**Author details**

Jorge Marques da Silva

Department of Plant Biology, Biosystems and Integrative Sciences Institute, University of Lisbon, Lisbon, Portugal

#### **References**

[1] United Nations (2014) Concise Report on the World Population Situation in 2014. Department of Economic and Social Affairs, Population Division, United Nations, New York.

[2] Godfray HCJ, Beddington JR, Crute JI, Haddad L, Lawrence D, Muir JF, Pretty J, Robinson S, Thomas S, Toulmin C (2010) Food security: the challenge of feeding 9 billion people. Science 327: 812–818.

**Technique Potential Limitations Current use**

equipment

**Table 1.** Applications of chlorophyll a fluorescence techniques in high-throughput plant phenotyping.

cence techniques, integrated in a systems approach to plant phenomics.

Note: JPPC: Jülich Plant Phenotyping Centre [119]; IPK: Leibniz Institute of Plant Genetics and Crop Plant Research

Chl fluorescence techniques will continue to play a major role on HTPP. Among these, imaging-PAM techniques will play a pivotal role, although specific cases will require different technological solutions. Moreover, field HTPP, which is expected to be fostered in the forthcoming years, will require technologies not dependent on sample dark adaptations and able to operate at medium-range distance, where the family of techniques based on LIF may play a role. Finally, the development of low-cost HTPP platforms [128], required to improve plant breeding in developing countries, is expected to make use of the less expensive Chl measurement techniques, namely passive fluorescence. On the other hand, high-technology in-house HTPP platforms are expected to make simultaneously use of different Chl fluores‐

Department of Plant Biology, Biosystems and Integrative Sciences Institute, University of

[1] United Nations (2014) Concise Report on the World Population Situation in 2014. Department of Economic and Social Affairs, Population Division, United Nations, New

Most protocols need a darkadaptation period; measurements possible only at close range Expensive and sensitive

Imaging PAM Allows mapping of the

12 Applied Photosynthesis - New Progress

**5. Prospective**

**Author details**

Jorge Marques da Silva

Lisbon, Lisbon, Portugal

**References**

York.

photosynthetic heterogeneity over an autotrophic surface; facilitates replication.

[120]; M3P: INRA—Montpellier Plant Phenotyping Platforms [124].

**Userdeveloped**

JPPC [123]; M3P

**Commercial**

PlantScreen (Photon System Instruments)


[30] Ralph PJ, Gademann R, Dennison WC (1998) In situ seagrass photosynthesis measured using a submersible, pulse-amplitude modulated fluorometer. Marine Biology 132: 367– 373.

[17] Parry MA, Hawkesford MJ (2012) An integrated approach to crop genetic improvement.

[18] Scheibe R, Backhausen JE, Emmerlich V, Holtgrefe S (2005) Strategies to maintain redox homeostasis during photosynthesis under changing conditions. Journal of Experimental

[19] Berberan-Santos MN, Bodunov EN, Valeur B (2005) Mathematical functions for the analysis of luminescence decays with underlying distributions 1. Kohlrausch decay

[20] Berberan-Santos MN, Bodunov EN, Valeur B (2008) Luminescence decays with underlying distributions of rate constants: general properties and selected cases. In: Fluorescence of Supermolecules, Polymers and Nano-systems, pp. 67–103 (Berberan-

[21] Li L, Zhang Q, Huang D (2014) A review of imaging techniques for plant phenotyping.

[22] Kautsky H, Hirsch A (1931) Neue Versuche zur Kohlensäureassimilation (New

[23] Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation

[24] Stokes GG (1852) On the change of refrangibility of light. Philosophical Transactions of

[25] Marques da Silva J, Bernardes da Silva A, Pádua M (2007) Modulated chlorophyll a fluorescence: a tool for teaching photosynthesis. Journal of Biological Education 41: 178–

[26] Cavaco AM, Antunes MDC, Marques da Silva J, Antunes R, Guerra R (2009) Preliminary results on the non-invasive diagnosis of superficial scald in 'Rocha' pear by fluorescence imaging. In: Proceedings of the 1st International Workshop in Computer Image Analysis

[27] Guerra R, Gardé I, Antunes M, Marques da Silva J, Antunes R, Cavaco AM (2012) A possibility for non-invasive diagnosis of superficial scald in 'Rocha' pear based on chlorophyll a fluorescence, colorimetry, and the relation between alpha-farnesene and

[28] Breia R, Vieira S, Marques da Silva J, Gerós H, Cunha A (2013) Mapping grape berry photosynthesis by chlorophyll fluorescence imaging: the effect of saturating pulse

[29] Ralph PJ, Schreiber U, Gademann R, Kühl M, Larkum AWD (2005) Coral photobiology studied with a new imaging pulse amplitude modulated fluorometer. Journal of

intensity in different tissues. Photochemistry & Photobiology 89: 579–585.

experiments on carbonic acid assimilation). Naturwissenschaften 19: 48.

function (stretched exponential). Chemical Physics 315: 171–182.

Journal of Integrative Plant Biology 54 (4): 250–259.

Botany 56 (416): 1481–1489.

14 Applied Photosynthesis - New Progress

Santos MN ed.), Springer, Berlin.

fluorometer. Photosynthesis Research 10: 51–62.

the Royal Society of London 142: 463–562.

in Agriculture, pp. 121–127, Potsdam.

Phycology 41: 335–342.

conjugated trienols. Scientia Horticulturae 134: 127–138.

Sensors 14: 20078–20111.

183.


[54] Demetriou G, Neonaki C, Navakoudis E, Kotzabasis K (2007) Salt stress impact on the molecular structure and function of the photosynthetic apparatus—the protective role of polyamines. Biochimica et Biophysica Acta 1767: 272–280.

[42] Misra AN, Misra M, Singh R (2012) Chlorophyll fluorescence in plant biology. In:

[43] Cendrero-Mateo MP, Moran MS, Papuga SA, Thorp KR, Alonso L, Moreno J, Ponce-Campos G, Rascher U, Wang G (2015) Plant chlorophyll fluorescence: active and passive measurements at canopy and leaf scales with different nitrogen treatments. Journal of

[45] Malkin S, Kok B (1966) Fluorescence induction studies in isolated chloroplasts. I. Number of components involved in the reaction and quantum yields. Biochimica Biophysica

[46] Lichtenthaler H, Rinderle U (1988) The role of chlorophyll fluorescence in the detection of stress conditions in plants. Critical Reviews in Analytical Chemistry 19: 29–85.

[47] Strasser RJ (1986) Mono- bi- tri- and polypartite models in photosynthesis. Photosynthesis

[48] Strasser BJ, Strasser RJ (1995) Measuring fast fluorescence transients to address environmental questions: the JIP‐test. In: Photosynthesis: From Light to Biosphere, pp.

[49] Strasser BJ (1997) Donor side capacity of photosystem II probed by chlorophyll a

[50] Govindjee (1995) Sixty-three years since Kautsky: chlorophyll a fluorescence. Australian

[51] Kalaji HM, Schansker G, Ladle RJ, Goltsev V, Bosa K, Allakhverdiev SI, Brestic M, Bussotti F, Calatayud A, Dabrowski P, Elsheery NI, Ferroni L, Guidi L, Hogewoning SW, Jajoo A, Misra AN, Nebauer SG, Pancaldi S, Penella C, Poli D, Pollastrini M, Romanowska-Duda ZB, Rutkowska B, Serôdio J, Suresh K, Szulc W, Tambussi E, Yanniccari M, Zivcak M (2014) Frequently asked questions about in vivo chlorophyll

[52] Srivastava A, Guissé B, Greppin H, Strasser RJ (1997) Regulation of antenna structure and electron transport in photosystem II of *Pisum sativum* under elevated temperature probed by the fast polyphasic chlorophyll a fluorescence transient: OKJIP. Biochimica

[53] Tsimilli‐Michael M, Eggenberg P, Biro B, Köves‐Pechy K, Vörös I, Strasser RJ (2000) Synergistic and antagonistic effects of arbuscular mycorrhizal fungi and *Azospirillum* and *Rizhobium* nitrogen‐fixers on the photosynthetic activity of alfalfa probed by the polyphasic chlorophyll a fluorescence transient O‐J‐I‐P. Applied Soil Ecology 15: 169–

977–980 (Mathis P ed.), Kluwer Academic Publishers, Dordrecht.

fluorescence: practical issues. Photosynthesis Research 122: 121–158.

fluorescence transients. Photosynthesis Research 52: 147–155.

Journal of Plant Physiology 22: 131–160.

et Biophysica Acta 1320: 95–106.

182.

[44] Hill R (1937) Oxygen evolved by isolated chloroplasts. Nature 139: 881–882.

Biophysics, pp. 171–192 (Misra AN ed.), InTech, Rijeka.

Experimental Botany 67 (1): 275–286.

Acta 126: 413–432.

16 Applied Photosynthesis - New Progress

Research 10: 255–276.


and Hydrology V", pp. 652–657 (Owe M, D'Urso G, Moreno JF, Calera A eds.), SPIE Press, Bellingham.

[78] Fateyeva NL, Klimkin AV, Bender OV, Zotikova AP, Yamburov MS (2006) Analysis of laser-induced fluorescence in wood plants under nitrogen soil pollution. Atmospheric and Oceanic Optics 19: 189–192.

[65] Zuev VV, Zueva NE, Grishaev MV (2009) Seasonal variations of fluorescence of Scotch pine according to data of measurements at Siberian Lidar Station. Atmospheric and

[66] Saito Y, Saito R, Kawahara TD, Nomura A, Takeda S (2000) Development and performance characteristics of laser-induced fluorescence imaging lidar for forestry

[67] Saito Y, Kurihara K, Takahashi H, Kobayashi F, Kawahara T, Nomura A, Takeda S (2002) Remote estimation of the chlorophyll concentration of living trees using laser-

[68] Richards TJ, Schuerger AC, Capelle G, Guikema JA (2003) Laser-induced fluorescence spectroscopy of dark- and light-adapted bean (*Phaseolus vulgaris* L.) and wheat (*Triticum aestivum* L.) plants grown under three irradiance levels and subjected to fluctuating

[69] Chappelle EW, Wood Jr. FM, McMurtrey III JE, Newcomb W (1984) Laser-induced fluorescence of green plants. 1: A technique for the remote detection of plant stress and

[70] Brach EJ, Molnar JM, Jasmin JJ (1977) Detection of lettuce maturity and variety by remote sensing techniques. Journal of Agricultural Engineering Research 22: 45–54.

[71] Lüdeker W Dahn H-G, Günther HP (1996) Detection of fungal infection of plants by laser-induced fluorescence: an attempt to use remote sensing. Journal of Plant Physiology

[72] Pereira FMV, Milori DMBP, Pereira-Filho ER, Venâncio AL, Russo MST, Cardinali MCB, Martins PK, Freitas-Astúa J (2011) Laser-induced fluorescence imaging method to monitor citrus greening disease. Computers and Electronics in Agriculture 79: 90–93.

[73] Lavrov A, Utkin AB, Marques da Silva J, Vilar R, Santos NM, Alves B (2012) Water stress assessment of cork oak leaves and maritime pine needles based on LIF spectra. Optics

[74] Gameiro C, Utkin AB, Cartaxana P, Marques da Silva J, Matos AR (2015) The use of laser induced chlorophyll fluorescence (LIF) as a fast and non-destructive method to investigate water deficit in Arabidopsis. Agricultural Water Management 164 (1): 127–

[75] Edner H, Johansson J, Svanberg S, Wallinder E (1994) Fluorescence lidar multicolor

[76] Grishin AI, Krekov GM, Krekova MM, Matvienko GG, Sukhanov AY, Timofeev VI, Fateyeva NL, Lisenko AA (2007) Investigation of organic aerosol of plants with

[77] Fateyeva NL, Matvienko GG (2004) Application of the method of laser-induced fluorescence. In: SPIE Proceedings 5232 "Remote Sensing for Agriculture, Ecosystems,

imaging of vegetation. Applied Optics 33: 2471–2479.

fluorescence lidar. Atmospheric and Ocean Optics 20: 328–337.

applications. Forest Ecology and Management 128: 129–137.

induced fluorescence imaging lidar. Optical Review 9 (2): 37–39.

lighting conditions. Remote Sensing of Environment 84: 323–341.

species identification. Applied Optics 23 (1): 134.

Oceanic Optics 22 (1): 42–48.

18 Applied Photosynthesis - New Progress

148: 579–585.

136.

and Spectroscopy 112: 271–279.


[102] Marques da Silva J (2007) Chlorophyll fluorescence parameters of three Mediterranean shrubs in a summer-autumn period in central Portugal. Biologia Plantarum 51: 741– 745.

[89] Raesch AR, Muller O, Pieruschka R, Rascher U (2014) Field observations with laserinduced fluorescence transient (LIFT) method in barley and sugar beet. Agriculture 4:

[90] Baker N, Bradbury M (1981) Possible applications of chlorophyll fluorescence techniques for studying photosynthesis in vivo. In: Plants and the Daylight Spectrum, pp. 355–

[91] Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. Journal of

[92] Kitajima M, Butler WL (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochimica et Biophysica

[93] Björkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170: 489–504.

[94] Havaux M, Strasser R (1992) Plasticity of the stress tolerance of the photosystem II in vivo. In: Research in Photosynthesis, vol. IV, pp. 149–152 (Murata N ed.), Kluwer

[95] Kovács L, Damkjaer J, Kereiche S, Ilioaia C, Ruban AV, Boekema EJ, Jansson S, Horton P (2006) Lack of the light-harvesting complex CP24 affects the structure and function of the grana membranes of higher plant chloroplasts. The Plant Cell 18 (11): 3106–3120.

[96] Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence.

[97] Serôdio J, Vieira S, Cruz S, Barroso F (2005) Short-term variability in the photosynthetic activity of microphytobenthos as detected by measuring rapid light curves using variable

[98] Perkins RG, Mouget JL, Lefebvre S, Lavaud J (2006) Light response curve methodology and possible implications in the application of chlorophyll fluorescence to benthic

[99] Nogués S, Baker NR (2000) Effects of drought on photosynthesis in Mediterranean plants grown under enhanced UV‐B radiation. Journal of Experimental Botany 51: 1309–

[100] Marques da Silva J, Arrabaça MC (l992). Characteristics of fluorescence emission by leaves of nitrogen starved *Paspalum dilatatum* POIR. Photosynthetica 26 (2): 253–256.

[101] Munne-Bosch S, Penuelas J (2003) Photo- and antioxidative protection, and a role for salicylic acid during drought and recovery in field-grown *Phillyrea angustifolia* plants.

372 (Smith H ed.), Academic Press, London.

Experimental Botany 51: 659–668.

Academic Publishers, Dordrecht.

Biochimica et Biophysica Acta 990: 87–92.

fluorescence. Marine Biology 146: 903–914.

diatoms. Marine Biology 149: 703–712.

1317.

Planta 217: 758–766.

Acta 376: 105–115.

159–169.

20 Applied Photosynthesis - New Progress

