Techniques for photosynthesis phenomics: gas exchange, fluorescence, and reflectance spectrums

Qingfeng Song*, Xin-Guang Zhu*

Crop and Environment ›› 2024, Vol. 3 ›› Issue (3) : 147-158.

PDF
Crop and Environment ›› 2024, Vol. 3 ›› Issue (3) : 147-158. DOI: 10.1016/j.crope.2024.05.002
Review article

Techniques for photosynthesis phenomics: gas exchange, fluorescence, and reflectance spectrums

  • Qingfeng Song*, Xin-Guang Zhu*
Author information +
History +

Abstract

Photosynthesis represents the most important biological process on earth and generates food and energy for most living organisms. Increasing photosynthetic efficiency in crops is a feasible strategy to enhance grain yield. Canopy photosynthesis, the integral of photosynthesis of all photosynthetic tissues of an entire plant canopy, is intrinsically linked to biomass production and crop yield and is influenced by both photosynthetic efficiency at the tissue level and canopy architecture, which determines the light environment at that tissue. This review summarizes current methodologies for measuring photosynthesis via gas exchange, fluorescence, and reflectance spectrum at the field, canopy, and leaf levels. Gas exchange techniques include eddy covariance, canopy gas exchange chambers, and organ-level gas exchange methods, which can measure CO2 and H2O fluxes. Chlorophyll fluorescence methods include solar-induced fluorescence (SIF), laser-induced fluorescence transient (LIFT), pulse amplitude modulated (PAM) fluorescence, and light induced chlorophyll a fluorescence rise (OJIP transient), which can be used to evaluate photosynthetic efficiency and plant stress responses. One of the commonly used reflectance spectrum methods for studying photosynthesis is the hyperspectral reflectance technique, which can estimate photosynthesis-related traits. High-throughput crop photosynthesis phenotyping can be performed with different combinations of these techniques. This review aims to provide a one-stop resource for researchers working in plant physiology, agronomy, and environmental science and working on either crop management or genetic enhancement to address either food security or the response of plants to global climate change.

Keywords

Chlorophyll fluorescence / Gas exchange techniques / Hyperspectral reflectance / Imaging technology / Phenotyping / Photosynthesis

Cite this article

Download citation ▾
Qingfeng Song, Xin-Guang Zhu. Techniques for photosynthesis phenomics: gas exchange, fluorescence, and reflectance spectrums. Crop and Environment, 2024, 3(3): 147‒158 https://doi.org/10.1016/j.crope.2024.05.002

References

[1] Ainsworth E.A., Rogers A., 2007. The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant Cell Environ. 30, 258-270.
[2] Ainsworth E.A., Serbin S.P., Skoneczka J.A., Townsend P.A., 2014. Using leaf optical properties to detect ozone effects on foliar biochemistry. Photosynth. Res. 119, 65-76.
[3] Ananyev G., Kolber Z.S., Klimov D., Falkowski P.G., Berry J.A., Rascher U., Martin R., Osmond B., 2005. Remote sensing of heterogeneity in photosynthetic efficiency, electron transport and dissipation of excess light in Populus deltoides stands under ambient and elevated CO2 concentrations, and in a tropical forest canopy, using a new laser-induced fluorescence transient device. Glob. Change Biol. 11, 1195-1206.
[4] Arriga N., Rannik Ü., Aubinet M., Carrara A., Vesala T., Papale D., 2017. Experimental validation of footprint models for eddy covariance CO2flux measurements above grassland by means of natural and artificial tracers. Agric. For. Meteorol. 242, 75-84.
[5] Assefa Y., Carter P., Hinds M., Bhalla G., Schon R., Jeschke M., Paszkiewicz S., Smith S., Ciampitti I.A., 2018. Analysis of long term study indicates both agronomic optimal plant density and increase maize yield per plant contributed to yield gain. Sci. Rep. 8, 4937.
[6] Aubinet M., Vesala T., Papale D., 2012. Eddy Covariance: a Practical Guide to Measurement and Data Analysis. Springer Science&Business Media, Dordrecht, Netherlands.
[7] Baker N.R.,2008. Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu. Rev. Plant Biol. 59, 89-113.
[8] Baldocchi D.D.,2003. Assessing the eddy covariance technique for evaluating carbon dioxide exchange rates of ecosystems: past, present and future. Glob. Change Biol. 9, 479-492.
[9] Bao Y., Tang L., Srinivasan S., Schnable P.S., 2019. Field-based architectural traits characterisation of maize plant using time-of-flight 3D imaging. Biosys. Eng. 178, 86-101.
[10] Barthel M., Sturm P., Gentsch L., Knohl A., 2010. Technical note: a combined soil/canopy chamber system for tracing δ13C in soil respiration after a 13CO2 canopy pulse labelling. Biogeosci. Disc. 7, 1603-1631.
[11] Bielczynski L.W., Schansker G., Croce R., 2016. Effect of light acclimation on the organization of photosystem II super- and sub-complexes in arabidopsis thaliana. Front. Plant Sci. 7, 105.
[12] Biriukova K., Celesti M., Evdokimov A., Pacheco-Labrador J., Julitta T., Migliavacca M., Giardino C., Miglietta F., Colombo R., Panigada C., Rossini M., 2020. Effects of varying solar-view geometry and canopy structure on solar-induced chlorophyll fluorescence and PRI. Int. J. Appl. Earth Obs. Geoinf. 89, 102069.
[13] Burkart S., Manderscheid R., Weigel H.J., 2007. Design and performance of a portable gas exchange chamber system for CO2- and H2O-flux measurements in crop canopies. Environ. Exp. Bot. 61, 25-34.
[14] Chang T., Shi Z., Zhao H., Song Q., He Z., Van Rie, J., Den Boer, B., Galle, A., Zhu, X., 2022. 3dCAP-wheat: an open-source comprehensive computational framework precisely quantifies wheat foliar, nonfoliar, and canopy photosynthesis. Plant Phenomics 2022, 9758148.
[15] Chang T., Song Q., Zhao H., Chang S., Xin C., Qu M., Zhu X., 2020. An in situ approach to characterizing photosynthetic gas exchange of rice panicle. Plant Methods 16, 92.
[16] Chen J., Cao F., Li H., Shan S., Tao Z., Lei T., Liu Y., Xiao Z., Zou Y., Huang M., Abou-Elwafa S.F., 2020. Genotypic variation in the grain photosynthetic contribution to grain filling in rice. J. Plant Physiol. 253, 153269.
[17] Cogliati S., Rossini M., Julitta T., Meroni M., Schickling A., Burkart A., Pinto F., Rascher U., Colombo R., 2015. Continuous and long-term measurements of reflectance and sun-induced chlorophyll fluorescence by using novel automated field spectroscopy systems. Remote Sens. Environ. 164, 270-281.
[18] Damm A., Erler A., Hillen W., Meroni M., Schaepman M.E., Verhoef W., Rascher U., 2011. Modeling the impact of spectral sensor configurations on the FLD retrieval accuracy of sun-induced chlorophyll fluorescence. Remote Sens. Environ. 115, 1882-1892.
[19] de Barros Dantas L.L., Eldridge B.M., Dorling J., Dekeya R., Lynch D.A., Dodd A.N., 2023. Circadian regulation of metabolism across photosynthetic organisms. Plant J. 116, 650-668.
[20] de Pury D.G.G., Farquhar G.D., 1997. Simple scaling of photosynthesis from leaves to canopies without the errors of big-leaf models. Plant Cell Environ. 20, 537-557.
[21] Dharni J.S., Dhatt B.K., Paul P., Gao T., Awada T., Bacher H., Peleg Z., Staswick P., Hupp J., Yu H., Walia H., 2022. A non-destructive approach for measuring rice panicle-level photosynthetic responses using 3D-image reconstruction. Plant Methods 18, 126.
[22] Emmel C., D’Odorico P., Revill A., Hörtnagl L., Ammann C., Buchmann N., Eugster W., 2020. Canopy photosynthesis of six major arable crops is enhanced under diffuse light due to canopy architecture. Glob. Change Biol. 26, 5164-5177.
[23] Evans J.R.,2013. Improving photosynthesis. Plant Physiol. 162, 1780-1793.
[24] Faralli M., Lawson T., 2020. Natural genetic variation in photosynthesis: an untapped resource to increase crop yield potential? Plant J. 101, 518-528.
[25] Feng X., Zhan Y., Wang Q., Yang X., Yu C., Wang H., Tang Z., Jiang D., Peng C., He Y., 2020. Hyperspectral imaging combined with machine learning as a tool to obtain high-throughput plant salt-stress phenotyping. Plant J. 101, 1448-1461.
[26] Flood P.J., Harbinson J., Aarts M.G.M., 2011. Natural genetic variation in plant photosynthesis. Trends Plant Sci. 16, 327-335.
[27] Fournier C., Andrieu B., Ljutovac S., Saint-Jean S., 2003. ADEL-Wheat: a 3D Architectural Model of Wheat Development. Springer Verlag, Berlin, Germany.
[28] Fu P., Meacham-Hensold K., Siebers M.H., Bernacchi C.J., 2020. The inverse relationship between solar-induced fluorescence yield and photosynthetic capacity: benefits for field phenotyping. J. Exp. Bot. 72, 1295-1306.
[29] Fu P., Montes C.M., Siebers M.H., Gomez-Casanovas N., McGrath J.M., Ainsworth E.A., Bernacchi C.J., 2022. Advances in field-based high-throughput photosynthetic phenotyping. J. Exp. Bot. 73, 3157-3172.
[30] Govindjee E.,1995. Sixty-three years since Kautsky: chlorophyll a fluorescence. Aust. J. Plant Physiol. 22, 131-160.
[31] Graydon J.A., St. Louis V.L., Lindberg S.E., Hintelmann H., Krabbenhoft D.P., 2006. Investigation of mercury exchange between forest canopy vegetation and the atmosphere using a new dynamic chamber. Environ. Sci. Technol. 40, 4680-4688.
[32] Gu L., Massman W.J., Leuning R., Pallardy S.G., Meyers T., Hanson P.J., Riggs J.S., Hosman K.P., Yang B., 2012. The fundamental equation of eddy covariance and its application in flux measurements. Agric. For. Meteorol. 152, 135-148.
[33] Gu L., Wood J.D., Chang C.Y.Y., Sun Y., Riggs J.S., 2019. Advancing terrestrial ecosystem science with a novel automated measurement system for sun-induced chlorophyll fluorescence for integration with eddy covariance flux networks. J. Geophys. Res. Biogeosci. 124, 127-146.
[34] Guo Q., Wu F., Pang S., Zhao X., Chen L., Liu J., Xue B., Xu G., Li L., Jing H., Chu C., 2018. Crop 3D -a LiDAR based platform for 3D high-throughput crop phenotyping. Sci. China Life Sci. 61, 328-339.
[35] He L., Magney T., Dutta D., Yin Y., Köhler P., Grossmann K., Stutz J., Dold C., Hatfield J., Guan K., Peng B., Frankenberg C., 2020. From the ground to space: using solar-induced chlorophyll fluorescence to estimate crop productivity. Geophys. Res. Lett. 47, e2020GL087474.
[36] Hennessey T.L., Field C.B., 1991. Circadian rhythms in photosynthesis: oscillations in carbon assimilation and stomatal conductance under constant conditions. Plant Physiol. 96, 831-836.
[37] Herritt M.T., Pauli D., Mockler T.C., Thompson A.L., 2020. Chlorophyll fluorescence imaging captures photochemical efficiency of grain sorghum (Sorghum bicolor) in a field setting. Plant Methods 16, 109.
[38] Hileman D.R., Huluka G., Kenjige P.K., Sinha N., Bhattacharya N.C., Biswas P.K., Lewin K.F., Nagy J., Hendrey G.R., 1994. Canopy photosynthesis and transpiration of field-grown cotton exposed to free-air CO2 enrichment (FACE) and differential irrigation. Agric. For. Meteorol. 70, 189-207.
[39] Keller B., Vass I., Matsubara S., Paul K., Jedmowski C., Pieruschka R., Nedbal L., Rascher U., Müller O., 2019. Maximum fluorescence and electron transport kinetics determined by light-induced fluorescence transients (LIFT) for photosynthesis phenotyping. Photosynth. Res. 140, 221-233.
[40] Keller B., Zimmermann L., Rascher U., Matsubara S., Steier A., Müller O., 2022. Toward predicting photosynthetic efficiency and biomass gain in crop genotypes over a field season. Plant Physiol. 188, 301-317.
[41] Khan N., Essemine J., Hamdani S., Qu M., Lyu M.J.A., Perveen S., Stirbet A., Govindjee G., Zhu X., 2021. Natural variation in the fast phase of chlorophyll a fluorescence induction curve (OJIP) in a global rice minicore panel. Photosynth. Res. 150, 137-158.
[42] Kim J.H., Lee J.W., Ahn T.I., Shin J.H., Park K.S., Son J.E., 2016. Sweet pepper (Capsicum annuum L.) canopy photosynthesis modeling using 3D plant architecture and light ray-tracing. Front. Plant Sci. 7, 1321.
[43] Kolber Z., Klimov D., Ananyev G., Rascher U., Berry J., Osmond B., 2005. Measuring photosynthetic parameters at a distance: laser induced fluorescence transient (LIFT) method for remote measurements of photosynthesis in terrestrial vegetation. Photosynth. Res. 84, 121-129.
[44] Kono M., Terashima I., 2014. Long-term and short-term responses of the photosynthetic electron transport to fluctuating light. J. Photochem. Photobiol. B Biol. 137, 89-99.
[45] Kramer D.M., Johnson G., Kiirats O., Edwards G.E., 2004. New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth. Res. 79, 209-218.
[46] Krause G.H., Weis E., 1991. Chlorophyll fluorescence and photosynthesis: the basics. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42, 313-349.
[47] Küpper H., Benedikty Z., Morina F., Andresen E., Mishra A., Trtílek M., 2019. Analysis of OJIP chlorophyll fluorescence kinetics and QA reoxidation kinetics by direct fast imaging. Plant Physiol. 179, 369-381.
[48] Lawson T., Milliken A.L., 2023. Photosynthesis-beyond the leaf. New Phytol. 238, 55-61.
[49] Lazár D.,2009. Modelling of light-induced chlorophyll a fluorescence rise (O-J-I-P transient) and changes in 820 nm-transmittance signal of photosynthesis. Photosynthetica 47, 483-498.
[50] Lichtenthaler H.K., Rinderle U., 1988. The role of chlorophyll fluorescence in the detection of stress conditions in plants. Crit. Rev. Anal. Chem. 19, S29-S85.
[51] Long S.P., Bernacchi C.J., 2003. Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. J. Exp. Bot. 54, 2393-2401.
[52] Long S.P., Farage P.K., Garcia R.L., 1996. Measurement of leaf and canopy photosynthetic CO2 exchange in the field. J. Exp. Bot. 47, 1629-1642.
[53] Long S.P., Zhu X., Naidu S.L., Ort D.R., 2006. Can improvement in photosynthesis increase crop yields? Plant Cell Environ. 29, 315-330.
[54] Luo L., Jiang X., Yang Y., Samy E.R.A., Lefsrud M., Hoyos-Villegas V., Sun S., 2023. Eff-3DPSeg: 3D organ-level plant shoot segmentation using annotation-efficient deep learning. Plant Phenomics 5, 0080.
[55] Mao L., Song Q., Li M., Liu X., Shi Z., Chen F., Chen G., Zheng H., Zhu X., 2023. Decreasing photosystem antenna size by inhibiting chlorophyll synthesis: A double-edged sword for photosynthetic efficiency. Crop Environ. 2, 46-58.
[56] Matthews J.S.A., Vialet-Chabrand S., Lawson T., 2018. Acclimation to fluctuating light impacts the rapidity of response and diurnal rhythm of stomatal conductance. Plant Physiol. 176, 1939-1951.
[57] Mauder M., Foken T., Aubinet M., Ibrom A., 2021. Eddy-covariance measurements. In: Handbook of Atmospheric Measurements. Springer, Berlin, Germany, pp. 1473-1504.
[58] Maydup M.L., Antonietta M., Guiamet J.J., Graciano C., López J.R., Tambussi E.A., 2010. The contribution of ear photosynthesis to grain filling in bread wheat (Triticum aestivum L.). Field Crops Res. 119, 48-58.
[59] Meacham-Hensold K., Fu P., Wu J., Serbin S., Montes C.M., Ainsworth E., Guan K., Dracup E., Pederson T., Driever S., Bernacchi C., 2020. Plot-level rapid screening for photosynthetic parameters using proximal hyperspectral imaging. J. Exp. Bot. 71, 2312-2328.
[60] 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 Sens. Environ. 113, 2037-2051.
[61] Molero G., Reynolds M.P., 2020. Spike photosynthesis measured at high throughput indicates genetic variation independent of flag leaf photosynthesis. Field Crops Res. 255, 107866.
[62] Moreau D., Allard V., Gaju O., Le Gouis J., Foulkes J.M., Martre P., 2012. Acclimation of leaf nitrogen to vertical light gradient at anthesis in wheat is a whole-plant process that scales with the size of canopy. Plant Physiol. 160, 1479-1490.
[63] Müller J., Eschenröder A., Diepenbrock W., 2009. Through-flow chamber CO2/H2O canopy gas exchange system-Construction, microclimate, errors, and measurements in a barley (Hordeum vulgare L.) field. Agric. For. Meteorol. 149, 214-229.
[64] Müller O., Keller B., Zimmermann L., Jedmowski C., Kleist E., Pingle V., Acebron K., Dos Santos, N.Z., Steier, A., Freiwald, L., Munoz-Fernandez, I., Wilke, N., Kraska, T., Pieruschka, R., Schurr, U., Rascher, U., 2018. Field phenotyping and an example of proximal sensing of photosynthesis under elevated CO2. In: International Geoscience and Remote Sensing Symposium (IGARSS), Valencia, Spain, pp. 8252-8254.
[65] Nedbal L., Whitmarsh J., 2004. Chlorophyll fluorescence imaging of leaves and fruits. In: Papageorgiou, G.C., Govindjee (Eds.), Chlorophyll a Fluorescence: A Signature of Photosynthesis. Springer, Dordrecht, Netherlands, pp. 389-407.
[66] Ortiz D., Hu J., Salas Fernandez M.G., 2017. Genetic architecture of photosynthesis in Sorghum bicolor under non-stress and cold stress conditions. J. Exp. Bot. 68, 4545-4557.
[67] 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, 1195-1205.
[68] Parry M.A.J., Reynolds M., Salvucci M.E., Raines C., Andralojc P.J., Zhu X., Price G.D., Condon A.G., Furbank R.T., 2011. Raising yield potential of wheat. II. Increasing photosynthetic capacity and efficiency. J. Exp. Bot. 62, 453-467.
[69] Paul M.J., Pellny T.K., 2003. Carbon metabolite feedback regulation of leaf photosynthesis and development. J. Exp. Bot. 54, 539-547.
[70] Peng S., Krieg D.R., 1991. Single leaf and canopy photosynthesis response to plant age in cotton. Agron. J. 83, 704-708.
[71] Pérez-Bueno M.L., Pineda M., Barón M., 2019. Phenotyping plant responses to biotic stress by chlorophyll fluorescence imaging. Front. Plant Sci. 10, 1135.
[72] Pérez-Priego O., Testi L., Orgaz F., Villalobos F.J., 2010. A large closed canopy chamber for measuring CO2and water vapour exchange of whole trees. Environ. Exp. Bot. 68, 131-138.
[73] Pieruschka R., Klimov D., Kolber Z.S., Berry J.A., 2010. Monitoring of cold and light stress impact on photosynthesis by using the laser induced fluorescence transient (LIFT) approach. Funct. Plant Biol. 37, 395-402.
[74] Pinto F., Damm A., Schickling A., Panigada C., Cogliati S., Müller-Linow M., Ballvora A., Rascher U., 2016. Sun-induced chlorophyll fluorescence from high- resolution imaging spectroscopy data to quantify spatio-temporal patterns of photosynthetic function in crop canopies. Plant Cell Environ. 39, 1500-1512.
[75] Qu M., Zheng G., Hamdani S., Essemine J., Song Q., Wang H., Chu C., Sirault X., Zhu X., 2017. Leaf photosynthetic parameters related to biomass accumulation in a global rice diversity survey. Plant Physiol. 175, 248-258.
[76] Quero G., Bonnecarrère V., Simondi S., Santos J., Fernández S., Gutierrez L., Garaycochea S., Borsani O., 2021. Genetic architecture of photosynthesis energy partitioning as revealed by a genome-wide association approach. Photosynth. Res. 150, 97-115.
[77] Rascher U., Alonso L., Burkart A., Cilia C., Cogliati S., Colombo R., Damm A., Drusch M., Guanter L., Hanus J., Hyvärinen T., Julitta T., Jussila J., Kataja K., Kokkalis P., Kraft S., Kraska T., Matveeva M., Moreno J., Müller O., Panigada C., Pikl M., Pinto F., Prey L., Pude R., Rossini M., Schickling A., Schurr U., Schüttemeyer D., Verrelst J., Zemek F., 2015. Sun-induced fluorescence -a new probe of photosynthesis: First maps from the imaging spectrometer HyPlant. Glob. Change Biol. 21, 4673-4684.
[78] Roberts D.A., Roth K.L., Wetherley E.B., Meerdink S.K., Perroy R.L., 2018. Hyperspectral vegetation indices. In: Hyperspectral Indices and Image Classifications for Agriculture and Vegetation. CRC Press, Florida, U.S.A., pp. 3-26
[79] Rousseau C., Belin E., Bove E., Rousseau D., Fabre F., Berruyer R., Guillaumès J., Manceau C., Jacques M.A., Boureau T., 2013. High throughput quantitative phenotyping of plant resistance using chlorophyll fluorescence image analysis. Plant Methods 9, 17.
[80] Sanchez-Bragado R., Molero G., Reynolds M.P., Araus J.L., 2016. Photosynthetic contribution of the ear to grain filling in wheat: a comparison of different methodologies for evaluation. J. Exp. Bot. 67, 2787-2798.
[81] Sanchez-Bragado R., Vicente R., Molero G., Serret M.D., Maydup M.L., Araus J.L., 2020. New avenues for increasing yield and stability in C3 cereals: exploring ear photosynthesis. Curr. Opin. Plant Biol. 56, 223-234.
[82] Scholes J.D., Rolfe S.A., 2009. Chlorophyll fluorescence imaging as tool for understanding the impact of fungal diseases on plant performance: a phenomics perspective. Funct. Plant Biol. 36, 880-892.
[83] Schreiber U.,2004. Pulse-Amplitude-Modulation (PAM) fluorometry and saturation pulse method: an overview. In: Papageorgiou, G.C., Govindjee (Eds.), Chlorophyll a Fluorescence: A Signature of Photosynthesis. Springer, Dordrecht, Netherlands, pp. 279-319.
[84] Serbin S.P., Dillaway D.N., Kruger E.L., Townsend P.A., 2012. Leaf optical properties reflect variation in photosynthetic metabolism and its sensitivity to temperature. J. Exp. Bot. 63, 489-502.
[85] Shu M., Shen M., Zuo J., Yin P., Wang M., Xie Z., Tang J., Wang R., Li B., Yang X., Ma Y., 2021. The application of UAV-based hyperspectral imaging to estimate crop traits in maize inbred lines. Plant Phenomics 2021, 9890745.
[86] Silva-Perez V., Molero G., Serbin S.P., Condon A.G., Reynolds M.P., Furbank R.T., Evans J.R., 2018. Hyperspectral reflectance as a tool to measure biochemical and physiological traits in wheat. J. Exp. Bot. 69, 483-496.
[87] Slattery R.A., Ort D.R., 2021. Perspectives on improving light distribution and light use efficiency in crop canopies. Plant Physiol. 185, 34-48.
[88] Smith P., Lanigan G., Kutsch W.L., Buchmann N., Eugster W., Aubinet M., Ceschia E., Béziat P., Yeluripati J.B., Osborne B., Moors E.J., Brut A., Wattenbach M., Saunders M., Jones M., 2010. Measurements necessary for assessing the net ecosystem carbon budget of croplands. Agric. Ecosyst. Environ. 139, 302-315.
[89] Song Q., Chu C., Parry M.A.J., Zhu X., 2016a. Genetics-based dynamic systems model of canopy photosynthesis: the key to improve light and resource use efficiencies for crops. Food Energy Secur. 5, 18-25.
[90] Song Q., Liu F., Bu H., Zhu X., 2023. Quantifying contributions of different factors to canopy photosynthesis in 2 maize varieties: development of a novel 3D canopy modeling pipeline. Plant Phenomics 5, 0075.
[91] Song Q., Van Rie J., Den Boer B., Galle A., Zhao H., Chang T., He Z., Zhu X.G., 2022. Diurnal and seasonal variations of photosynthetic energy conversion efficiency of field grown wheat. Front. Plant Sci. 13, 817654.
[92] Song Q., Xiao H., Xiao X., Zhu X., 2016b. A new canopy photosynthesis and transpiration measurement system (CAPTS) for canopy gas exchange research. Agric. For. Meteorol. 217, 101-107.
[93] Song Q., Zhang G., Zhu X., 2013. Optimal crop canopy architecture to maximise canopy photosynthetic CO2uptake under elevated CO2 -a theoretical study using a mechanistic model of canopy photosynthesis. Funct. Plant Biol. 40, 109-124.
[94] Song Q., Zhu X., 2024. Measuring canopy gas exchange using canopy photosynthesis and transpiration systems (CAPTS). In: Covshoff, S. (Ed.), Photosynthesis: Methods and Protocols. Springer, New York, U.S.A., pp. 213-226.
[95] Steduto P., Cetinkoku O., Albrizio R., Kanber R., 2002. Automated closed-system canopy-chamber for continuous field-crop monitoring of CO2 and H2O fluxes. Agric. For. Meteorol. 111, 171-186.
[96] 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.
[97] Strauss A.J., Kruger G.H.J., Strasser R.J., Heerden P.D.R.V., 2006. Ranking of dark chilling tolerance in soybean genotypes probed by the chlorophyll a fluorescence transient O-J-I-P. Environ. Exp. Bot. 56, 147.
[98] Tanaka Y., Adachi S., Yamori W., 2019. Natural genetic variation of the photosynthetic induction response to fluctuating light environment. Curr. Opin. Plant Biol. 49, 52-59.
[99] Testa G., Reyneri A., Blandino M., 2016. Maize grain yield enhancement through high plant density cultivation with different inter-row and intra-row spacings. Eur. J. Agron. 72, 28-37.
[100] Thach L.B., Shapcott A., Schmidt S., Critchley C., 2007. The OJIP fast fluorescence rise characterizes Graptophyllum species and their stress responses. Photosynth. Res. 94, 423-436.
[101] Theeuwen T.P.J.M., Logie L.L., Harbinson J., Aarts M.G.M., 2022. Genetics as a key to improving crop photosynthesis. J. Exp. Bot. 73, 3122-3137.
[102] Townsend A.J., Retkute R., Chinnathambi K., Randall J.W.P., Foulkes J., Carmo-Silva E., Murchie E.H., 2018. Suboptimal acclimation of photosynthesis to light in wheat canopies. Plant Physiol. 176, 1233-1246.
[103] van Bezouw R.F.H.M., Keurentjes J.J.B., Harbinson J., Aarts M.G.M., 2019. Converging phenomics and genomics to study natural variation in plant photosynthetic efficiency. Plant J. 97, 112-133.
[104] Vekuri H., Tuovinen J.P., Kulmala L., Papale D., Kolari P., Aurela M., Laurila T., Liski J., Lohila A., 2023. A widely-used eddy covariance gap-filling method creates systematic bias in carbon balance estimates. Sci. Rep. 13, 1720.
[105] Vialet-Chabrand S., Dreyer E., Brendel O., 2013. Performance of a new dynamic model for predicting diurnal time courses of stomatal conductance at the leaf level. Plant Cell Environ. 36, 1529-1546.
[106] Wagner S.W., Reicosky D.C., 1992. Closed-chamber effects on leaf temperature, canopy photosynthesis, and evapotranspiration. Agron. J. 84, 731-738.
[107] Wagner S.W., Reicosky D.C., Alessi R.S., 1997. Regression models for calculating gas fluxes measured with a closed chamber. Agron. J. 89, 279-284.
[108] Wang H., Qian X., Zhang L., Xu S., Li H., Xia X., Dai L., Xu L., Yu J., Liu X., 2018. A method of high throughput monitoring crop physiology using chlorophyll fluorescence and multispectral imaging. Front. Plant Sci. 9, 00407.
[109] Wang L., Yang Y., Zhang S., Che Z., Yuan W., Yu D., 2020. GWAS reveals two novel loci for photosynthesis-related traits in soybean. Mol. Genet. Genom. 295, 705-716.
[110] Wang N., Suomalainen J., Bartholomeus H., Kooistra L., Masiliunas D., Clevers J.G.P.W., 2021. Diurnal variation of sun-induced chlorophyll fluorescence of agricultural crops observed from a point-based spectrometer on a UAV. Int. J. Appl. Earth Obs. Geoinf. 96, 102276.
[111] Wang Y., Xi W., Wang Z., Wang B., Xu X., Han M., Zhou S., Zhang Y., 2016. Contribution of ear photosynthesis to grain yield under rainfed and irrigation conditions for winter wheat cultivars released in the past 30 years in North China Plain. J. Integr. Agric. 15, 2247-2256.
[112] Wei J., Tang X., Gu Q., Wang M., Ma M., Han X., 2019. Using solar-induced chlorophyll fluorescence observed by OCO-2 to predict autumn crop production in China. Rem. Sens. 11, 1715.
[113] Wu A., Hammer G.L., Doherty A., von Caemmerer S., Farquhar G.D., 2019. Quantifying impacts of enhancing photosynthesis on crop yield. Nat. Plants 5, 380-388.
[114] Wu S., Wen W., Wang Y., Fan J., Wang C., Gou W., Guo X., 2020. MVS-Pheno: a portable and low-cost phenotyping platform for maize shoots using multiview stereo 3D reconstruction. Plant Phenomics 2020, 1848437.
[115] Xiao S., Fei S., Li Q., Zhang B., Chen H., Xu D., Cai Z., Bi K., Guo Y., Li B., Chen Z., Ma Y., 2023. The importance of using realistic 3D canopy models to calculate light interception in the field. Plant Phenomics 5, 0082.
[116] Xin C., Yang J., Zhu X., 2013. A model of chlorophyll a fluorescence induction kinetics with explicit description of structural constraints of individual photosystem II units. Photosynth. Res. 117, 339-354.
[117] Xu R., Li C., 2022. A review of high-throughput field phenotyping systems: focusing on ground robots. Plant Phenomics 2022, 9760269.
[118] Yan H., Fu Y., Xiao X., Huang H., He H., Ediger L., 2009. Modeling gross primary productivity for winter wheat-maize double cropping system using MODIS time series and CO2 eddy flux tower data. Agric. Ecosyst. Environ. 129, 391-400.
[119] Yang X., Tang J., Mustard J.F., Lee J.E., Rossini M., Joiner J., Munger J.W., Kornfeld A., Richardson A.D., 2015. Solar-induced chlorophyll fluorescence that correlates with canopy photosynthesis on diurnal and seasonal scales in a temperate deciduous forest. Geophys. Res. Lett. 42, 2977-2987.
[120] Yendrek C.R., Tomaz T., Montes C.M., Cao Y., Morse A.M., Brown P.J., McIntyre L.M., Leakey A.D.B., Ainsworth E.A., 2017. High-throughput phenotyping of maize leaf physiological and biochemical traits using hyperspectral reflectance. Plant Physiol. 173, 614-626.
[121] Yi Q., López-Malvar A., Álvarez-Iglesias L., Romay M.C., Revilla P., 2023. Genome- wide association analysis identified newly natural variation for photosynthesis-related traits in a large maize panel. Agronomy 13, 801.
[122] Zarco-Tejada P.J., Catalina A., González M.R., Martín P., 2013. Relationships between net photosynthesis and steady-state chlorophyll fluorescence retrieved from airborne hyperspectral imagery. Remote Sens. Environ. 136, 247-258.
[123] Zavafer A., Labeeuw L., Mancilla C., 2020. Global trends of usage of chlorophyll fluorescence and projections for the next decade. Plant Phenomics 2020, 6293145.
[124] Zelitch I.,1982. The close relationship between net photosynthesis and crop yield. Bioscience 32, 796-802.
[125] Zendonadi Dos Santos N., Piepho H.P., Condorelli G.E., Licieri Groli E., Newcomb M., Ward R., Tuberosa R., Maccaferri M., Fiorani F., Rascher U., Müller O., 2021. High-throughput field phenotyping reveals genetic variation in photosynthetic traits in durum wheat under drought. Plant Cell Environ. 44, 2858-2878.
[126] Zhai Y., Zhou L., Qi H., Gao P., Zhang C., 2023. Application of visible/near-infrared spectroscopy and hyperspectral imaging with machine learning for high-throughput plant heavy metal stress phenotyping: a review. Plant Phenomics 5, 0124.
[127] Zhang F., Zhu K., Wang Y., Zhang Z., Lu F., Yu H., Zou J., 2019. Changes in photosynthetic and chlorophyll fluorescence characteristics of sorghum under drought and waterlogging stress. Photosynthetica 57, 1156-1164.
[128] Zhang Q., Tang W., Peng S., Li Y., 2022. Limiting factors for panicle photosynthesis at the anthesis and grain filling stages in rice (Oryza sativa L.). Plant J. 109, 77-91.
[129] Zheng B., Shi L., Ma Y., Deng Q., Li B., Guo Y., 2008. Comparison of architecture among different cultivars of hybrid rice using a spatial light model based on 3-D digitising. Funct. Plant Biol. 35, 900-910.
[130] Zhu X., Long S.P., Ort D.R., 2010. Improving photosynthetic efficiency for greater yield. Annu. Rev. Plant Biol. 61, 235-261.
[131] Zhu X., Song Q., Ort D.R., 2012. Elements of a dynamic systems model of canopy photosynthesis. Curr. Opin. Plant Biol. 15, 237-244.
Funding
* E-mail addresses: songqf@cemps.ac.cn (Q. Song), zhuxg@cemps.ac.cn (X.-G. Zhu).
PDF

Accesses

Citations

Detail

Sections
Recommended

/