosynthetic currencies for eukaryotic phytoplankton.CrossRef |

Suorsa M, Järvi S, Grieco M, Nurmi M, Pietrzykowska M, Rantala M, Kangasjärvi S, Paakkarinen V, Tikkanen M, Jansson S, Aro E-M (2012) PROTON GRADIENT REGULATION5 is essential for proper acclimation of Arabidopsis photosystem I to naturally and artificially fluctuating light conditions. The Plant Cell 24, 2934–2948.
PROTON GRADIENT REGULATION5 is essential for proper acclimation of Arabidopsis photosystem I to naturally and artificially fluctuating light conditions.CrossRef | 1:CAS:528:DC%2BC38XhtlChsbzO&md5=c17f0a6d177c931a7701022b5c357adbCAS |

Terao T, Katoh S (1996) Antenna sizes of photosystem I and photosystem II in chlorophyll b-deficient mutants of rice. Evidence for an antenna function of photosystem II centers that are inactive in electron transport. Plant & Cell Physiology 37, 307–312.
Antenna sizes of photosystem I and photosystem II in chlorophyll b-deficient mutants of rice. Evidence for an antenna function of photosystem II centers that are inactive in electron transport.CrossRef | 1:CAS:528:DyaK28Xis12ksb8%3D&md5=869c84d7b18810ffa98f4bdb00047b36CAS |

Terashima I, Inoue I (1984) Comparative photosynthetic properties of palisade tissue chloroplasts and spongy tissue chloroplasts of Camellia japonica L.: ffunctional adjustment of the photosynthetic apparatus to light environment within a leaf. Plant & Cell Physiology 25, 555–563.

Tikkanen M, Pippo M, Suorsa M, Sirpiö S, Mulo P, Vainonen J, Vener AV, Allahverdiyeva Y, Aro E-M (2006) State transitions revisited: a buffering system for dynamic low light acclimation of Arabidopsis. Plant Molecular Biology 62, 779
State transitions revisited: a buffering system for dynamic low light acclimation of Arabidopsis.CrossRef |

Vredenberg W (2015) A simple routine for quantitative analysis of light and dark kinetics of photochemical and non-photochemical quenching of chlorophyll fluorescence in intact leaves. Photosynthesis Research 124, 87–106.
A simple routine for quantitative analysis of light and dark kinetics of photochemical and non-photochemical quenching of chlorophyll fluorescence in intact leaves.CrossRef | 1:CAS:528:DC%2BC2MXjvVGnsbw%3D&md5=23d91416a5cf011afdeca6ed32b9c375CAS |

Walker DA (1981) Secondary fluorescence kinetics of spinach leaves in relation to the onset of photosynthetic carbon assimilation. Planta 153, 273–278.
Secondary fluorescence kinetics of spinach leaves in relation to the onset of photosynthetic carbon assimilation.CrossRef | 1:CAS:528:DyaL38XjvVyj&md5=468f5bd519f7e285961a76d22926b529CAS |

Walker DA, Sivak MN, Cerovic ZG (1984) The relationships between photosynthetic carbon metabolism and chlorophyll a fluorescence. In ‘Advances in photosynthesis research Vol. III’. (Eds C Sybesma, M Nijhoff) pp. 645–648. (Dr W Junk Publishers: The Hague)

Ware MA, Belgio E, Ruban AV (2015) Photoprotective capacity of non-photochemical quenching in plants acclimated to different light intensities. Photosynthesis Research 126, 261–274.
Photoprotective capacity of non-photochemical quenching in plants acclimated to different light intensities.CrossRef | 1:CAS:528:DC%2BC2MXjt1Sgurw%3D&md5=3d1ed9c14f788f37e14a43834aad2ee3CAS |

Watling JR, Robinson SA, Woodrow IE, Osmond CB (1997) Responses of rainforest understorey plants to excess light during sunflecks. Australian Journal of Plant Physiology 24, 17–23.
Responses of rainforest understorey plants to excess light during sunflecks.CrossRef |

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 in press.



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