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Survey of Tools for Measuring In Vivo Photosynthesis

  • Berkley J. Walker
  • Florian A. Busch
  • Steven M. Driever
  • Johannes Kromdijk
  • Tracy Lawson
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 1770)

Abstract

Measurements of in vivo photosynthesis are powerful tools that probe the largest fluxes of carbon and energy in an illuminated leaf, but often the specific techniques used are so varied and specialized that it is difficult for researchers outside the field to select and perform the most useful assays for their research questions. The goal of this chapter is to provide a broad overview of the current tools available for the study of in vivo photosynthesis so as to provide a foundation for selecting appropriate techniques, many of which are presented in detail in subsequent chapters. This chapter also organizes current methods into a comparative framework and provides examples of how they have been applied to research questions of broad agronomical, ecological, or biological importance. The chapter closes with an argument that the future of in vivo measurements of photosynthesis lies in the ability to use multiple methods simultaneously and discusses the benefits of this approach to currently open physiological questions. This chapter, combined with the relevant methods chapters, could serve as a laboratory course in methods in photosynthesis research or as part of a more comprehensive laboratory course in general plant physiology methods.

Key words

Photosynthesis CO2 exchange O2 exchange Chlorophyll fluorescence Online mass spectrometry 

References

  1. 1.
    Wu A, Song Y, van Oosterom EJ, Hammer GL (2016) Connecting biochemical photosynthesis models with crop models to support crop improvement. Front Plant Sci 7:1518. https://doi.org/10.3389/fpls.2016.01518 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    De Pury D, Farquhar GD (1997) Simple scaling of photosynthesis from leaves to canopies without the errors of big-leaf models. Plant Cell Environ 20(5):537–557CrossRefGoogle Scholar
  3. 3.
    von Caemmerer S (2000) Biochemical models of leaf photosynthesis, Techniques in plant sciences, vol 2. CSIRO, CollingwoodGoogle Scholar
  4. 4.
    Galmés J, Hermida-Carrera C, Laanisto L, Niinemets Ü (2016) A compendium of temperature responses of Rubisco kinetic traits: variability among and within photosynthetic groups and impacts on photosynthesis modeling. J Exp Bot 67(17):5067–5091. https://doi.org/10.1093/jxb/erw267 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Hermida-Carrera C, Kapralov MV, Galmés J (2016) Rubisco catalytic properties and temperature response in crops. Plant Phys 171(4):2549–2561. https://doi.org/10.1104/pp.16.01846
  6. 6.
    Orr D, Alcântara A, Kapralov MV, Andralojc J, Carmo-Silva E, Parry MAJ (2016) Surveying Rubisco diversity and temperature response to improve crop photosynthetic efficiency. Plant Phys 172(2):707–717. https://doi.org/10.1104/pp.16.00750 CrossRefGoogle Scholar
  7. 7.
    Fullana-Pericàs M, Conesa MÀ, Soler S, Ribas-Carbó M, Granell A, Galmés J (2016) Variations of leaf morphology, photosynthetic traits and water-use efficiency in Western-Mediterranean tomato landraces. Photosynthetica 55(1):121–133. https://doi.org/10.1007/s11099-016-0653-4 CrossRefGoogle Scholar
  8. 8.
    Gu J, Yin X, Stomph T-J, Wang H, Struik PC (2012) Physiological basis of genetic variation in leaf photosynthesis among rice (Oryza sativa L.) introgression lines under drought and well-watered conditions. J Exp Bot 63(14):5137–5153. https://doi.org/10.1093/jxb/ers170 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Sun J, Sun J, Feng Z (2015) Modelling photosynthesis in flag leaves of winter wheat Triticum aestivum considering the variation in photosynthesis parameters during development. Funct Plant Biol 42(11):1036–1044. https://doi.org/10.1071/FP15140 CrossRefGoogle Scholar
  10. 10.
    Gaastra P (1959) Photosynthesis of crop plants as influenced by light, carbon dioxide, temperature, and stomatal diffusion resistance. Wageningen University, Wageningen: VeenmanGoogle Scholar
  11. 11.
    Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149(1):78–90. https://doi.org/10.1007/bf00386231 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153(4):376–387CrossRefGoogle Scholar
  13. 13.
    Harley P, Sharkey T (1991) An improved model of C3 photosynthesis at high CO2: reversed O2 sensitivity explained by lack of glycerate reentry into the chloroplast. Photosynth Res 27(3):169–178PubMedPubMedCentralGoogle Scholar
  14. 14.
    Busch FA (2017) Photosynthetic gas exchange in land plants at the leaf level. In: Covshoff S (ed) Photosynthesis: methods and protocols, vol 1. Springer Press, New YorkGoogle Scholar
  15. 15.
    Farquhar G, Wong S (1984) An empirical model of stomatal conductance. Funct Plant Biol 11(3):191–210. https://doi.org/10.1071/PP9840191 CrossRefGoogle Scholar
  16. 16.
    von Caemmerer S, Evans J, Hudson G, Andrews T (1994) The kinetics of ribulose-1, 5-bisphosphate carboxylase/oxygenase in vivo inferred from measurements of photosynthesis in leaves of transgenic tobacco. Planta 195(1):88–97CrossRefGoogle Scholar
  17. 17.
    Bernacchi CJ, Pimentel C, Long SP (2003) In vivo temperature response functions of parameters required to model RuBP-limited photosynthesis. Plant Cell Environ 26(9):1419–1430. https://doi.org/10.1046/j.0016-8025.2003.01050.x CrossRefGoogle Scholar
  18. 18.
    Walker BJ, Ariza LS, Kaines S, Badger MR, Cousins AB (2013) Temperature response of in vivo Rubisco kinetics and mesophyll conductance in Arabidopsis thaliana: comparisons to Nicotiana tabacum. Plant Cell Environ 36(12):2108–2119. https://doi.org/10.1111/pce.12166 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Busch FA, Sage TL, Cousins AB, Sage RF (2013) C3 plants enhance rates of photosynthesis by reassimilating photorespired and respired CO2. Plant Cell Environ 36(1):200–212. https://doi.org/10.1111/j.1365-3040.2012.02567.x CrossRefPubMedGoogle Scholar
  20. 20.
    Ma F, Jazmin LJ, Young JD, Allen DK (2014) Isotopically nonstationary (13)C flux analysis of changes in Arabidopsis thaliana leaf metabolism due to high light acclimation. Proc Natl Acad Sci U S A 111(47):16967–16972. https://doi.org/10.1073/pnas.1319485111 CrossRefGoogle Scholar
  21. 21.
    Abadie C, Boex-Fontvieille ERA, Carroll AJ, Tcherkez G (2016) In vivo stoichiometry of photorespiratory metabolism. Nat Plants 2:15220CrossRefPubMedGoogle Scholar
  22. 22.
    George GM, Kölling K, Kuenzli R, Hirsch-Hoffmann M, Flütsch P, Zeeman SC (2017) Design and use of a digitally-controlled device for accurate, multiplexed gas exchange measurements of the complete foliar parts of plants. In: Covshoff S (ed) Photosynthesis: methods and protocols, vol 1. Springer Press, New YorkGoogle Scholar
  23. 23.
    Dutton RG, Jiao J, Tsujita MJ, Grodzinski B (1988) Whole plant CO2 exchange measurements for nondestructive estimation of growth. Plant Phys 86(2):355–358. https://doi.org/10.1104/pp.86.2.355 CrossRefGoogle Scholar
  24. 24.
    Zeeman SC, Rees TA (1999) Changes in carbohydrate metabolism and assimilate export in starch-excess mutants of Arabidopsis. Plant Cell Environ 22(11):1445–1453. https://doi.org/10.1046/j.1365-3040.1999.00503.x CrossRefGoogle Scholar
  25. 25.
    Baldocchi DD, Amthor JS (2001) Canopy photosynthesis: history, measurements, and models. In: Roy J, Mooney HA, Saugier B (eds) Terrestrial global productivity. Academic Press, USA, pp 9–31CrossRefGoogle Scholar
  26. 26.
    Hall DO, Scurlock J, Bolhar-Nordenkampf H, Leegood RC, Long S (1993) Photosynthesis and production in a changing environment: a field and laboratory manual. Chapman & Hall, LondonGoogle Scholar
  27. 27.
    Kölling K, George GM, Künzli R, Flütsch P, Zeeman SC (2015) A whole-plant chamber system for parallel gas exchange measurements of Arabidopsis and other herbaceous species. Plant Methods 11(1):48. https://doi.org/10.1186/s13007-015-0089-z CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Barton CVM, Ellsworth DS, Medlyn BE, Duursma RA, Tissue DT, Adams MA, Eamus D, Conroy JP, McMurtrie RE, Parsby J, Linder S (2010) Whole-tree chambers for elevated atmospheric CO2 experimentation and tree scale flux measurements in south-eastern Australia: The Hawkesbury Forest Experiment. Agric For Meteorol 150(7–8):941–951. https://doi.org/10.1016/j.agrformet.2010.03.001 CrossRefGoogle Scholar
  29. 29.
    Drake JE, Tjoelker MG, Aspinwall MJ, Reich PB, Barton CVM, Medlyn BE, Duursma RAC (2016) Does physiological acclimation to climate warming stabilize the ratio of canopy respiration to photosynthesis? New Phytol 211(3):850–863. https://doi.org/10.1111/nph.13978 CrossRefPubMedGoogle Scholar
  30. 30.
    Baldocchi DD (2003) Assessing the eddy covariance technique for evaluating carbon dioxide exchange rates of ecosystems: past, present and future. Glob Chang Biol 9(4):479–492. https://doi.org/10.1046/j.1365-2486.2003.00629.x CrossRefGoogle Scholar
  31. 31.
    Song Q, Zhu X-G (2017) Measuring canopy gas exchange using CAnopy Photosynthesis and Transpiration Systems (CAPTS). In: Covshoff S (ed) Photosynthesis: methods and protocols. Springer Press, New YorkGoogle Scholar
  32. 32.
    Schmid HP (1994) Source areas for scalars and scalar fluxes. Boundary-Layer Meteorol 67(3):293–318. https://doi.org/10.1007/bf00713146 CrossRefGoogle Scholar
  33. 33.
    Raupach MR (1979) Anomalies in flux-gradient relationships over forest. Boundary-Layer Meteorol 16(3):467–486. https://doi.org/10.1007/bf03335385 CrossRefGoogle Scholar
  34. 34.
    Simpson IJ, Thurtell GW, Neumann HH, Den Hartog G, Edwards GC (1998) The validity of similarity theory in the roughness sublayer above forests. Boundary-Layer Meteorol 87(1):69–99. https://doi.org/10.1023/a:1000809902980 CrossRefGoogle Scholar
  35. 35.
    Severinghaus JW (2002) The invention and development of blood gas analysis apparatus. Anesthesiology 97(1):253–256CrossRefPubMedGoogle Scholar
  36. 36.
    Clark LC, Lyons C (1962) Electrode systems for continuous monitoring in cardiovascular surgery. Ann N Y Acad Sci 102(1):29–45. https://doi.org/10.1111/j.1749-6632.1962.tb13623.x CrossRefPubMedGoogle Scholar
  37. 37.
    Shevela D, Schröder WP, Messinger J (2017) Liquid-phase measurements of photosynthetic oxygen evolution. In: Covshoff S (ed) Photosynthesis: methods and protocols. Springer Press, New YorkGoogle Scholar
  38. 38.
    Driever SM, Baker NR (2017) Measurement of O2 uptake and evolution in leaves in vivo using stable isotopes and membrane inlet mass spectrometry. In: Covshoff S (ed) Photosynthesis: methods and protocols, vol 1. Springer Press, New YorkGoogle Scholar
  39. 39.
    Hill JF, Govindjee (2014) The controversy over the minimum quantum requirement for oxygen evolution. Photosynth Res 122(1):97–112. https://doi.org/10.1007/s11120-014-0014-8 CrossRefPubMedGoogle Scholar
  40. 40.
    Ubierna N, Holloway-Phillips M-M, Farquhar GD (2017) Using carbon stable isotopes to study C3 and C4 photosynthesis: models and calculations. In: Covshoff S (ed) Photosynthesis: methods and protocols. Springer Press, New YorkGoogle Scholar
  41. 41.
    Evans JR, Kaldenhoff R, Genty B, Terashima I (2009) Resistances along the CO2 diffusion pathway inside leaves. J Exp Bot 60(8):2235–2248. https://doi.org/10.1093/jxb/erp117 CrossRefPubMedGoogle Scholar
  42. 42.
    Cernusak LA, Ubierna N, Winter K, Holtum JAM, Marshall JD, Farquhar GD (2013) Environmental and physiological determinants of carbon isotope discrimination in terrestrial plants. New Phytol 200(4):950–965. https://doi.org/10.1111/nph.12423 CrossRefGoogle Scholar
  43. 43.
    Raven JA, Beardall J (2016) The ins and outs of CO2. J Exp Bot 67(1):1–13CrossRefPubMedGoogle Scholar
  44. 44.
    Barbour MMC (2016) Understanding regulation of leaf internal carbon and water transport using online stable isotope techniques. New Phytol 213(1):83–88. https://doi.org/10.1111/nph.14171 CrossRefPubMedGoogle Scholar
  45. 45.
    Canvin DT, Berry JA, Badger MR, Fock H, Osmond CB (1980) Oxygen exchange in leaves in the light. Plant Phys 66(2):302–307. https://doi.org/10.1104/pp.66.2.302 CrossRefGoogle Scholar
  46. 46.
    Badger MR (1985) Photosynthetic oxygen exchange. Annu Rev Plant Physiol 36(1):27–53. https://doi.org/10.1146/annurev.pp.36.060185.000331 CrossRefGoogle Scholar
  47. 47.
    Haupt-Herting S, Klug K, Fock HP (2001) A new approach to measure gross CO2 fluxes in leaves. Gross CO2 sssimilation, photorespiration, and mitochondrial respiration in the light in tomato under drought stress. Plant Phys 126(1):388–396. https://doi.org/10.1104/pp.126.1.388 CrossRefGoogle Scholar
  48. 48.
    Maxwell K, Badger M, Osmond C (1998) A comparison of CO2 and O2 exchange patterns and the relationship with chlorophyll fluorescence during photosynthesis in C3 and CAM plants. Aust J Plant Physiol 25(1):45–52CrossRefGoogle Scholar
  49. 49.
    Ruuska SA, Badger MR, Andrews TJ, von Caemmerer S (2000) Photosynthetic electron sinks in transgenic tobacco with reduced amounts of Rubisco: little evidence for significant Mehler reaction. J Exp Bot 51:357–368. https://doi.org/10.1093/jexbot/51.suppl_1.357 CrossRefPubMedGoogle Scholar
  50. 50.
    Driever SM, Baker NR (2011) The water–water cycle in leaves is not a major alternative electron sink for dissipation of excess excitation energy when CO2 assimilation is restricted. Plant Cell Environ 34(5):837–846. https://doi.org/10.1111/j.1365-3040.2011.02288.x CrossRefPubMedGoogle Scholar
  51. 51.
    Peltier G, Cournac L, Despax V, Dimon B, Fina L, Genty B, Rumeau D (1995) Carbonic anhydrase activity in leaves as measured in vivo by 18O exchange between carbon dioxide and water. Planta 196(4):732–739. https://doi.org/10.1007/bf01106768 CrossRefGoogle Scholar
  52. 52.
    Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59(1):89–113. https://doi.org/10.1146/annurev.arplant.59.032607.092759 CrossRefPubMedGoogle Scholar
  53. 53.
    Maxwell K, Johnson G (2000) Chlorophyll fluorescence-a practical guide. J Exp Bot 51(345):659–668CrossRefPubMedGoogle Scholar
  54. 54.
    Butler WL (1978) Energy distribution in the photochemical apparatus of photosynthesis. Annu Rev Plant Physiol 29(1):345–378CrossRefGoogle Scholar
  55. 55.
    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 Gen Subj 990(1):87–92. https://doi.org/10.1016/S0304-4165(89)80016-9 CrossRefGoogle Scholar
  56. 56.
    Bradbury M, Baker NR (1981) Analysis of the slow phases of the in vivo chlorophyll fluorescence induction curve. Changes in the redox state of Photosystem II electron acceptors and fluorescence emission from Photosystems I and II. Biochim Biophys Acta Bioenerg 635(3):542–551. https://doi.org/10.1016/0005-2728(81)90113-4 CrossRefGoogle Scholar
  57. 57.
    Loriaux SD, Avenson TJ, Welles JM, McDermitt DK, Eckles RD, Riensche B, Genty B (2013) Closing in on maximum yield of chlorophyll fluorescence using a single multiphase flash of sub-saturating intensity. Plant Cell Environ 36(10):1755–1770. https://doi.org/10.1111/pce.12115 CrossRefPubMedGoogle Scholar
  58. 58.
    Schreiber U, Neubauer C (1987) The polyphasic rise of chlorophyll fluorescence upon onset of strong continuous illumination: II. Partial control by the Photosystem II donor side and possible ways of interpretation. Zeitschrift für Naturforschung C 42(11–12):255–1264. https://doi.org/10.1515/znc-1987-11-1218 CrossRefGoogle Scholar
  59. 59.
    Ajigboye OO, Ray RV, Murchie EH (2017) Chlorophyll fluorescence on the fast timescale. In: Covshoff S (ed) Photosynthesis: methods and protocols. Springer Press, New YorkGoogle Scholar
  60. 60.
    Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot 64(13):3983–3998. https://doi.org/10.1093/jxb/ert208 CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55(403):1607–1621. https://doi.org/10.1093/jxb/erh196 CrossRefPubMedGoogle Scholar
  62. 62.
    Fryer MJ, Oxborough K, Martin B, Ort DR, Baker NR (1995) Factors associated with depression of photosynthetic quantum efficiency in maize at low growth temperature. Plant Phys 108(2):761–767CrossRefGoogle Scholar
  63. 63.
    Fracheboud Y, Leipner J (2003) The application of chlorophyll fluorescence to study light, temperature, and drought stress. In: DeEll JR, Toivonen PMA (eds) Practical applications of chlorophyll fluorescence in plant biology. Springer, Boston, MA, pp 125–150. https://doi.org/10.1007/978-1-4615-0415-3_4 CrossRefGoogle Scholar
  64. 64.
    Gray GR, Chauvin LP, Sarhan F, Huner N (1997) Cold acclimation and freezing tolerance (A complex interaction of light and temperature). Plant Phys 114(2):467–474. https://doi.org/10.1104/pp.114.2.467 CrossRefGoogle Scholar
  65. 65.
    Avenson TJ, Saathoff AJ (2017) Sub-saturating multiphase flash irradiances to estimate maximum fluorescence yield. In: Covshoff S (ed) Photosynthesis: methods and protocols. Springer Press, New YorkGoogle Scholar
  66. 66.
    Poulson ME, Edwards GE, Browse J (2002) Photosynthesis is limited at high leaf to air vapor pressure deficit in a mutant of Arabidopsis thaliana that lacks trienoic fatty acids. Photosynth Res 72(1):55–63. https://doi.org/10.1023/a:1016054027464 CrossRefPubMedGoogle Scholar
  67. 67.
    Rizza F, Pagani D, Stanca AM, Cattivelli L (2001) Use of chlorophyll fluorescence to evaluate the cold acclimation and freezing tolerance of winter and spring oats. Plant Breed 120(5):389–396. https://doi.org/10.1046/j.1439-0523.2001.00635.x CrossRefGoogle Scholar
  68. 68.
    Lawson T, Oxborough K, Morison JIL, Baker NR (2002) Responses of photosynthetic electron transport in stomatal guard cells and mesophyll cells in intact leaves to light, CO2, and humidity. Plant Phys 128(1):52–62. https://doi.org/10.1104/pp.010317 CrossRefGoogle Scholar
  69. 69.
    Lawson T, Oxborough K, Morison JIL, Baker NR (2003) The responses of guard and mesophyll cell photosynthesis to CO2, O2, light, and water stress in a range of species are similar. J Exp Bot 54(388):1743–1752. https://doi.org/10.1093/jxb/erg186 CrossRefPubMedGoogle Scholar
  70. 70.
    Baker NR, Oxborough K, Lawson T, Morison JIL (2001) High resolution imaging of photosynthetic activities of tissues, cells and chloroplasts in leaves. J Exp Bot 52(356):615–621. https://doi.org/10.1093/jxb/52.356.615 CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Simkin AJ, McAusland L, Headland LR, Lawson T, Raines CA (2015) Multigene manipulation of photosynthetic carbon assimilation increases CO2 fixation and biomass yield in tobacco. J Exp Bot 66(13):4075–4090. https://doi.org/10.1093/jxb/erv204 CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Barbagallo RP, Oxborough K, Pallett KE, Baker NR (2003) Rapid, noninvasive screening for perturbations of metabolism and plant growth using chlorophyll fluorescence imaging. Plant Phys 132(2):485–493. https://doi.org/10.1104/pp.102.018093 CrossRefGoogle Scholar
  73. 73.
    Caspari O, Meyer M, Tolleter D, Wittkopp T, Cunniffe N, Lawson T, Grossman A, Griffiths H (2017) Pyrenoid loss in Chlamydomonas reinhardtii causes limitations in CO2 supply, but not thylakoid operating efficiency. J Exp Bot 68(14):3903–3913CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Oxborough K (2004) Imaging of chlorophyll a fluorescence: theoretical and practical aspects of an emerging technique for the monitoring of photosynthetic performance. J Exp Bot 55(400):1195–1205. https://doi.org/10.1093/jxb/erh145 CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    von Caemmerer S, Lawson T, Oxborough K, Baker NR, Andrews TJ, Raines CA (2004) Stomatal conductance does not correlate with photosynthetic capacity in transgenic tobacco with reduced amounts of Rubisco. J Exp Bot 55(400):1157–1166. https://doi.org/10.1093/jxb/erh128 CrossRefGoogle Scholar
  76. 76.
    Lawson T, Lefebvre S, Baker NR, Morison JIL, Raines CA (2008) Reductions in mesophyll and guard cell photosynthesis impact on the control of stomatal responses to light and CO2. J Exp Bot 59(13):3609–3619. https://doi.org/10.1093/jxb/ern211 CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    McAusland L, Vialet-Chabrand SRM, Matthews JSA, Lawson T (2015) Spatial and temporal responses in stomatal behaviour, photosynthesis and implications for water-use efficiency. In: Mancuso S, Shabala S (eds) Rhythms in plants: dynamic responses in a dynamic environment. Springer International Publishing, Cham, pp 97–119. https://doi.org/10.1007/978-3-319-20517-5_5 CrossRefGoogle Scholar
  78. 78.
    Morison JIL, Gallouët E, Lawson T, Cornic G, Herbin R, Baker NR (2005) Lateral diffusion of CO2 in leaves is not sufficient to support photosynthesis. Plant Phys 139(1):254–266. https://doi.org/10.1104/pp.105.062950 CrossRefGoogle Scholar
  79. 79.
    Badger MR, Fallahi H, Kaines S, Takahashi S (2009) Chlorophyll fluorescence screening of Arabidopsis thaliana for CO2 sensitive photorespiration and photoinhibition mutants. Funct Plant Biol 36(11):867–873. https://doi.org/10.1071/FP09199 CrossRefGoogle Scholar
  80. 80.
    Lawson T, Vialet-Chabrand S (2017) Chlorophyll fluorescence imaging. In: Covshoff S (ed) Photosynthesis: Methods and Protocols, vol 1. Springer Press, New YorkGoogle Scholar
  81. 81.
    Baker NR, Harbinson J, Kramer DM (2007) Determining the limitations and regulation of photosynthetic energy transduction in leaves. Plant Cell Environ 30(9):1107–1125. https://doi.org/10.1111/j.1365-3040.2007.01680.x CrossRefPubMedGoogle Scholar
  82. 82.
    Harbinson J, Woodward FI (1987) The use of light-induced absorbance changes at 820 nm to monitor the oxidation state of P-700 in leaves. Plant Cell Environ 10(2):131–140. https://doi.org/10.1111/1365-3040.ep11602090 CrossRefGoogle Scholar
  83. 83.
    Sacksteder C, Kramer D (2000) Dark-interval relaxation kinetics (DIRK) of absorbance changes as a quantitative probe of steady-state electron transfer. Photosynth Res 66(1):145–158CrossRefPubMedGoogle Scholar
  84. 84.
    Cruz JA, Sacksteder CA, Kanazawa A, Kramer DM (2001) Contribution of electric field (Δψ) to steady-state transthylakoid proton motive force (pmf) in vitro and in vivo. Control of pmf parsing into Δψ and ΔpH by ionic strength. Biochemistry 40(5):1226–1237. https://doi.org/10.1021/bi0018741 CrossRefPubMedGoogle Scholar
  85. 85.
    Kramer DM, Evans JR (2011) The importance of energy balance in improving photosynthetic productivity. Plant Phys 155(1):70–78. https://doi.org/10.1104/pp.110.166652 CrossRefGoogle Scholar
  86. 86.
    Walker BJ, Strand DD, Kramer DM, Cousins AB (2014) The response of cyclic electron flow around photosystem I to changes in photorespiration and nitrate assimilation. Plant Phys 165(1):453–462. https://doi.org/10.1104/pp.114.238238 CrossRefGoogle Scholar
  87. 87.
    Finazzi G, Rappaport F, Furia A, Fleischmann M, Rochaix JD, Zito F, Forti G (2002) Involvement of state transitions in the switch between linear and cyclic electron flow in Chlamydomonas reinhardtii. EMBO Rep 3(3):280–285. https://doi.org/10.1093/embo-reports/kvf047 CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Avenson TJ, Cruz JA, Kanazawa A, Kramer DM (2005) Regulating the proton budget of higher plant photosynthesis. Proc Natl Acad Sci U S A 102(27):9709–9713. https://doi.org/10.1073/pnas.0503952102 CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Laisk A, Oja V (1994) Range of photosynthetic control of postillumination P700+ reduction rate in sunflower leaves. Photosynth Res 39(1):39–50. https://doi.org/10.1007/bf00027141 CrossRefPubMedGoogle Scholar
  90. 90.
    Harbinson J (1994) The responses of thylakoid electron transport and light utilisation efficiency to sink limitation of electron transport. In: Baker NR, Bowyer J (eds) Photoinhibition of photosynthesis. Bios Scientific Publishers, Oxford, pp 273–295Google Scholar
  91. 91.
    Kramer DM, Avenson TJ, Edwards GE (2004) Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions. Trends Plant Sci 9(7):349–357CrossRefPubMedGoogle Scholar
  92. 92.
    Cruz JA, Avenson TJ, Kanazawa A, Takizawa K, Edwards GE, Kramer DM (2005) Plasticity in light reactions of photosynthesis for energy production and photoprotection. J Exp Bot 56(411):395–406. https://doi.org/10.1093/jxb/eri022 CrossRefPubMedGoogle Scholar
  93. 93.
    Coe RA, Lin H (2017) Light-response curves in land plants. In: Covshoff S (ed) Photosynthesis: methods and protocols. Springer Press, New YorkGoogle Scholar
  94. 94.
    Emerson R, Chalmers RV (1958) Speculations concerning the function and phylogenetic significance of the accessory pigments of algae. Phycol Soc News Bull 11:51–56Google Scholar
  95. 95.
    Hill R, Bendall F (1960) Function of the two cytochrome components in chloroplasts: A working hypothesis. Nature 186(4719):136–137CrossRefGoogle Scholar
  96. 96.
    Kromdijk J, Głowacka K, Leonelli L, Gabilly ST, Iwai M, Niyogi KK, Long SP (2016) Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354(6314):857–861. https://doi.org/10.1126/science.aai8878 CrossRefPubMedGoogle Scholar
  97. 97.
    Singsaas E, Ort D, DeLucia E (2001) Variation in measured values of photosynthetic quantum yield in ecophysiological studies. Oecologia 128(1):15–23. https://doi.org/10.1007/s004420000624 CrossRefPubMedGoogle Scholar
  98. 98.
    Skillman JB (2008) Quantum yield variation across the three pathways of photosynthesis: not yet out of the dark. J Exp Bot 59(7):1647–1661. https://doi.org/10.1093/jxb/ern029 CrossRefPubMedGoogle Scholar
  99. 99.
    Serôdio J, Ezequiel J, Frommlet J, Laviale M, Lavaud J (2013) A method for the rapid generation of nonsequential light-response curves of chlorophyll fluorescence. Plant Phys 163(3):1089–1102. https://doi.org/10.1104/pp.113.225243 CrossRefGoogle Scholar
  100. 100.
    Loreto F, Harley PC, Di Marco G, Sharkey TD (1992) Estimation of mesophyll conductance to CO2 flux by three different methods. Plant Phys 98(4):1437–1443. https://doi.org/10.1104/pp.98.4.1437 CrossRefGoogle Scholar
  101. 101.
    Kuhlgert S, Austic G, Zegarac R, Osei-Bonsu I, Hoh D, Chilvers MI, Roth MG, Bi K, TerAvest D, Weebadde P, Kramer DM (2016) MultispeQ Beta: a tool for large-scale plant phenotyping connected to the open PhotosynQ network. R Soc Open Sci 3(10):160592. https://doi.org/10.1098/rsos.160592 CrossRefPubMedPubMedCentralGoogle Scholar
  102. 102.
    Korte A, Farlow A (2013) The advantages and limitations of trait analysis with GWAS: a review. Plant Methods 9(1):29. https://doi.org/10.1186/1746-4811-9-29 CrossRefPubMedPubMedCentralGoogle Scholar
  103. 103.
    Koornneef M, Alonso-Blanco C, Vreugdenhil D (2004) Naturally occurring genetic variation in Arabidopsis thaliana. Annu Rev Plant Biol 55:141–172CrossRefPubMedGoogle Scholar
  104. 104.
    Perdomo JA, Sales CRG, Carmo-Silva E (2017) Quantification of photosynthetic enzymes in leaf extracts by immunoblotting. In: Covshoff S (ed) Photosynthesis: methods and protocols, vol 1. Springer Press, New YorkGoogle Scholar
  105. 105.
    Orr DJ, Carmo-Silva E (2017) Extraction of Rubisco to determine catalytic constants. In: Covshoff S (ed) Photosynthesis: methods and protocols, vol 1. Springer Press, New YorkGoogle Scholar
  106. 106.
    Sales CRG, Degen GE, da Silva AB, Carmo-Silva E (2017) Spectrophotometric determination of Rubisco activity and activation state in leaf extracts. In: Covshoff S (ed) Photosynthesis: methods and protocols, vol 1. Springer Press, New YorkGoogle Scholar
  107. 107.
    Kirchhoff H, Yarbrough R (2017) Evaluation of lipids for the study of photosynthetic membranes. In: Covshoff S (ed) Photosynthesis: methods and protocols, vol 1. Springer Press, New YorkGoogle Scholar
  108. 108.
    Palmer WM, Flynn JR, Martin AP, Reed SL, Grof CPL, White RG, Furbank RT (2017) 3D clearing and molecular labeling in plant tissues. In: Covshoff S (ed) Photosynthesis: methods and protocols, vol 1. Springer Press, New YorkGoogle Scholar
  109. 109.
    Khoshravesh R, Sage TL (2017) Creating leaf cell suspensions for characterization of mesophyll and bundle sheath cellular features. In: Covshoff S (ed) Photosynthesis: methods and protocols, vol 1. Springer Press, New YorkGoogle Scholar
  110. 110.
    Serbin SP, Dillaway DN, Kruger EL, Townsend PA (2011) Leaf optical properties reflect variation in photosynthetic metabolism and its sensitivity to temperature. J Exp Bot 63(1):489–502CrossRefPubMedPubMedCentralGoogle Scholar
  111. 111.
    Yendrek C, Tomaz T, Montes CM, Cao Y, Morse AM, Brown PJ, McIntyre L, Leakey A, Ainsworth E (2016) High-throughput phenotyping of maize leaf physiology and biochemistry using hyperspectral reflectance. Plant Phys. https://doi.org/10.1104/pp.16.01447
  112. 112.
    Stinziano JR, Morgan PB, Lynch DJ, Saathoff AJ, McDermitt DK, Hanson DT (2017) The rapid A–Ci response: photosynthesis in the phenomic era. Plant Cell Environ 40(8):1256–1262. https://doi.org/10.1111/pce.12911 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Berkley J. Walker
    • 1
  • Florian A. Busch
    • 2
  • Steven M. Driever
    • 3
  • Johannes Kromdijk
    • 4
  • Tracy Lawson
    • 5
  1. 1.Biochemistry of PlantsHeinrich-Heine UniversityDüsseldorfGermany
  2. 2.Research School of Biology and ARC Centre of Excellence for Translational PhotosynthesisThe Australian National UniversityActonAustralia
  3. 3.Centre for Crop Systems AnalysisWageningen University and ResearchWageningenThe Netherlands
  4. 4.Carl R. Woese Institute for Genomic BiologyUniversity of IllinoisUrbanaUSA
  5. 5.School of Biological SciencesUniversity of EssexColchesterUK

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