Dynamic response of plant chlorophyll fluorescence to light, water and nutrient availability
M. Pilar Cendrero-Mateo A B F H , A. Elizabete Carmo-Silva C G , Albert Porcar-Castell D , Erik P. Hamerlynck B , Shirley A. Papuga A E and M. Susan Moran B
+ Author Affiliations
- Author Affiliations
A Soil Water and Environmental Science, The University of Arizona, 1177 East Fourth Street, Tucson 85721, USA.
B USDA Southwest Watershed Research Centre, 2000 East Allen Road, Tucson, AZ 85719, USA.
C USDA Arid-Land Agricultural Research Center, 21881 North Cardon Lane, Maricopa, AZ 85138, USA.
D Department of Forest Sciences, University of Helsinki, PO Box 27, 00014 Helsinki, Finland.
E School of Natural Resources, The University of Arizona, 325 Biosciences East, Tucson, AZ 85721, USA.
F Present address: Institute of Bio- and Geosciences, Forschungszentrum Jülich GmbH, Leo-Brandt-Str., 52425 Jülich, Germany.
G Present address: Rothamsted Research, Plant Biology and Crop Science, Harpenden, Herts., AL5 2JQ, UK.
H Corresponding author. Email: p.cendrero@fz-juelich.de
Functional Plant Biology 42(8) 746-757 https://doi.org/10.1071/FP15002
Submitted: 8 January 2015 Accepted: 21 April 2015 Published: 1 June 2015
Abstract
Chlorophyll molecules absorb photosynthetic active radiation (PAR). The resulting excitation energy is dissipated by three competing pathways at the level of photosystem: (i) photochemistry (and, by extension, photosynthesis); (ii) regulated and constitutive thermal energy dissipation; and (iii) chlorophyll-a fluorescence (ChlF). Because the dynamics of photosynthesis modulate the regulated component of thermal energy dissipation (widely addressed as non-photochemical quenching (NPQ)), the relationship between photosynthesis, NPQ and ChlF changes with water, nutrient and light availability. In this study we characterised the relationship between photosynthesis, NPQ and ChlF when conducting light-response curves of photosynthesis in plants growing under different water, nutrient and ambient light conditions. Our goals were to test whether ChlF and photosynthesis correlate in response to water and nutrient deficiency, and determine the optimum PAR level at which the correlation is maximal. Concurrent gas exchange and ChlF light-response curves were measured for Camelina sativa (L.) Crantz and Triticum durum (L.) Desf plants grown under (i) intermediate light growth chamber conditions, and (ii) high light environment field conditions respectively. Plant stress was induced by withdrawing water in the chamber experiment, and applying different nitrogen levels in the field experiment. Our study demonstrated that ChlF was able to track the variations in photosynthetic capacity in both experiments, and that the light level at which plants were grown was optimum for detecting both water and nutrient deficiency with ChlF. The decrease in photosynthesis was found to modulate ChlF via different mechanisms depending on the treatment: through the action of NPQ in response to water stress, or through the action of changes in leaf chlorophyll concentration in response to nitrogen deficiency. This study provides support for the use of remotely sensed ChlF as a proxy to monitor plant stress dynamics from space.
Additional keywords: nitrogen, non-photochemical quenching, photosynthesis, water deficit.
References
Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annual Review of Plant Physiology and Plant Molecular Biology 50, 601–639.| The water–water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkt1yktr0%3D&md5=38dc5a3182287eec0281a2a43a9c0b4fCAS | 15012221PubMed |
Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annual Review of Plant Biology 59, 89–113.
| Chlorophyll fluorescence: a probe of photosynthesis in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqsL8%3D&md5=33f955b1e24713e0894a7b2e44b9779aCAS | 18444897PubMed |
Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. Journal of Experimental Botany 55, 1607–1621.
| Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntValtrw%3D&md5=17e6d870fdb31172760fae6521695047CAS | 15258166PubMed |
Björkman O (1981) Responses to different quantum flux densities. In ‘Physiological plant ecology I’. (Eds PDOL Lange, PPS Nobel, PCB Osmond, PDH Ziegler) pp. 57–107. (Springer: Berlin)
Buschmann C (2007) Variability and application of the chlorophyll fluorescence emission ratio red/far-red of leaves. Photosynthesis Research 92, 261–271.
| Variability and application of the chlorophyll fluorescence emission ratio red/far-red of leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXosFKqu7Y%3D&md5=796012b369a05637b0dac05dc167ae0cCAS | 17525834PubMed |
Chaves MM (1991) Effects of water deficits on carbon assimilation. Journal of Experimental Botany 42, 1–16.
| Effects of water deficits on carbon assimilation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXhtFyntrw%3D&md5=85622ff776b9917e97f96cb34de6734eCAS |
Choudhury BJ (2001) Estimating gross photosynthesis using satellite and ancillary data: approach and preliminary results. Remote Sensing of Environment 75, 1–21.
| Estimating gross photosynthesis using satellite and ancillary data: approach and preliminary results.Crossref | GoogleScholarGoogle Scholar |
Delegido J, Alonso L, González G, Moreno J (2010) Estimating chlorophyll content of crops from hyperspectral data using a normalized area over reflectance curve (NAOC). International Journal of Applied Earth Observation and Geoinformation 12, 165–174.
| Estimating chlorophyll content of crops from hyperspectral data using a normalized area over reflectance curve (NAOC).Crossref | GoogleScholarGoogle Scholar |
Demmig-Adams B, Adams WW (1992) Photoprotection and other responses of plants to high light stress. Annual Review of Plant Physiology and Plant Molecular Biology 43, 599–626.
| Photoprotection and other responses of plants to high light stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xks1Knu70%3D&md5=a487c3f3d7f6863f0b0fbac9cde54d89CAS |
Demmig-Adams B, Adams WW (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytologist 172, 11–21.
| Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVyisrnE&md5=497a5c0bf8ec24a4dd9d9bad57a7ad7eCAS | 16945085PubMed |
Ensminger I, Busch F, Huner NPA (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiologia Plantarum 126, 28–44.
| Photostasis and cold acclimation: sensing low temperature through photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFKjtbs%3D&md5=1c3262c75df06e0221eccaf22b2fed75CAS |
Flexas J, Medrano H (2002) Drought‐inhibition of photosynthesis in C3 plants: stomatal and non‐stomatal limitations revisited. Annals of Botany 89, 183–189.
| Drought‐inhibition of photosynthesis in C3 plants: stomatal and non‐stomatal limitations revisited.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkslymsLs%3D&md5=23f4b7dd87bafbfc33253bf248580c34CAS | 12099349PubMed |
Flexas J, Escalona JM, Medrano H (1999) Water stress induces different levels of photosynthesis and electron transport rate regulation in grapevines. Plant, Cell & Environment 22, 39–48.
| Water stress induces different levels of photosynthesis and electron transport rate regulation in grapevines.Crossref | GoogleScholarGoogle Scholar |
Fröhlich A, Rice B (2005) Evaluation of Camelina sativa oil as a feedstock for biodiesel production. Industrial Crops and Products 21, 25–31.
| Evaluation of Camelina sativa oil as a feedstock for biodiesel production.Crossref | GoogleScholarGoogle Scholar |
Gamon JA, Peñuelas J, Field CB (1992) A narrow-waveband spectral index that tracks diurnal changes in photosynthetic efficiency. Remote Sensing of Environment 41, 35–44.
| A narrow-waveband spectral index that tracks diurnal changes in photosynthetic efficiency.Crossref | GoogleScholarGoogle Scholar |
Gilmore AM (1997) Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves. Physiologia Plantarum 99, 197–209.
| Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjtFWrt70%3D&md5=41a979dfc25219ab7df2d3a030a3abf9CAS |
Keck Institute for Space Studies (2013) ‘New methods for measurements of photosynthesis from space.’ (Keck Institute for Space Studies: Pasadena, CA)
Kou J, Takahashi S, Oguchi R, Fan D-Y, Badger MR, Chow WS (2013) Estimation of the steady-state cyclic electron flux around PSI in spinach leaf discs in white light, CO2-enriched air and other varied conditions. Functional Plant Biology 40, 1018–1028.
| Estimation of the steady-state cyclic electron flux around PSI in spinach leaf discs in white light, CO2-enriched air and other varied conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVKltLrO&md5=8c2afebd694c4d95dabed160ea0cf59bCAS |
Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynthesis Research 79, 209–218.
| New fluorescence parameters for the determination of QA redox state and excitation energy fluxes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtV2qu70%3D&md5=581084d3ac2b7cce5755a180a50d4f16CAS | 16228395PubMed |
Krause GH, Weis E (1984) Chlorophyll fluorescence as a tool in plant physiology. Photosynthesis Research 5, 139–157.
| Chlorophyll fluorescence as a tool in plant physiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXlt1Kku7o%3D&md5=62f6ba0f88ae83af25562e865e043118CAS | 24458602PubMed |
Laisk A, Oja V, Rasulov B, Eichelmann H, Sumberg A (1997) Quantum yields and rate constants of photochemical and nonphotochemical excitation quenching (experiment and model). Plant Physiology 115, 803–815.
Magnani F, Raddi S, Porcar-Castell A (2014) Modelling photochemistry from seasonal changes in steady-state fluorescence under field conditions in Pinus sylvestris. In ‘5th International Workshop on Remote Sensing of Vegetation Fluorescence’. (European Space Agency (ESA: Paris)
Makino A, Miyake C, Yokota A (2002) Physiological functions of the water–water cycle (Mehler reaction) and the cyclic electron flow around PSI in rice leaves. Plant & Cell Physiology 43, 1017–1026.
| Physiological functions of the water–water cycle (Mehler reaction) and the cyclic electron flow around PSI in rice leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XntlGjurk%3D&md5=695852de0cc6887da0c8b84aa3afa806CAS |
Malenovsky Z, Mishra KB, Zemek F, Rascher U, Nedbal L (2009) Scientific and technical challenges in remote sensing of plant canopy reflectance and fluorescence. Journal of Experimental Botany 60, 2987–3004.
| Scientific and technical challenges in remote sensing of plant canopy reflectance and fluorescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpsValsbg%3D&md5=3c85b2e3f8a24f988ce314b517883d82CAS | 19465688PubMed |
Martin EC (2007) Arizona irrigation scheduling system (AZSched). Available at http://ag.arizona.edu/crop/irrigation/azsched/azsched.html [Verified 30 April 2015]
Meroni M, Rossini M, Guanter L, Alonso L, Rascher U, Colombo R, Moreno J (2009) Remote sensing of solar-induced chlorophyll fluorescence: Review of methods and applications. Remote Sensing of Environment 113, 2037–2051.
| Remote sensing of solar-induced chlorophyll fluorescence: Review of methods and applications.Crossref | GoogleScholarGoogle Scholar |
Mohammed G, Goulas Y, Magnani F, Moreno J, Olejníčková J, Rascher U, van der Tol C, Verhoef W, Ač A, Daumard F, Galle A, Malenovský Z, Pernokis D, Rivera JP, Verrelst J, Drusch M (2014) 2012 FLEX/Sentinel-3 tandem mission photosynthesis study. Final report no. ESTEC Contract no. 4000106396/12/NL/AF.
Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiology 125, 1558–1566.
| Non-photochemical quenching. A response to excess light energy.Crossref | GoogleScholarGoogle Scholar | 11299337PubMed |
Niinemets U, Kull O, Tenhunen JD (1999) Variability in leaf morphology and chemical composition as a function of canopy light environment in coexisting deciduous trees. International Journal of Plant Sciences 160, 837–848.
| Variability in leaf morphology and chemical composition as a function of canopy light environment in coexisting deciduous trees.Crossref | GoogleScholarGoogle Scholar | 10506464PubMed |
Porcar-Castell A (2011) A high-resolution portrait of the annual dynamics of photochemical and non-photochemical quenching in needles of Pinus sylvestris. Physiologia Plantarum 143, 139–153.
| A high-resolution portrait of the annual dynamics of photochemical and non-photochemical quenching in needles of Pinus sylvestris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1WjtrnE&md5=e0b764e6009a8ce2e3d4edf6c7289816CAS | 21615415PubMed |
Porcar-Castell A, Garcia-Plazaola JI, Nichol CJ, Kolari P, Olascoaga B, Kuusinen N, Fernández-Marín B, Pulkkinen E, Nikinmaa E (2012) Physiology of the seasonal relationship between the photochemical reflectance index and photosynthetic light use efficiency. Oecologia 170, 313–323.
| Physiology of the seasonal relationship between the photochemical reflectance index and photosynthetic light use efficiency.Crossref | GoogleScholarGoogle Scholar | 22481306PubMed |
Porcar-Castell A, Tyystjärvi E, Atherton J, van der Tol C, Flexas J, Pfündel E, Moreno J, Frankenberg C, Berry JA (2014) Linking chlorophyll-a fluorescence to photosynthesis for remote sensing applications: mechanisms and challenges. Journal of Experimental Botany 65, 4065–4095.
| Linking chlorophyll-a fluorescence to photosynthesis for remote sensing applications: mechanisms and challenges.Crossref | GoogleScholarGoogle Scholar | 24868038PubMed |
Rawson HM, Gómez Macpherson H (2000) ‘Irrigated wheat: managing your crop.’ (FAO: Rome)
Rosema A, Snel JFH, Zahn H, Buurmeijer WF, Van Hove LWA (1998) The relation between laser-induced chlorophyll fluorescence and photosynthesis. Remote Sensing of Environment 65, 143–154.
| The relation between laser-induced chlorophyll fluorescence and photosynthesis.Crossref | GoogleScholarGoogle Scholar |
Schreiber U, Neubauer C (1990) O2-dependent electron flow, membrane energization and the mechanism of non-photochemical quenching of chlorophyll fluorescence. Photosynthesis Research 25, 279–293.
| O2-dependent electron flow, membrane energization and the mechanism of non-photochemical quenching of chlorophyll fluorescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXjs1ek&md5=4746b0a05c8d1b17e8ea1af0fef022cfCAS | 24420358PubMed |
Serôdio J, Lavaud J (2011) A model for describing the light response of the nonphotochemical quenching of chlorophyll fluorescence. Photosynthesis Research 108, 61–76.
| A model for describing the light response of the nonphotochemical quenching of chlorophyll fluorescence.Crossref | GoogleScholarGoogle Scholar | 21516348PubMed |
Stylinski C, Gamon J, Oechel W (2002) Seasonal patterns of reflectance indices, carotenoid pigments and photosynthesis of evergreen chaparral species. Oecologia 131, 366–374.
| Seasonal patterns of reflectance indices, carotenoid pigments and photosynthesis of evergreen chaparral species.Crossref | GoogleScholarGoogle Scholar |
Tyner EH, Webb JR (1946) The relation of corn yields to nutrient balance as revealed by leaf analysis. Agronomy Journal 38, 173–185.
| The relation of corn yields to nutrient balance as revealed by leaf analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaH28XhtlGnug%3D%3D&md5=d942fae42f043d5ce4ba63a66701df64CAS |
van der Tol C, Verhoef W, Rosema A (2009) A model for chlorophyll fluorescence and photosynthesis at leaf scale. Agricultural and Forest Meteorology 149, 96–105.
| A model for chlorophyll fluorescence and photosynthesis at leaf scale.Crossref | GoogleScholarGoogle Scholar |
Verhoef W (2004) Extension of SAIL to model solar-induced canopy fluorescence spectra. In ‘Proceedings of 2nd International Workshop on Remote Sensing of Vegetation Fluorescence, Saint-Hubert, Canada’.
Verhoeven AS, Demmig-Adams B, Adams WW (1997) Enhanced employment of the xanthophyll cycle and thermal energy dissipation in spinach exposed to high light and N stress. Plant Physiology 113, 817–824.
Verma S, Sellers P, Walthall C, Hall F, Kim J, Goetz S (1993) Photosynthesis and stomatal conductance related to reflectance on the canopy scale. Remote Sensing of Environment 44, 103–116.
| Photosynthesis and stomatal conductance related to reflectance on the canopy scale.Crossref | GoogleScholarGoogle Scholar |
Zar JH (1974) ‘Biostatistical analysis.’ (Prentice Hall: Englewood Cliffs, NJ, USA)
