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Overview of Fluorescence Protocols: Theory, Basic Concepts, and Practice

  • Yannick Huot
  • Marcel Babin
Chapter
Part of the Developments in Applied Phycology book series (DAPH, volume 4)

Abstract

At the request of the editors, this chapter is based on the book section written by Babin (2008), however, much of the manuscript has been revised and updated to address different readerships. While Babin (2008) is aimed at a more general audience interested in understanding the basis of the measurement and the current instruments available, this chapter is aimed at those who will use the fluorescence tool and are interested in understanding more of its underlying theory, as well as the assumptions associated with it. In short, while the first chapter was aimed more at a beginning user, this one is aimed more at an intermediate user. Nevertheless, some sections have seen little changes.

Keywords

Quantum Yield Reaction Centre Photosynthetic Pigment Charge Separation Colored Dissolve Organic Matter 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

We are very thankful to John Cullen for sharing with us his insights on chlorophyll fluorescence over the years. This work was funded by a CNES grant to M. Babin and a CNES fellowship to Y. Huot.

References

  1. Abbott MR, Richerson PJ, Powell TM (1982) In situ response of phytoplankton fluorescence to rapid variations in light. Limnol Oceanogr 27:218–225Google Scholar
  2. Ahn TK et al (2008) Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science 320:794–797Google Scholar
  3. Aro E-M, Ohad I (2003) Redox regulation of thylakoid protein phosphorylation. Antioxidants and Redox Signaling 5:55–67Google Scholar
  4. Aro E-M, Soursa M, Rokka A, Allahverdiyeva Y, Paakkarinen V, Saleem A, battchikova N, Rintamäki E (2005) Dynamics of photosystem II: a proteomics approach to thylakoid protein complexes. J Exp Bot 56:347–356Google Scholar
  5. Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134Google Scholar
  6. Babin M (2008) Phytoplankton fluorescence: theory, current literature and in situ measurement. In: Babin M, Roesler CS, Cullen JJ (eds) Real-time coastal observing systems for marine ecosystem dynamics and harmful algal blooms. UNESCO Publishing, Paris. p 860Google Scholar
  7. Babin M, Morel A, Claustre H, Bricaud A, Kolber Z, Falkowski PG (1996a) Nitrogen- and irradiance-dependent variations of the maximum quantum yield of carbon fixation in eutrophic, mesotrophic and oligotrophic marine systems. Deep Sea Res I 43:1241–1272Google Scholar
  8. Babin M, Morel A, Gentili B (1996b) Remote sensing of sea surface sun-induced chlorophyll fluorescence: consequences of natural variations in the optical characteristics of phytoplankton and the quantum yield of chlorophyll a fluorescence. Int J Remote Sens 17:2417–2448Google Scholar
  9. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev PlantBiol 59:89–113Google Scholar
  10. Barber J (2006) Photosystem II: an enzyme of global significance. Biochem Soc Trans 34:619–631Google Scholar
  11. Bassi R, Pineau B, Dainese P, Marquardt J (1993) Carotenoid-binding proteins of photosystem II. Eur J Biochem 212:297–303Google Scholar
  12. Behrenfeld MJ, Bale AJ, Kolber ZS, Aiken J, Falkowski PG (1996) Confirmation of iron limitation of phytoplankton photosynthesis in the equatorial Pacific Ocean. Nature 383:508–511Google Scholar
  13. Behrenfeld MJ, Boss E (2006) Beam attenuation and chlorophyll concentration as alternative optical indices of phytoplankton biomass. J Mar Res 64:431–451Google Scholar
  14. Behrenfeld MJ, Kolber Z (1999) Widespread iron limitation of phytoplankton in the South Pacific Ocean. Science 283:840–843Google Scholar
  15. Behrenfeld MJ, Prasil O, Babin M, Bruyant F (2004) In search of a physiological basis for covariations in light-limited and light-saturated photosynthesis. J Phycol 40:4–25Google Scholar
  16. Behrenfeld MJ, Worthington K, Sherrell RM, Chavez FP, Strutton P, McPhaden M, Shea DM (2006) Controls on tropical Pacific Ocean productivity revealed through nutrient stress diagnostics. Nature 442:1025–1028Google Scholar
  17. Beutler M, Wiltshire KH, Arp M, Kruse J, Moldaenke C, Hansen UP (2003) A reduced model of the fluorescence from cyanobacterial photosynthetic apparatus designed for the in situ detection of cyanobacteria. Biochim Biophys Acta 1604:33–46Google Scholar
  18. Beutler M, Wiltshire KH, Meyer B, Moldaenke C, Lüring C, Meyerhöfer M, Hansen UP, Dau H (2002) A fluorometric method for the differentiation of algal populations in vivo and in situ. Photosynth Res 72:39–53Google Scholar
  19. Beutler M, Wiltshire KH, Reineke C, Hansen UP (2004) Algorithms and practical fluorescence models of the photosynthetic apparatus of red cyanobacteria and Cryptophyta designed for the fluorescence detection of red cyanobacteria and cryptophytes. Aquat Microb Ecol 35:115–129Google Scholar
  20. Bidigare RR, Ondrusek ME, Morrow JH, Kiefer DA (1990) In vivo absorption properties of algal pigments. In: Spinrad RW (ed) Ocean optics X. Proc SPIE 1302:290–302Google Scholar
  21. Blankenship RE (2002) Molecular mechanisms of photosynthesis. Blackwell Science, OxfordGoogle Scholar
  22. Boisvert S, Joly D, Carpentier R (2006) Quantitative analysis of the experimental O-J-I-P chlorophyll fluorescence induction kinetics. FEBS J 273:4770–4777Google Scholar
  23. Bricaud A, Claustre H, Ras J, Oubelkheir K (2004) Natural variability of phytoplankton absorption in oceanic waters: influence of the size structure of algal populations. J Geophys Res-Oceans 109:C11010. doi:11010.11029/12004JC002419Google Scholar
  24. Bricaud A, Morel A, Babin M, Allali K, Claustre H (1998) Variations of light absorption by suspended particles with the chlorophyll a concentration in oceanic (Case 1) waters: analysis and implications for bio-optical models. J Geophys Res-Oceans 103:31033–31044Google Scholar
  25. Bristow M, Nielsen D, Bundy D, Furtek R (1981) Use of water Raman emission to correct airborne laser fluorosensor data for effects of water optical attenuation. Appl Optics 20:2889–2906Google Scholar
  26. Browell EV (1977) Analysis of laser fluorosensor systems for remote algae detection and quantification. In: NASA technical note. National Aeronoutics and Space Administration, Washington, DC p 39Google Scholar
  27. Bruyant F, babin M, genty B, Prasil O, Behrenfeld MJ, Claustre H, Bricaud A, Garczarek L, Holtzendorff J, Koblizek M, Dousova H, Partensky F (2005) Diel variations in the photosynthetic parameters of Prochlorococcus strain PCC 9511: Combined effects of light and cell cycle. Limnol Oceanogr 50:850–863Google Scholar
  28. Bryant DA, Frigaard N-U (2006) Prokaryotic photosynthesis and phototrophy illuminated. Trends Microbiol 14:488–496Google Scholar
  29. Butler WL (1978) Energy distribution in the photochemical apparatus of photosynthesis. Annu Rev Plant Physiol 29:345–378Google Scholar
  30. Campbell D, Vaughan H, Clarke AK, Gustafsson P, Öquist G (1998) Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiol Mol Biol Rev 62:667–683Google Scholar
  31. Chamberlin WS, Booth CR, Kiefer DA, Morrow JH, Murphy RC (1990) Evidence for a simple relationship between natural fluorescence, photosynthesis and chlorophyll in the sea. Deep Sea Res 37:951–973Google Scholar
  32. Chekalyuk AM, Hafez M (2008) Advanced laser fluorometry of natural aquatic environments. Limnol Oceanogr Meth 6:591–609Google Scholar
  33. Chekalyuk AM, Hoge FE, Wright CW, Swift RN, Yungel JK (2000) Airborne test of laser pump-and-probe technique for assessment of phytoplankton photochemical characteristics. Photosynth Res 66:45–56Google Scholar
  34. Chow WS (2001) The photoinactivation of photosystem II in leaves: a personal perspective. J Photosci 2001:43–53Google Scholar
  35. Claustre H, Morel A, Babin M, Cailliau C, Marie D, Marty J-C, Taillez D, Vaulot D (1999) Variability in particle attenuation and chlorophyll fluorescence in the tropical Pacific: Scales, patterns, and biogeochemical implications. J Geophys Res 104:3401–3422Google Scholar
  36. Claustre H, Sciandra A, Vaulot D (2008) Introduction to the special section bio-optical and biogeochemical conditions in the South East Pacific in late 2004: the BIOSOPE program. Biogeosciences 5:679–691Google Scholar
  37. Clayton RK (1980) Photosynthesis. Cambridge University Press, CambridgeGoogle Scholar
  38. Collins DJ, Kiefer DA, SooHoo JB, McDermid IS (1985) The role of reabsorption in the spectral distribution of phytoplankton fluorescence emission. Deep Sea Res 32:983–1003Google Scholar
  39. Cowles TJ, Desiderio RA, Neuer S (1993) In situ characterization of phytoplankton from vertical profiles of fluorescence emission spectra. Mar Biol 115:217–222Google Scholar
  40. Cullen JJ, Davis RF (2003) The blank can make a big difference in oceanographic measurements. Limnol Oceanogr Bull 12:21–35Google Scholar
  41. Cullen JJ, Lewis MR (1995) Biological processes and optical measurements near the sea-surface: some issues relevant to remote sensing. J Geophys Res 100:13255–13266Google Scholar
  42. Cullen JJ, Renger EH (1979) Continuous measurement of the DCMU-induced fluorescence response of natural phytoplankton populations. Mar Biol 53:13–20Google Scholar
  43. Cullen JJ, Xiaolong Y, MacIntyre HL (1992) Nutrient limitation of marine photosynthesis. In: Falkowski PG (ed) Primary productivity and biogeochemical cycles in the sea. Plenum Press, NY, pp 69–88Google Scholar
  44. Cullen JJ, Yentsch CS, Cucci TL, MacIntyre HL (1988) Autofluorescence and other optical properties as tools in biological oceanography. Proc SPIE, Int Soci Opt Eng 925:149–156Google Scholar
  45. Dandonneau Y, Neveux J (1997) Diel variations of the in vivo fluorescence in the eastern equatorial Pacific: an unvarying pattern. Deep Sea Res II 44:1869–1880Google Scholar
  46. Demmig-Adams B, Adams WW III (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43:599–626Google Scholar
  47. Desiderio RA, Moore C, Lantz C, Cowles TJ (1997) Multiple excitation fluorometer for in situ oceanographic applications. Appl Optics 36:1289–1296Google Scholar
  48. Dubinsky Z, Falkowski PG, Wyman K (1986) Light Harvesting and utilization by phytoplankton. Plant Cell Physiol 27:1335–1349Google Scholar
  49. Exton RJ, Houghton WM, Esaias W, Harriss RC, Farmer FH, White HH (1983) Laboratory analysis of techniques for remote sensing of estuarine parameters using laser excitation. Appl Optics 22:54–64Google Scholar
  50. Falkowski PG, Fujita Y, Ley A, Mauzerall D (1986) Evidence for cyclic electron flow around photosystem-II in Chlorella pyrenoidosa. Plant Physiol 81:310–312Google Scholar
  51. Falkowski PG, Greene RM, Kolber Z (1995) Light utilization and photoinhibition of photosynthesis in marine phytoplankton. In: Baker NR, Bowyer JR (eds) Photoinhibition of photosynthesis from molecular mechanisms to the field Environmental plant biology. Bios Scientific Publishers, Oxford, pp 407–432Google Scholar
  52. Falkowski PG, Kiefer DA (1985) Chlorophyll a fluorescence in phytoplankton: relationship to photosynthesis and biomass. J Plankton Res 7:715–731Google Scholar
  53. Falkowski PG, LaRoche J (1991) Acclimation to spectral irradiance in algae. J Phycol 27:8–14Google Scholar
  54. Falkowski PG, Raven JA (2007) Aquatic photosynthesis. Princeton University Press, Princeton, NJGoogle Scholar
  55. Falkowski PG, Ziemann D, Kolber Z, Bienfang PK (1991) Role of eddy pumping in enhancing primary production in the ocean. Nature 352:55–58Google Scholar
  56. Finazzi G, Rapaport F, Furia A, Fleischmann M, Rochaix J-D, Zito F, Forti G (2002) Involvement of state transitions in the switch between linear and cyclic electron flow in Chlamydomonas reihardtii. EMBO Reports 3:280–285Google Scholar
  57. Fisher J, Kronfeld U (1990) Sun-stimulated chlorophyll fluorescence 1: influence of oceanic properties. Int J Remote Sens 11:2125–2147Google Scholar
  58. Franck F, Juneau P, Popovic R (2002) Resolution of the photosystem I and photosystem II contributions to chlorophyll fluorescence of intact leaves at room temperature. Biochim Biophys Acta 1556:239–246Google Scholar
  59. Fuchs E, Zimmerman RC, Jaffe JS (2002) The effect of elevated levels of phaeophytin in natural water on variable fluorescence measured from phytoplankton. J Plankton Res 24:1221–1229Google Scholar
  60. Geider RJ, Osborne BA (1992) Algal photosynthesis. Chapman & Hall, New YorkGoogle Scholar
  61. Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92Google Scholar
  62. Gilmore AM, Govindjee (1999) How higher plants respond to excess light: energy dissipation in photosystem II. In: Singhal GS, Renger R, Sopory SK, Irrgang K-D, Govindjee (eds) Concepts in photobiology: photosynthesis and photomorphogenesis. Narosa-Publishing, New Delhi, pp 513–548Google Scholar
  63. Gorbunov MY, Falkowski PG, Kolber ZS (2000) Measurement of photosynthetic parameters in benthic organisms in situ using a SCUBA-based repetition rate fluorometer. Limnol Oceanogr 45:242–245Google Scholar
  64. Gorbunov MY, Kolber ZS, Falkowski PG (1999) Measuring phtosynthetic parameters in individual algal cells by Fast Repetition Rate fluorometry. Photosynth Res 62:141–153Google Scholar
  65. Gorbunov MY, Kolber ZS, Lesser MP, Falkowski PG (2001) Photosynthesis and photoprotection in symbiotic corals. Limnol Oceanogr 46:75–85Google Scholar
  66. Gordon HR (1979) Diffuse reflectance of the ocean: the theory of its augmentation by chlorophyll a fluorescence. Appl Optics 21:2489–2492Google Scholar
  67. Govindjee, Satoh K (1986) Fluorescence properties of chlorophyll b- and chlorophyll c-containing algae. In: Govindjee, Amesz J, Fork DC (eds) Light emission by plant and bacteria. Academic Press, Orlando, pp 497–537Google Scholar
  68. Govindjee (1995) Sixty-three years since Kautsky: chlorophyll a fluorescence. Aust J Plant Physiol 22:131–160Google Scholar
  69. Gower JFR, Brown L, Borstad GA (2004) Observations of chlorophyll fluorescence in west coast waters of Canada using the MODIS satellite sensor. Can J Remote Sens 30:17–25Google Scholar
  70. Gower JFR, Doerffer R, Borstad GA (1999) Interpretation of the 685 nm peak in water-leaving radiance spectra in terms of fluorescence, absorption and scattering, and its observation by MERIS. Int J Remote Sens 20:1771–1786Google Scholar
  71. Greene RM, Kolber ZS, Swift DG, Tindale NW, Falkowski PG (1994) Physiological limitation of phytoplankton photosynthesis in the eastern equatorial Pacific determined from variability in the quantum yield of fluorescence. Limnol Oceanogr 39:1061–1074Google Scholar
  72. Hall DO, Rao KK (1999) Photosynthesis, 6th edn. Cambridge University Press, CambridgeGoogle Scholar
  73. Han BP (2001) Photosynthesis-irradiance response at physiological level: A mechanistic model. J Theoret Biol 213:121–127Google Scholar
  74. Han BP (2002) A mechanistic model of algal photoinhibition induced by photodamage to Photosystem-II. J Theoret Biol 214:519–527Google Scholar
  75. Hankamer B, Barber J, Boekema EJ (1997) Structure and membrane organization of photosystem II in green plants. Annu Rev Plant Physiol Plant Mol Biol 48:641–671Google Scholar
  76. Havaux M, Strasser RJ, Greppin H (1991) A theoretical and experimental analysis of the qp and qn coefficients of chlorophyll fluorescence quenching and their relation to photochemical and nonphotochemical events. Photosynth Res 27:41–55Google Scholar
  77. Hofstraat JW, Rubelowsky K, Slutter S (1992) Corrected fluorescence excitation and emission spectra of phytoplankton: toward a more uniform approach to fluorescence measurements. J Plankton Res 14:625–636Google Scholar
  78. Hoge FE, Swift RN (1981) Airborne simultaneous spectroscopic detection of laser-induced water Raman backscatter and fluorescence from chlorophyll a and other naturally occurring pigments. Appl Optics 20:3197–3205Google Scholar
  79. Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47:655–684Google Scholar
  80. Huot Y, Brown CA, Cullen JJ (2005) New algorithms for MODIS sun-induced chlorophyll fluorescence and a comparison with present data products. Limnol Oceanogr Meth 3:108–130Google Scholar
  81. Huot Y, Brown CA, Cullen JJ (2007) Retrieval of phytoplankton biomass from simultaneous inversion of reflectance, the diffuse attenuation coefficient, and Sun-induced fluorescence in coastal waters. J Geophys Res 112. doi:10.1029/2006JC003794Google Scholar
  82. Ivanov AG, Hurry V, Prafullanchandra VS, Öquist G, Huner NPA (2008a) Reaction centre quenching of excess light energy and photoprotection of photosystem II. J Plant Biol 51:85–96Google Scholar
  83. Ivanov AG, Prafullanchandra VS, Hurry V, Öquist G, Huner NPA (2008b) Photosystem II reaction centre quenching: mechanisms and physiological role. Photosynth Res 98:565–574Google Scholar
  84. Jeffrey SW, Vesk M (1997) Introduction to marine phytoplankton and their pigment signature. In: Jeffrey SW, Mantoura RFC, Wright SW (eds) Phytoplankton pigments in oceanography. UNESCO Publishing, RomeGoogle Scholar
  85. Johnsen G, Prézelin BB, Jovine RVM (1997) Fluorescence excitation spectra and light utilization in two red tide dinoflagellates. Limnol Oceanogr 42:1166–1177Google Scholar
  86. Karapetyan NV (2007) Non-photochemical quenching of fluorescence in cyanobacteria. Biochemistry (Moscow) 72:1127–1135Google Scholar
  87. Kargul J, Barber J (2008) Photosynthetic acclimation: Structural reorganisation of light harvesting antenna - role of redox-dependent phophorylation of major and minor chlorophyll a/b binding proteins. FEBS J 275:1056–1068Google Scholar
  88. Kiefer DA (1973a) Chlorophyll a fluorescence in marine centric diatoms: responses of chloroplasts to light and nutrient stress. Mar Biol 23:39–46Google Scholar
  89. Kiefer DA (1973b) Fluorescence properties of natural phytoplankton populations. Mar Biol 22:263–269Google Scholar
  90. Kiefer DA, Chamberlin WS, Booth CR (1989) Natural fluorescence of chlorophyll a: relationship to photosynthesis and chlorophyll concentration in the western South Pacific gyre. Limnol Oceanogr 34:868–881Google Scholar
  91. Kiefer DA, Reynolds RA (1992) Advances in understanding phytoplankton fluorescence and photosynthesis. In: Falkowski PG (ed) Primary productivity and biogeochemical cycles in the sea. Plenum Press, New York, pp 155–174Google Scholar
  92. Kim HH (1973) New algae mapping technique by the use of an airborne laser fluorosensor. Appl Optics 12:1454–1459Google Scholar
  93. Kolber Z, Falkowski PG (1993) Use of active fluorescence to estimate phytoplankton photosynthesis in situ. Limnol Oceanogr 38:1646–1665Google Scholar
  94. Kolber Z, Wyman KD, Falkowski PG (1990) Natural variability in photosynthetic energy-conversion efficiency – A field-study in the Gulf of Maine. Limnol Oceanogr 35:72–79Google Scholar
  95. Kolber Z, Zehr JR, Falkowski PG (1988) Effects of growth irradiance and nitrogen limitation on photosynthetic energy conversion in photosystem II. Plant Physiol 88:923–929Google Scholar
  96. Kolber ZS, Barber RT, Coale KH, Fitzwater SE, Greene RM, Johnson S, Lindley KS, Falkowski PG (1994) Iron limitation of phytoplankton photosynthesis in the equatorial Pacific Ocean. Nature 371:145–149Google Scholar
  97. Kolber ZS, Prásil O, Falkowski PG (1998) Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. Biochim Biophys Acta 1367:88–106Google Scholar
  98. Kopf U, Heinze J (1984) 2, 7-Bis(diethylamino)phenazoxonium chloride as a quantum counter for emission measurements between 240 and 700 nm. Anal Chem 56:1931–1935Google Scholar
  99. Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of Q(A) redox state and excitation energy fluxes. Photosynth Res 79:209–218Google Scholar
  100. Krause GH, Jahns P (2004) Non-photochemical energy dissipation determined by chlorophyll fluorescence quenching: characterization and function. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Springer, Berlin, pp 463–495Google Scholar
  101. Krause GH, Weis E (1991) Chlorophyll fluorescence: the basics. Annu Rev Plant Physiol 42:313–349Google Scholar
  102. Kromkamp JC, Forster RM (2003) The use of variable fluorescence measurements in aquatic ecosystems: differences between multiple and single turnover measuring protocols and suggested terminology. Eur J Phycol 38:103–112Google Scholar
  103. Laney SR (2003) Assessing the error in photosynthetic properties determined by fast repetition rate fluorometry. Limnol Oceanogr 48:2234–2242Google Scholar
  104. Laney SR, Letelier RM (2008) Artifacts in measurements of chlorophyll fluorescence transients, with specific application to fast repetition rate fluorometry. Limnol Oceanogr Meth 6:40–50Google Scholar
  105. Lavaud J, Rousseau B, Etienne A-L (2004) General features of photoprotection by energy dissipation in planktonic diatoms (Bacillariophyceae). J Phycol 40:130–137Google Scholar
  106. Lavergne J, Trissl H-W (1995) Theory of fluorescence induction in photosystem II: Derivation of analytical expressions in a model including exciton-radial-pair equilibrium and restricted energy transfer between photosynthetic units. Biophys J 68:2474–2492Google Scholar
  107. Laws EA (1991) Photosynthetic quotients, new production and net community production in the open ocean. Deep Sea Res Part A 38:143–167Google Scholar
  108. Lazar D (2003) Chlorophyll a fluorescence rise induced by high light illumination of dark-adapted plant tissue studied by means of a model of photosystem II and considering photosystem II heterogeneity. J Theoret Biol 220:469–503Google Scholar
  109. Lazár D (1999) Chlorophyll a fluorescence induction. Biochim Biophys Acta 1412:1–28Google Scholar
  110. Lazár D (2006) The polyphasic chlorophyll a fluorecence rise measured under high intensity of exciting light. Funct Plant Biol 33:9–30Google Scholar
  111. Letelier R, Abbott MR (1996) An analysis of chlorophyll fluorescence algorithms for the Moderate Resolution Imaging Spectrometer (MODIS). Remote Sens Environ 58:215–223Google Scholar
  112. Liu G, Janowitz GS, Kamykowski D (2001) A biophysical model of population dynamics of the autotrophic dinoflagellate Gymnodinium breve. Mar Ecol Prog Ser 210:101–124Google Scholar
  113. Loftus ME, Seliger HH (1975) Some limitations of the in vivo fluorescence technique. Chesapeake Sci 16:79–92Google Scholar
  114. Lorenzen CJ (1966) A method for the continuous measurement of in vivo chlorophyll concentration. Deep Sea Res 13:223–227Google Scholar
  115. Lutz VA, Sathyendranath S, Head EJH, Li WKW (1998) Differences between in vivo absorption and fluorescence excitation spectra in natural samples of phytoplankton. J Phycol 34:214–227Google Scholar
  116. Lutz VA, Sathyendranath S, Head EJH, Li WKW (2001) Changes in the in vivo absorption and fluorescence excitation spectra with growth irradiance in three species of phytoplankton. J Plankton Res 23:555–569Google Scholar
  117. MacIntyre HL, Kana TM, Anning T, Geider RJ (2002) Photoacclimation of photosynthesis irradiance response curves and photosynthetic pigments in microalgae and cyanobacteria. J Phycol 38:17–38Google Scholar
  118. Maritorena S, Morel A, Gentili B (2000) Determination of the fluorescence quantum yield by oceanic phytoplankton in their natural habitat. Appl Optics 39:6725–6737Google Scholar
  119. Marshall HL, Geider RJ, Flynn KJ (2000) A mechanistic model of photoinhibition. New Phytol 145:347–359Google Scholar
  120. Mauzerall DC (1972) Light-induced changes in Chlorella, and the primary photoreaction for the production of oxygen. Proc Nat Acad Sci USA 69:1358–1362Google Scholar
  121. Mauzerall DC, Greenbaum NL (1989) The absolute size of a photosynthetic unit. Bioch Biophys Acta 974:119–140Google Scholar
  122. Melis A (1999) Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo. Trends Plant Sci 4:130–135Google Scholar
  123. Miller WL, Moran MA, Sheldon WM, Zepp RG, Opsahl S (2002) Determination of apparent quantum yield spectra for the formation of biologically labile photoproducts. Limnol Oceanogr 47:343–352Google Scholar
  124. Millie DF, Schofield OME, Kirkpatrick GJ, Johnsen G, Evens TJ (2002) Using absorbance and fluorescence spectra to discriminate microalgae. Eur J Phycol 37:313–322Google Scholar
  125. Mitchell BG, Kiefer DA (1988) Chlorophyll a specific absorption and fluorescence excitation spectra for light-limited phytoplankton. Deep Sea Res 35:639–663Google Scholar
  126. Mobley CD (1994) Light and water radiative transfer in natural waters, 1st edn. Academic Press, San DiegoGoogle Scholar
  127. Moore CM, Suggett DM, Hickman AE, Kim Y-N, Tweddle JF, Sharples J, Geider RJ, Holligan PM (2006) Phytoplankton photoacclimation and photoadaptation in response to environmental gradients in a shelf sea. Limnol Oceanogr 51: 936–949Google Scholar
  128. Morel A (1988) Optical modeling of the upper ocean in relation to its biogenous matter content (case 1 waters). J Geophys Res-Oceans 93:10749–10768Google Scholar
  129. Morel A, Bricaud A (1981) Theoretical results concerning light absorption in a discrete medium, and application to specific absorption of phytoplankton. Deep-Sea Res 28:1375–1393Google Scholar
  130. Morel A, Bricaud A (1986) Inherent properties of algal cells including picoplankton: Theoretical and experimental results. In: Platt T, Li WKW (eds) Photosynthetic picoplankton. Can Bull Fish Aquat Sci 214:521–559Google Scholar
  131. Morel A, Prieur L (1977) Analysis of variations in ocean color. Limnol Oceanogr 22:709–722Google Scholar
  132. Morrison JR (2003) In situ determination of the quantum yield of phytoplankton chlorophyll a fluorescence: a simple algorithm, observations, and a model. Limnol Oceanogr 48:618–631Google Scholar
  133. Neale PJ, Cullen JJ, Yentsch CM (1989) Bio-optical inferences from chlorophyll a fluorescence: what kind of fluorescence is measured in flow cytometry? Limnol Oceanogr 34:1739–1748Google Scholar
  134. Nelson N, Yocum CF (2006) Structure and function of photosystems I and II. Annu Rev Plant Biol 57:521–565Google Scholar
  135. Neori A, Vernet M, Holm-Hansen O, Haxo FT (1986) Relationship between action spectra for chlorophyll a fluorescence and photosynthetic O2 evolution in algae. J Plankton Res 8:537–548Google Scholar
  136. Neori A, Vernet M, Holm-Hansen O, Haxo FT (1988) Comparison of chlorophyll far-red and red fluorescence excitation spectra with photosynthetic oxygen action spectra for photosystem II in algae. Mar Ecol Prog Ser 44:297–302Google Scholar
  137. Neville RA, Gower JFR (1977) Passive remote sensing of phytoplankton via chlorophyll fluorescence. J Geophys Res 82:3487–3493Google Scholar
  138. Niyogi KK (1999) Photoprotection revisited: Genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359Google Scholar
  139. Noctor G, Foyer CH (2000) Homeostasis of adenylate status during photosynthesis in a fluctuating environment. J Exp Bot 51:347–356Google Scholar
  140. Olaizola M, Geider RJ, Harrison WG, Graziano LM, Ferrari GM, Schlittenhardt PM (1996) Synoptic study of variations in the fluorescence-based maximum quantum efficiency of photosynthesis across the North Atlantic Ocean. Limnol Oceanogr 41:755–765Google Scholar
  141. Olaizola M, Yamamoto HY (1994) Short-term responses of the diadinoxanthin cycle and fluorescence yield in Chaetoceros muelleri. J Phycol 30:606–612Google Scholar
  142. Olson RJ, Chekalyuk AM, Sosik HM (1996) Phytoplankton photosynthetic characteristics from fluorescence induction assays of individual cells. Limnol Oceanogr 41:1253–1263Google Scholar
  143. Olson RJ, Sosik HM, Chekalyuk AM (1999) Photosynthetic characteristics of marine phytoplankton from pump-during-probe fluorometry of individual cells at sea. Cytometry 37:1–13Google Scholar
  144. Olson RJ, Zettler ER, Chisholm SW, Dusenberry JA (1991) Flow cytometry in oceanography. In: Demers S (ed) Particle analysis in oceanography. Springer, Berlin, pp 351–399Google Scholar
  145. Ostrowska M, Darecki M, Wozniak B (1997) An attempt to use measurements of sun-induced chlorophyll fluorescence to estimate chlorophyll a concentration in the Baltic Sea. Proc SPIE, Int Soci Optical Eng 3222:528–537Google Scholar
  146. Ostrowska M, Majchrowski R, Matorin DN, Wozniak B (2000a) Variability of the specific fluorescence of chlorophyll in the ocean. Part 1. Theory of classical in situ chlorophyll fluorometry. Oceanologia 42:203–219Google Scholar
  147. Ostrowska M, Matorin DN, Ficek D (2000b) Variability of the specific fluorescence of chlorophyll in the ocean. Part 2. Fluorometric method of chlorophyll a determination. Oceanologia 42:221–229Google Scholar
  148. Oxborough K, Baker NR (2000) An evaluation of the potential triggers of photoinactivation of photosystem II in the context of a Stern-Volmer model for downregulation and the reversible radical pair equilibrium. Phil Trans Roy Soc London 355:1489–1498Google Scholar
  149. Park Y-I, Chow WS, Anderson JM (1995) Light inactivation of functional photosystem II in leaves of peas grown in moderate light depends on photon exposure. Planta 196:401–411Google Scholar
  150. Parkhill J-P, Maillet G, Cullen JJ (2001) Fluorescence-based maximal quantum yield for PSII as a diagnostic of nutrient stress. J Phycol 37:517–529Google Scholar
  151. Poole LR, Esaias WE (1982) Water Raman normalization of airborn laser fluorosensor measurements: a computer model study. Appl Optics 21:1982Google Scholar
  152. Prézelin BB (1981) Light reactions in photosynthesis. In: Platt T (ed) Physiological bases of phytoplankton ecology. Can Bull Fish Aquat Sciences 210:1–43Google Scholar
  153. Prezelin BB, Boczar BA (1986) Molecular bases of cell absorption and fluorescence in phytoplankton: potential applications to studies in optical oceanography. Prog Phycol Res 4:349–464Google Scholar
  154. Raateoja M, Seppälä J, Ylöstalo P (2004) Fast repetition rate fluorometry is not applicable to studies of filamentous cyanobacteria from the Baltic Sea. Limnol Oceanogr 49:1006–1012Google Scholar
  155. Raven JA, Geider RJ (2003) Adaptation, acclimation and regulation in algal phtosynthesis. In: Larkum AWD, Douglas SE, Raven JA (eds) Photosynthesis in algae. Kluwer, Dordrecht, pp 385–412Google Scholar
  156. Roesler CS, Perry MJ (1995) In situ phytoplankton absorption, fluorescence emission, and particulate backscattering spectra determined from reflectance. J Geophys Res 100:13279–13294Google Scholar
  157. Rohácek K (2002) Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. Photosynthetica 40:13–29Google Scholar
  158. Rohácek K, Barták M (1999) Technique of the modulated chlorophyll fluorescence: basic concepts, useful parameters, and some applications. Photosynthetica 37:339–363Google Scholar
  159. Roy S, Legendre L (1979) DCMU-enhanced fluorescence as an index of photosynthetic activity of phytoplankton. Mar Biol 55:93–101Google Scholar
  160. Ruban AV Berera R, Ilioaia C, van Stokkum IHM, Kennis JTM, Pascal AA, van Amerongen H, Robert B, Horton P, van Grondelle R (2007) Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450:575–578Google Scholar
  161. Ruban AV, Lavaud J, Rousseau B, Guglielmi G, Horton P, Etienne A-L (2004) The super-excess energy dissipation in diatom algae: comparative analysis with higher plants. Photosynth Res 82:165–175Google Scholar
  162. Sakshaug E, Johnsen G, Andresen K, Vernet M (1991) Modeling of light-dependent algal photosynthesis and growth: experiments with the Barents Sea diatoms Thalassiosira nordenskioeldii and Chaetoceros furcellatus. Deep Sea Res A 38:415–430Google Scholar
  163. Sathyendranath S, Platt T, Irwin B, Horne E, Borstad G, Stuart V, Payzant L, Maass H, Kepkay P, Li P, Spry J, Gower J (2004) A multispectral remote sensing study of coastal waters off Vancouver Island. Int J Remote Sens 25:893–919Google Scholar
  164. Schallenberg C, Lewis MR, Kelley DE, Cullen JJ (2008) The inferred influence of nutrient availability on the relationship between sun-induced fluorescence and incident irradiance in the Bering Sea. J Geophys Res 113:C07046. doi:07010.01029/02007JC004355Google Scholar
  165. Schatz GH, Brock H, Holzwarth AR (1988) Kinetic and energetic model for the primary processes in photosystem II. Biophys J 54:397–405Google Scholar
  166. Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62Google Scholar
  167. Sciandra A, Lazzara L, Claustre H, Babin M (2000) Responses of growth rate, pigment composition and optical properties of Cryptomonas sp. to light and nitrogen stresses. Mar Ecol Prog Ser 201:107–120Google Scholar
  168. Smyth TJ, Pemberton KL, Aiken J, Geider RJ (2004) A methodology to determine primary production and phytoplankton photosynthetic parameters from fast repetition rate fluorometry. J Plankton Res 26:1337–1350Google Scholar
  169. SooHoo JB, Kiefer DA (1982) Vertical distribution of phaeopigments — II. Rates of production and kinetics of photooxidation. Deep-Sea Res 29:1553–1563Google Scholar
  170. Sosik HM, Mitchell BG (1995) Light absorption by phytoplankton, photosynthetic pigments and detritus in the California Current System. Deep Sea Res I 42:1717–1748Google Scholar
  171. Sosik HM, Olson JS, Neubert MG, Shalapyonok A, Solow AR (2003) Growth rates of coastal phytoplankton from time-series measurements with a submersible flow cytometer. Limnol Oceanog 48:1756–1765Google Scholar
  172. Stegmann PM, Lewis MR, Davis CO, Cullen JJ (1992) Primary production estimates from recordings of solar-stimulated fluorescence in the Equatorial Pacific at 150˚W. J Geophys Res 97:627–638Google Scholar
  173. Stirbet A, Govindjee SBJ, Strasser RJ (1998) Chlorophyll a fluorescence induction in higher plants: modelling and numerical simulation. J Theoret Biol 193:131–151Google Scholar
  174. Strasser RJ, Srivastava A, Govindgee (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61:32–42Google Scholar
  175. Suggett DJ, Kraay G, Holligan P, Davey M, Aiken J, Geider RJ (2001) Assessment of photosynthesis in a spring cyanobacterial bloom by use of a fast repetition rate fluorometer. Limnol Oceanogr 46:802–810Google Scholar
  176. Suggett DJ, MacIntyre HL, Geider RJ (2004) Evaluation of biophysical and optical determination of light absorption by photosystem II in phytoplankton. Limnol Oceanogr Meth 2:316–332Google Scholar
  177. Suggett DJ, Moore CM, Hickman AE, Geider RJ (2009) Interpretation of fast repetition rate (FRR) fluorescence: signature of phytoplankton community structure versus physiological state. Mar Ecol Prog Ser 376:1–19Google Scholar
  178. Suggett DJ, Oxborough K, Baker NR, MacIntyre HL, Kana TM, Geider RJ (2003) Fast repetition rate and pulse amplitude modulation chlorophyll a fluorescence measurements for assessment of photosynthetic electron transport in marine phytoplankton. Eur J Phycol 38:371–384Google Scholar
  179. Timmermans KR, van der Woerd HJ, Wernand MR, Sligting M, Uitz J, de Baar HJW (2008) In situ and remote-sensed chlorophyll fluorescence as indicator of the physiological state of phytoplankton near the Isles Kerguelen (Souther Ocean). Polar Biol 31:617–628Google Scholar
  180. Ting CS, Rocap G, King J, Chisholm SW (2002) Cyanobacterial photosynthesis in the oceans: the origins and significance of divergent light-harvesting strategies. Trends Microbiol 10:134–142Google Scholar
  181. Trees CC, Clark DK, Bidigare RR, Ondrusek ME, Mueller JL (2000) Accessory pigments versus chlorophyll a concentrations within the euphotic zone: A ubiquitous relationship. Limnol Oceanogr 45:1130–1143Google Scholar
  182. Trissl H-W, Lavergne J (1995) Fluorescence Induction from photosystem II: Analytical equations for the yields of photochemistry and fluorescence derived from analysis of a model including exciton-radical pair equilibrium and restricted energy transfer between photosynthetic units. Aust J Plant Physiol 22:183–193Google Scholar
  183. Vaulot D, Marie D (1999) Diel variability of photosynthetic picolankton in the equatorial Pacific. J Geophys Res 104:3297–3310Google Scholar
  184. Vermotte C, Etienne A-L, Briantais J-M (1979) Quenching of the system II chlorophyll fluorescence by the plastoquinone pool. Biochim Biophys Acta 545:519–527Google Scholar
  185. Vincent WF (1981) Photosynthetic capacity measured by DCMU-induced chlorophyll fluorescence in an oligotrophic lake. Freshw Biol 11:61–78Google Scholar
  186. Welschmeyer NA (1994) Fluorometric analysis of chlrophyll a in the presence of chlorophyll b and pheopigments. Limnol Oceanogr 39:1985–1992Google Scholar
  187. Westberry TK, Siegel DA (2003) Phytoplankton natural fluorescence variability in the Sargasso Sea. Deep Sea Res I 50:417–434Google Scholar
  188. White AJ, Critchley C (1999) Rapid light curves: a new fluorescence method to assess the state of the photosynthetic apparatus. Photosynth Res 59:63–72Google Scholar
  189. Whitmarsh J, Govindjee (1999) The photosynthetic process. In: Singhal GS, Renger R, Sopory SK, Irrgang K-D, Govindjee (eds) Concepts in photobiology: photosynthesis and photomorphogenesis. Narosa-Publishing, New Delhi, pp 11–51Google Scholar
  190. Yentsch CM, Horan PK, Muirhead K, Dortch Q, Haugen E, Legendre L, Muphy LS, Perry MJ, Phinney DA, pomponi SA, Spinrad RW, Wood M, Yentsch CS Zahoranec BJ (1983) Flow cytometry and cell sorting: a technique for analysis and sorting of aquatic particles. Limnol Oceanogr 28:1275–1280Google Scholar
  191. Yentsch CS, Menzel DW (1963) A method for the determination of phytoplankton chlorophyll and phaeophytin by fluorescence. Deep Sea Res 10:221–231Google Scholar
  192. Yentsch CS, Phinney DA (1985) Spectral fluorescence: a taxonomic tool for studying the structure of phytoplankton populations. J Plankton Res 7:617–632Google Scholar
  193. Yentsch CS, Yentsch CA (1979) Fluorescence spectral signatures: the characterization of phytoplankton populations by the use of excitation and emission. J Mar Res 37:471–483Google Scholar
  194. Zonneveld C (1997) Modelling the effects of photoadaptation on the photosynthesis-irradiance curve. J Theoret Biol 186:381–388Google Scholar
  195. Zouni A, Witt HT, Fromme P, Krauss N, Saenger W, Orth P (2001) Crystal structure of photosystem II from Synechococcus elongatus a 3.8Å resolution. Nature 409:739–743Google Scholar

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© Springer Netherlands 2010

Authors and Affiliations

  1. 1.Département de Géomatique AppliquéeUniversité de SherbrookeSherbrookeCanada
  2. 2.Laboratoire d’Océanographie de Villefranche, UMR 7093Université Pierre et Marie Curie-Paris 6ParisFrance

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