Chlorophyll Fluorescence for High-Throughput Screening of Plants During Abiotic Stress, Aging, and Genetic Perturbation

Chapter

Summary

Chlorophyll (Chl) is nature’s gift to oxygenic photosynthetic organisms which capture solar radiation and convert it into chemical energy to drive the whole process of photosynthesis for proper growth and development of plants. Understanding the responses of photosynthetic apparatus in crop plants under various stress conditions has become a major target for many research programs. In this chapter, we describe the principal of Chl fluorescence and the recent advances in the application of Chl fluorescence. Chl fluorescence measurement is one of the most useful, cost-effective, and non-invasive tools to measure efficiency of photosystem II photochemistry. Incorporated with improved imaging and computer technologies, it can be utilized on a small or large scale for examination of photosynthetic performance, stress tolerance, and aging. Further advancements are being made to develop efficient more tools to apply Chl fluorescence measurement for large-scale high-throughput photosynthesis phenotyping, forestry and crop management.

Keywords

Chlorophyll fluorescence High-throughput screening Photosynthesis Abiotic stress Aging Large-scale phenomics studies Forestry and crop management 

References

  1. Allen JF (1975) Oxygen reduction and optimum production of ATP in photosynthesis. Nature 256:599–600. doi: 10.1038/256599a0 CrossRefGoogle Scholar
  2. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399.CrossRefPubMedGoogle Scholar
  3. Araújo WL, Nunes-Nesi A, Fernie AR (2014) On the role of plant mitochondrial metabolism and its impact on photosynthesis in both optimal and sub-optimal growth conditions. Photosynth Res 119:141–156.CrossRefPubMedGoogle Scholar
  4. Araus JL, Cairns JE (2014) Field high-throughput phenotyping: the new crop breeding frontier. Trends Plant Sci 19:52–61. doi: 10.1016/j.tplants.2013.09.008 CrossRefPubMedGoogle Scholar
  5. Arnon DI (1959) Conversion of light into chemical energy in photosynthesis. Nature 184:10–20.PubMedGoogle Scholar
  6. Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: An overview. Photosynthetica 51:163–190.CrossRefGoogle Scholar
  7. Baker NR (2008) Chlorophyll Fluorescence: A Probe of Photosynthesis In Vivo. Annu Rev Plant Biol 59:89–113. doi: 10.1146/annurev.arplant.59.032607.092759 CrossRefPubMedGoogle Scholar
  8. Baker NR, Harbinson J, Kramer DM (2007) Determining the limitations and regulation of photosynthetic energy transduction in leaves. Plant, cell & Environ 30:1107–1125.CrossRefGoogle Scholar
  9. Balazadeh S, Riaño-Pachón DM, Mueller-Roeber B (2008) Transcription factors regulating leaf senescence In Arabidopsis thaliana. Plant Biol 10:63–75. doi: 10.1111/plb.2008.10.issue-s1 CrossRefPubMedGoogle Scholar
  10. Baret F, Guyot G (1991) Potentials and limits of vegetation indices for LAI and APAR assessment. Remote Sens Environ 35:161–173.CrossRefGoogle Scholar
  11. Björkman O, Demmig-Adams B (1995) Regulation of photosynthetic light energy capture, conversion, and dissipation in leaves of higher plants. In: Ecophysiology of photosynthesis. Springer, pp 17–47Google Scholar
  12. Björn LO, Papageorgiou GC, Blankenship RE, Govindjee (2009) A viewpoint: Why chlorophyll a? Photosynth Res 99:85–98. doi: 10.1007/s11120-008-9395-x CrossRefPubMedGoogle Scholar
  13. Breeze E, Harrison E, McHattie S, et al (2011) High-Resolution Temporal Profiling of Transcripts during Arabidopsis Leaf Senescence Reveals a Distinct Chronology of Processes and Regulation. Plant Cell 23:873–894. doi: 10.1105/tpc.111.083345 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Buchanan-Wollaston V (1997) The molecular biology of leaf senescence. J Exp Bot 48:181–199.CrossRefGoogle Scholar
  15. Chaerle L, Leinonen I, Jones HG, Van Der Straeten D (2007) Monitoring and screening plant populations with combined thermal and chlorophyll fluorescence imaging. J Exp Bot 58:773–784.CrossRefPubMedGoogle Scholar
  16. Cortese K, Diaspro A, Tacchetti C (2009) Advanced Correlative Light/Electron Microscopy: Current Methods and New Developments Using Tokuyasu Cryosections. J Histochem Cytochem 57:1103–1112. doi: 10.1369/jhc.2009.954214 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Damm A, Elbers JAN, Erler A, et al (2010) Remote sensing of sun-induced fluorescence to improve modeling of diurnal courses of gross primary production (GPP). Glob Chang Biol 16:171–186.CrossRefGoogle Scholar
  18. Dobrowski SZ, Pushnik JC, Zarco-Tejada PJ, Ustin SL (2005) Simple reflectance indices track heat and water stress-induced changes in steady-state chlorophyll fluorescence at the canopy scale. Remote Sens Environ 97:403–414.CrossRefGoogle Scholar
  19. Dohleman FG, Long SP (2009) More productive than maize in the Midwest: how does Miscanthus do it? Plant Physiol 150:2104–2115.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Eberhard S, Finazzi G, Wollman F-A (2008) The Dynamics of Photosynthesis. Annu Rev Genet 42:463–515. doi: 10.1146/annurev.genet.42.110807.091452 CrossRefPubMedGoogle Scholar
  21. Finkel E (2009) With “Phenomics,” Plant Scientists Hope to Shift Breeding Into Overdrive. Science 325:380–381.Google Scholar
  22. Flexas J, Briantais J-M, Cerovic Z, et al (2000) Steady-state and maximum chlorophyll fluorescence responses to water stress in grapevine leaves: a new remote sensing system. Remote Sens Environ 73:283–297.CrossRefGoogle Scholar
  23. Flexas J, Escalona JM, Evain S, et al (2002) Steady-state chlorophyll fluorescence (Fs) measurements as a tool to follow variations of net CO2 assimilation and stomatal conductance during water-stress in C3 plants. Physiol Plant 114:231–240.CrossRefPubMedGoogle Scholar
  24. Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant, Cell & Environ 28:1056–1071.CrossRefGoogle Scholar
  25. Freedman A, Cavender-Bares J, Kebabian PL, et al (2002) Remote sensing of solar-excited plant fluorescence as a measure of photosynthetic rate. Photosynthetica 40:127–132.CrossRefGoogle Scholar
  26. Furbank RT, Tester M (2011) Phenomics – technologies to relieve the phenotyping bottleneck. Trends Plant Sci. 16:635–644.CrossRefPubMedGoogle Scholar
  27. Gamon JA, Field CB, Bilger W, et al (1990) Remote sensing of the xanthophyll cycle and chlorophyll fluorescence in sunflower leaves and canopies. Oecologia 85:1–7.CrossRefPubMedGoogle Scholar
  28. Garbulsky MF, Filella I, Verger A, Peñuelas J (2013) Photosynthetic light use efficiency from satellite sensors: From global to Mediterranean vegetation.Google Scholar
  29. Gepstein S (2004) Leaf senescence-not just awear and tear’phenomenon. Genome Biol 5:212–212.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930.CrossRefPubMedGoogle Scholar
  31. Govindjee (1995) 63 Years since Kautsky Chlorphyll -a fluorescence. Aust J Plant Physiol 131–160.Google Scholar
  32. Guo Y, Gan S (2005) Leaf Senescence: Signals, Execution, and Regulation. ElsevierGoogle Scholar
  33. Havaux M, Niyogi KK (1999) The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proc Natl Acad Sci 8762–8767.Google Scholar
  34. Hörtensteiner S (2009) Stay-green regulates chlorophyll and chlorophyll-binding protein degradation during senescence. Trends Plant Sci 14:155–162. doi: 10.1016/j.tplants.2009.01.002 CrossRefPubMedGoogle Scholar
  35. Huner NPA, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci. 3:224–230.CrossRefGoogle Scholar
  36. Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim et Biophys Acta 1817:182–193. doi: 10.1016/j.bbabio.2011.04.012 CrossRefGoogle Scholar
  37. Khush GS (2001) Green revolution: the way forward. Nat Rev Genet 2:815–822.CrossRefPubMedGoogle Scholar
  38. Kim HJ, Ryu H, Hong SH, et al (2006) Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis. Proc Natl Acad Sci United States Am 103:814–819.CrossRefGoogle Scholar
  39. Kim JH, Woo HR, Kim J, et al (2009) Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis. Science 323:1053–1057.CrossRefPubMedGoogle Scholar
  40. Konishi A, Eguchi A, Hosoi F, Omasa K (2009) 3D monitoring spatio–temporal effects of herbicide on a whole plant using combined range and chlorophyll a fluorescence imaging. Funct Plant Biol 36:874–879.CrossRefGoogle Scholar
  41. Kreslavski VD, Zorina AA, Los DA, Fomina IR, and Allakhverdiev SI (2013) Molecular Mechanisms of StressResistance of Photosynthetic Machinery. Mol. Stress Physiol. Plants 21–50.Google Scholar
  42. Kusaba M, Ito H, Morita R, et al (2007) Rice NON-YELLOW COLORING1 Is Involved in Light-Harvesting Complex II and Grana Degradation during Leaf Senescence. Plant Cell 19:1362–1375. doi: 10.1105/tpc.106.042911 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Kusaba M, Tanaka A, Tanaka R (2013) Stay-green plants: what do they tell us about the molecular mechanism of leaf senescence. Photosynth Res 117:221–234.CrossRefPubMedGoogle Scholar
  44. Lausch A, Pause M, Merbach I, et al (2013) A new multiscale approach for monitoring vegetation using remote sensing-based indicators in laboratory, field, and landscape. Environ Monit Assess 185:1215–1235.CrossRefPubMedGoogle Scholar
  45. Li J, Pandeya D, Nath K, et al (2010) ZEBRA-NECROSIS, a thylakoid-bound protein, is critical for the photoprotection of developing chloroplasts during early leaf development. Plant J 62:713–725.CrossRefPubMedGoogle Scholar
  46. Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136. doi: 10.1146/annurev.arplant.57.032905.105316 CrossRefPubMedGoogle Scholar
  47. Lu Y, Hall DA, Last RL (2011a) A small zinc finger thylakoid protein plays a role in maintenance of photosystem II in Arabidopsis thaliana. Plant Cell 1861–1875.Google Scholar
  48. Lu Y, Savage LJ, Larson MD, et al (2011b) Chloroplast 2010: a database for large-scale phenotypic screening of Arabidopsis mutants. Plant Physiol 155:1589–1600.CrossRefPubMedPubMedCentralGoogle Scholar
  49. Malenovsky Z, Mishra KB, Zemek F, et al (2009) Scientific and technical challenges in remote sensing of plant canopy reflectance and fluorescence. J Exp Bot 60:2987–3004.CrossRefPubMedGoogle Scholar
  50. Matile P, Schellenberg M, Peisker C (1992) Production and release of a chlorophyll catabolite in isolated senescent chloroplasts. Planta 187:230–235.CrossRefPubMedGoogle Scholar
  51. Maxwell K (2000) Chlorophyll fluorescence–a practical guide. J Exp Bot 51:659–668. doi: 10.1093/jexbot/51.345.659 PubMedGoogle Scholar
  52. Meroni M, Rossini M, Guanter L, et al (2009) Remote sensing of solar-induced chlorophyll fluorescence: Review of methods and applications. Remote Sens Environ 113:2037–2051.CrossRefGoogle Scholar
  53. Miller MB, Tang Y-W (2009) Basic concepts of microarrays and potential applications in clinical microbiology. Clin Microbiol Rev 22:611–633.CrossRefPubMedPubMedCentralGoogle Scholar
  54. Mishra A, Mishra KB, Höermiller II, et al (2011) Chlorophyll fluorescence emission as a reporter on cold tolerance in Arabidopsis thaliana accessions.Google Scholar
  55. Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19.CrossRefPubMedGoogle Scholar
  56. Mohapatra PK, Joshi P, Ramaswamy NK, et al (2013) Damage of photosynthetic apparatus in the senescing basal leaf of Arabidopsis thaliana: A plausible mechanism of inactivation of reaction center II. Plant Physiol Biochem 62:116–121.CrossRefPubMedGoogle Scholar
  57. Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566.CrossRefPubMedPubMedCentralGoogle Scholar
  58. Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot 64:3983–3998.CrossRefPubMedGoogle Scholar
  59. Nath K, Jajoo A, Poudyal RS, et al (2013a) Towards a critical understanding of the photosystem II repair mechanism and its regulation during stress conditions. FEBS Lett 587:3372–3381. doi: 10.1016/j.febslet.2013.09.015 CrossRefPubMedGoogle Scholar
  60. Nath K, Phee B-K, Jeong S, et al (2013b) Age-dependent changes in the functions and compositions of photosynthetic complexes in the thylakoid membranes of Arabidopsis thaliana. Photosynth. Res. 117:547–556.CrossRefPubMedGoogle Scholar
  61. Nath K, Poudyal RS, Eom J-S, et al (2013c) Loss-of-function of OsSTN8 suppresses the photosystem II core protein phosphorylation and interferes with the photosystem II repair mechanism in rice (Oryza sativa). Plant J 76:675–686. doi: 10.1111/tpj.2013.76.issue-4 CrossRefPubMedGoogle Scholar
  62. Oh M-H (2003) Increased Stability of LHCII by Aggregate Formation during Dark-Induced Leaf Senescence in the Arabidopsis Mutant, ore10. Plant Cell Physiol. 44:1368–1377.CrossRefPubMedGoogle Scholar
  63. Oh SA, Park J-H, Lee GI, et al (1997) Identification of three genetic loci controlling leaf senescence in Arabidopsis thaliana. Plant J 12:527–535.CrossRefPubMedGoogle Scholar
  64. Omasa K, Konishi A, Tamura H, Hosoi F (2009) 3D confocal laser scanning microscopy for the analysis of chlorophyll fluorescence parameters of chloroplasts in intact leaf tissues. Plant cell Physiol 50:90–105.CrossRefPubMedGoogle Scholar
  65. Oxborough K, Baker NR (1997) An instrument capable of imaging chlorophyll a fluorescence from intact leaves at very low irradiance and at cellular and subcellular levels of organization. Plant, Cell & Environ 20:1473–1483.CrossRefGoogle Scholar
  66. Park S-Y, Yu J-W, Park J-S, et al (2007) The Senescence-Induced Staygreen Protein Regulates Chlorophyll Degradation. Plant Cell 19:1649–1664. doi: 10.1105/tpc.106.044891 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Pennell RI, Lamb C (1997) Programmed cell death in plants.Google Scholar
  68. Porcar-Castell A (2011) A high-resolution portrait of the annual dynamics of photochemical and non-photochemical quenching in needles of Pinus sylvestris. Physiol Plant 143:139–153.CrossRefPubMedGoogle Scholar
  69. Pottier M, Masclaux-Daubresse C, Yoshimoto K, Thomine S (2014) Autophagy as a possible mechanism for micronutrient remobilization from leaves to seeds. Front Plant Sci. doi: 10.3389/fpls.2014.00011 PubMedPubMedCentralGoogle Scholar
  70. Rascher U, Agati G, Alonso L, et al (2009) CEFLES2: the remote sensing component to quantify photosynthetic efficiency from the leaf to the region by measuring sun-induced fluorescence in the oxygen absorption bands.Google Scholar
  71. Rascher U, Damm A, van der Linden S, et al (2010) Sensing of photosynthetic activity of crops. In: Precision Crop Protection-the Challenge and Use of Heterogeneity. Springer, pp 87–99Google Scholar
  72. Rauf M, Arif M, Dortay H, et al (2013) ORE1 balances leaf senescence against maintenance by antagonizing G2-like-mediated transcription. EMBO reports – Issue 14:382–388. doi: 10.1038/embor.2013.24 CrossRefGoogle Scholar
  73. Rousseau C, Belin E, Bove E, et al (2013) High throughput quantitative phenotyping of plant resistance using chlorophyll fluorescence image analysis. Plant Methods 9:17.CrossRefPubMedPubMedCentralGoogle Scholar
  74. Saibo NJM, Lourenco T, Oliveira MM (2009) Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses. Ann. Bot. 103:609–622.CrossRefPubMedGoogle Scholar
  75. Sakuraba Y, Schelbert S, Park S-Y, et al (2012) STAY-GREEN and Chlorophyll Catabolic Enzymes Interact at Light-Harvesting Complex II for Chlorophyll Detoxification during Leaf Senescence in Arabidopsis. Plant Cell 24:507–518. doi: 10.1105/tpc.111.089474 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Sharkey TD (2005) Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene. Plant, Cell & Environ 28:269–277.CrossRefGoogle Scholar
  77. Slonim DK, Yanai I, Troyanskaya OG (2009) Getting Started in Gene Expression Microarray Analysis. PLoS Comput Biol 5:1000543. doi: 10.1371/journal.pcbi.1000543 CrossRefGoogle Scholar
  78. Soukupová J, Cséfalvay L, Urban O, et al (2008) Annual variation of the steady-state chlorophyll fluorescence emission of evergreen plants in temperate zone. Funct Plant Biol 35:63–76.CrossRefGoogle Scholar
  79. Sperdouli I, Moustakas M (2011) Spatio-temporal heterogeneity in Arabidopsis thaliana leaves under drought stress. Plant Biol. doi: 10.1111/j.1438-8677.2011.00473.x PubMedGoogle Scholar
  80. Stirbet A, Govindjee (2011) On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: Basics and applications of the OJIP fluorescence transient. J Photochem Photobiol B: Biol 104:236–257. doi: 10.1016/j.jphotobiol.2010.12.010 CrossRefGoogle Scholar
  81. Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13:178–182. doi: 10.1016/j.tplants.2008.01.005 CrossRefPubMedGoogle Scholar
  82. Tessmer OL, Jiao Y, Cruz JA, et al (2013) Functional approach to high-throughput plant growth analysis. BMC Syst Biol 7:1–13.CrossRefGoogle Scholar
  83. Thomas H, Howarth CJ (2000) Five ways to stay green. J Exp Bot 51:329–337.CrossRefPubMedGoogle Scholar
  84. Thomas H, Ougham H, Canter P, Donnison I (2002) What stay-green mutants tell us about nitrogen remobilization in leaf senescence. J Exp Bot 53:801–808.CrossRefPubMedGoogle Scholar
  85. Tikkanen M, Nurmi M, Kangasjärvi S, Aro E-M (2008) Core protein phosphorylation facilitates the repair of photodamaged photosystem II at high light. Biochim et Biophys Acta 1777:1432–1437.CrossRefGoogle Scholar
  86. Vranova E, Inze D, Van Breusegem F (2002) Signal transduction during oxidative stress. J Exp Bot 53:1227–1236.CrossRefPubMedGoogle Scholar
  87. Whitmarsh J (1999) The photosynthetic process. In: Concepts in Photobiology. Springer, pp 11–51Google Scholar
  88. Woo HR, Chung KM, Park J-H, et al (2001) ORE9, an F-box protein that regulates leaf senescence in Arabidopsis. Plant Cell 1779–1790.Google Scholar
  89. Woo HR, Kim JH, Nam HG, Lim PO (2004) The delayed leaf senescence mutants of Arabidopsis, ore1, ore3, and ore9 are tolerant to oxidative stress. Plant Cell Physiol 45:923–932.CrossRefPubMedGoogle Scholar
  90. Woo HR, Kim HJ, Nam HG, Lim PO (2012) Plant leaf senescence and death – regulation by multiple layers of control and implications for aging in general. J cell Sci 126:4823–4833. doi: 10.1242/jcs.109116 CrossRefGoogle Scholar
  91. Yang Z, Ohlrogge JB (2008) Turnover of fatty acids during natural senescence of Arabidopsis, Brachypodium, and switchgrass and in Arabidopsis ?-oxidation mutants. Plant Physiol 150:1981–1989.CrossRefGoogle Scholar
  92. Zarco-Tejada PJ, Pushnik JC, Dobrowski S, Ustin SL (2003) Steady-state chlorophyll a fluorescence detection from canopy derivative reflectance and double-peak red-edge effects. Remote Sens Environ 283–294.Google Scholar
  93. Zarco-Tejada PJ, Morales A, Testi L, Villalobos FJ (2013) Spatio-temporal patterns of chlorophyll fluorescence and physiological and structural indices acquired from hyperspectral imagery as compared with carbon fluxes measured with eddy covariance. Remote Sens Environ 133:102–115.CrossRefGoogle Scholar
  94. Zivcak M, Brestic M, Kalaji HM, Govindjee (2014) Photosynthetic responses of sun- and shade-grown barley leaves to high light: is the lower PSII connectivity in shade leaves associated with protection against excess of light? Photosynth. Res. 119:339–354.Google Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Department of Biological SciencesWestern Michigan UniversityKalamazooUSA

Personalised recommendations