{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,11,18]],"date-time":"2025-11-18T09:20:11Z","timestamp":1763457611618,"version":"build-2065373602"},"reference-count":54,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2017,6,14]],"date-time":"2017-06-14T00:00:00Z","timestamp":1497398400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Australian Research Council Discovery grant","award":["DP140101488"],"award-info":[{"award-number":["DP140101488"]}]},{"name":"Australian Government Research Training Program Scholarship"},{"DOI":"10.13039\/501100001777","name":"University of Wollongong","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100001777","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Remote Sensing"],"abstract":"<jats:p>Solar induced chlorophyll fluorescence (SIF) emissions of photosynthetically active plants retrieved from space-borne observations have been used to improve models of global primary productivity. However, the relationship between SIF and photosynthesis in diurnal and seasonal cycles is still not fully understood, especially at large spatial scales, where direct measurements of photosynthesis are unfeasible. Motivated by up-scaling potential, this study examined the diurnal and seasonal relationship between SIF and photosynthetic parameters measured at the level of individual leaves. We monitored SIF in two plant species, avocado (Persea Americana) and orange jasmine (Murraya paniculatta), throughout 18 diurnal cycles during the Southern Hemisphere spring, summer and autumn, and compared them with simultaneous measurements of photosynthetic yields, and leaf and global irradiances. Results showed that at seasonal time scales SIF is principally correlated with changes in leaf irradiance, electron transport rates (ETR) and constitutive heat dissipation (YNO; p &lt; 0.001). Multiple regression models of correlations between photosynthetic parameters and SIF at diurnal time scales identified leaf irradiance as the principle predictor of SIF (p &lt; 0.001). Previous studies have identified correlations between photosynthetic yields, ETR and SIF at larger spatial scales, where heterogeneous canopy architecture and landscape spatial patterns influence the spectral and photosynthetic measurements. Although this study found a significant correlation between leaf-measured YNO and SIF, future dedicated up-scaling experiments are required to elucidate if these observations are also found at larger spatial scales.<\/jats:p>","DOI":"10.3390\/rs9060604","type":"journal-article","created":{"date-parts":[[2017,6,14]],"date-time":"2017-06-14T10:49:53Z","timestamp":1497437393000},"page":"604","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":21,"title":["Do Daily and Seasonal Trends in Leaf Solar Induced Fluorescence Reflect Changes in Photosynthesis, Growth or Light Exposure?"],"prefix":"10.3390","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9811-6228","authenticated-orcid":false,"given":"Rhys","family":"Wyber","sequence":"first","affiliation":[{"name":"Centre for Sustainable Ecosystem Solutions, School of Biological Sciences, University of Wollongong, Wollongong 2522, Australia"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1271-8103","authenticated-orcid":false,"given":"Zbyn\u011bk","family":"Malenovsk\u00fd","sequence":"additional","affiliation":[{"name":"Centre for Sustainable Ecosystem Solutions, School of Biological Sciences, University of Wollongong, Wollongong 2522, Australia"},{"name":"Department of Remote Sensing, Global Change Research Institute CAS, B\u011blidla 986\/4a, CZ-60300 Brno, Czech Republic"}]},{"given":"Michael","family":"Ashcroft","sequence":"additional","affiliation":[{"name":"Centre for Sustainable Ecosystem Solutions, School of Biological Sciences, University of Wollongong, Wollongong 2522, Australia"}]},{"given":"Barry","family":"Osmond","sequence":"additional","affiliation":[{"name":"Centre for Sustainable Ecosystem Solutions, School of Biological Sciences, University of Wollongong, Wollongong 2522, Australia"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7130-9617","authenticated-orcid":false,"given":"Sharon","family":"Robinson","sequence":"additional","affiliation":[{"name":"Centre for Sustainable Ecosystem Solutions, School of Biological Sciences, University of Wollongong, Wollongong 2522, Australia"}]}],"member":"1968","published-online":{"date-parts":[[2017,6,14]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Field, C.B., Barros, V.R., Dokken, D.J., Mach, K.J., Mastrandrea, M.D., Bilir, T.E., Chatterjee, M., Ebi, K.L., Estrada, Y.O., and Genova, R.C. (2014). Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part A: Global and Sectoral Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press.","DOI":"10.1017\/CBO9781107415379"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"968","DOI":"10.1071\/FP11164","article-title":"Non-invasive approaches for phenotyping of enhanced performance traits in bean","volume":"38","author":"Rascher","year":"2011","journal-title":"Funct. Plant Biol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"659","DOI":"10.1093\/jexbot\/51.345.659","article-title":"Chlorophyll fluorescence\u2014A practical guide","volume":"51","author":"Maxwell","year":"2000","journal-title":"J. Exp. Bot."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1071\/FP11255","article-title":"Canopy conundrums: Building on the Biosphere 2 experience to scale measurements of inner and outer canopy photoprotection from the leaf to the landscape","volume":"39","author":"Nichol","year":"2012","journal-title":"Funct. Plant Biol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1111\/j.1365-2486.2009.01908.x","article-title":"Remote sensing of sun-induced fluorescence to improve modeling of diurnal courses of gross primary production (GPP)","volume":"16","author":"Damm","year":"2010","journal-title":"Glob. Chang. Biol."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Rossini, M., Meroni, M., Celesti, M., Cogliati, S., Julitta, T., Panigada, C., Rascher, U., van der Tol, C., and Colombo, R. (2016). Analysis of Red and Far-Red Sun-Induced Chlorophyll Fluorescence and Their Ratio in Different Canopies Based on Observed and Modeled Data. Remote Sens., 8.","DOI":"10.3390\/rs8050412"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1093\/jxb\/erv456","article-title":"Plant chlorophyll fluorescence: Active and passive measurements at canopy and leaf scales with different nitrogen treatments","volume":"67","author":"Moran","year":"2016","journal-title":"J. Exp. Bot."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Pinto, F., Damm, A., Schickling, A., Panigada, C., Cogliati, S., M\u00fcller-Linow, M., Balvora, A., and 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.","DOI":"10.1111\/pce.12710"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"716","DOI":"10.1111\/gcb.13136","article-title":"Improving the monitoring of crop productivity using spaceborne solar-induced fluorescence","volume":"22","author":"Guan","year":"2016","journal-title":"Glob. Chang. Biol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"3727","DOI":"10.1111\/gcb.12664","article-title":"Estimation of vegetation photosynthetic capacity from space-based measurements of chlorophyll fluorescence for terrestrial biosphere models","volume":"20","author":"Zhang","year":"2014","journal-title":"Glob. Chang. Biol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1327","DOI":"10.1073\/pnas.1320008111","article-title":"Global and time-resolved monitoring of crop photosynthesis with chlorophyll fluorescence","volume":"111","author":"Guanter","year":"2014","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"637","DOI":"10.5194\/bg-8-637-2011","article-title":"First observations of global and seasonal terrestrial chlorophyll fluorescence from space","volume":"8","author":"Joiner","year":"2011","journal-title":"Biogeosciences"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"4065","DOI":"10.1093\/jxb\/eru191","article-title":"Linking chlorophyll a fluorescence to photosynthesis for remote sensing applications: Mechanisms and challenges","volume":"65","author":"Atherton","year":"2014","journal-title":"J. Exp. Bot."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1063\/PT.3.2924","article-title":"Photosynthetic fluorescence, from molecule to planet","volume":"68","author":"Berry","year":"2015","journal-title":"Phys. Today"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"492","DOI":"10.1007\/s004420050337","article-title":"The photochemical reflectance index: An optical indicator of photosynthetic radiation use efficiency across species, functional types, and nutrient levels","volume":"112","author":"Gamon","year":"1997","journal-title":"Oecologia"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1016\/S0034-4257(02)00010-X","article-title":"Relationships between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages","volume":"81","author":"Sims","year":"2002","journal-title":"Remote Sens. Environ."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1016\/j.rse.2016.05.015","article-title":"Consistency between sun-induced chlorophyll fluorescence and gross primary production of vegetation in North America","volume":"183","author":"Zhang","year":"2016","journal-title":"Remote Sens. Environ."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1007\/s11120-012-9747-4","article-title":"Relationships between the photochemical reflectance index (PRI) and chlorophyll fluorescence parameters and plant pigment indices at different leaf growth stages","volume":"113","author":"Munehiro","year":"2012","journal-title":"Photosynth. Res."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Schickling, A., Matveeva, M., Damm, A., Schween, J.H., Wahner, A., Graf, A., Crewell, S., and Rascher, U. (2016). Combining Sun-Induced Chlorophyll Fluorescence and Photochemical Reflectance Index Improves Diurnal Modeling of Gross Primary Productivity. Remote Sens., 8.","DOI":"10.3390\/rs8070574"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1023\/B:PRES.0000015391.99477.0d","article-title":"New fluorescence parameters for the determination of QA redox state and excitation energy fluxes","volume":"79","author":"Kramer","year":"2004","journal-title":"Photosynth. Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"3232","DOI":"10.3390\/rs70303232","article-title":"Early water stress detection using leaf-level measurements of chlorophyll fluorescence and temperature data","volume":"7","author":"Ni","year":"2015","journal-title":"Remote Sens."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Osmond, B., Chow, W.S., Wyber, R., Zavaleta, A., Keller, B., Pogson, B., and Robinson, A.S. (2017). Relative functional and optical absorption cross sections of PSII and other photosynthetic parameters monitored in situ, at a distance with a time resolution of a few seconds, using a prototype Light Induced Fluorescence Transient (LIFT) device. Funct. Plant Biol., in press.","DOI":"10.1071\/FP17024"},{"key":"ref_23","unstructured":"Kolber, Z. (2014). Light Induced Fluorescence Transient\u2013Fast Repetition Rate (LIFT-FRR) Fluorometer Operating Manual, Soliense Inc."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1002\/rob.21508","article-title":"HyperUAS\u2014Imaging spectroscopy from a multirotor unmanned aircraft system","volume":"31","author":"Lucieer","year":"2014","journal-title":"J. Field Robot."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1179","DOI":"10.1104\/pp.108.131417","article-title":"De Novo Synthesis and Degradation of Lx and V Cycle Pigments during Shade and Sun Acclimation in Avocado Leaves","volume":"149","author":"Osmond","year":"2009","journal-title":"Plant Physiol."},{"key":"ref_26","first-page":"1627","article-title":"Arabidopsis carotenoid mutants demonstrate that lutein is not essential for photosynthesis in higher plants","volume":"8","author":"Pogson","year":"1996","journal-title":"Plant Cell."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"526","DOI":"10.1007\/BF00203591","article-title":"Adenine nucleotides and the xanthophyll cycle in leaves","volume":"192","author":"Gilmore","year":"1994","journal-title":"Planta"},{"key":"ref_28","unstructured":"R Core Team (2013). R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/S0304-4165(89)80016-9","article-title":"The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence","volume":"990","author":"Genty","year":"1989","journal-title":"(BBA) Gen. Subj."},{"key":"ref_30","first-page":"27","article-title":"Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the Saturation Pulse method","volume":"1","author":"Klughammer","year":"2008","journal-title":"PAM Appl. Notes"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1007\/s11119-008-9074-0","article-title":"Spatio-temporal variations of photosynthesis: The potential of optical remote sensing to better understand and scale light use efficiency and stresses of plant ecosystems","volume":"9","author":"Rascher","year":"2008","journal-title":"Precis. Agric."},{"key":"ref_32","unstructured":"Rouse, J. (1974). Monitoring the Vernal Advancement and Retrogradation (Green Wave Effect) of Natural Vegetation, Texas A & M University, Remote Sensing Centre."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1111\/j.1365-3040.1990.tb01302.x","article-title":"Chlorophyll fluorescence measured using the Fraunhofer line-depth principle and relationship to photosynthetic rate in the field","volume":"13","author":"Carter","year":"1990","journal-title":"Plant Cell Environ."},{"key":"ref_34","unstructured":"McDonald, M., Schepers, J., Tartly, L., Toai, T.V., and Major, D. (2003). Sun-induced fluorescence: A new tool for precision farming. Digital Imaging and Spectral Techniques: Applications to Precision Agriculture and Crop Physiology, American Society of Agronomy Special Publication."},{"key":"ref_35","unstructured":"Oksanen, J., Blanchet, F., Kindt, R., Legendre, P., Minchin, P., O\u2019Hara, R., Simpson, G., Solymos, P., Stevens, M., and Wagner, H. (2016, July 03). Vegan: Community Ecology Package. R Package Vegan, Vers. 2.2-1; 2015. Available online: https:\/\/cran.r-project.org\/web\/packages\/vegan\/index.html."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Venables, W.N., and Ripley, B.D. (2002). Modern Applied Statistics with S, Springer. [4th ed.].","DOI":"10.1007\/978-0-387-21706-2"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/j.rse.2016.03.024","article-title":"Seasonal stability of chlorophyll fluorescence quantified from airborne hyperspectral imagery as an indicator of net photosynthesis in the context of precision agriculture","volume":"179","author":"Fereres","year":"2016","journal-title":"Remote Sens. Environ."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/j.rse.2005.01.013","article-title":"Remote sensing of sunlight-induced chlorophyll fluorescence and reflectance of Scots pine in the boreal forest during spring recovery","volume":"96","author":"Louis","year":"2005","journal-title":"Remote Sens. Environ."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"270","DOI":"10.1016\/j.rse.2015.03.027","article-title":"Continuous and long-term measurements of reflectance and sun-induced chlorophyll fluorescence by using novel automated field spectroscopy systems","volume":"164","author":"Cogliati","year":"2015","journal-title":"Remote Sens. Environ."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1093\/jxb\/eri012","article-title":"Slowly reversible de-epoxidation of lutein-epoxide in deep shade leaves of a tropical tree legume may \u2018lock-in\u2019 lutein-based photoprotection during acclimation to strong light","volume":"56","author":"Matsubara","year":"2005","journal-title":"J. Exp. Bot."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Wu, C., Liu, Z., and Xu, S. (2016). Remote sensing of crop light use efficiency using photochemical reflectance index. IEEE Trans. Geosci. Remote Sens., 1719\u20131722.","DOI":"10.1109\/IGARSS.2016.7729440"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1207","DOI":"10.1080\/01431160110106096","article-title":"The photochemical reflectance index as a measure of photosynthetic light use efficiency for plants with varying foliar nitrogen contents","volume":"23","author":"Trotter","year":"2002","journal-title":"Int. J. Remote Sens."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1740","DOI":"10.3390\/s8031740","article-title":"Assessing steady-state fluorescence and PRI from hyperspectral proximal sensing as early indicators of plant stress: The case of ozone exposure","volume":"8","author":"Meroni","year":"2008","journal-title":"Sensors"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1104\/pp.111.173369","article-title":"Lutein from deepoxidation of lutein epoxide replaces zeaxanthin to sustain an enhanced capacity for nonphotochemical chlorophyll fluorescence quenching in avocado shade leaves in the dark","volume":"156","author":"Pogson","year":"2011","journal-title":"Plant Physiol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"2037","DOI":"10.1016\/j.rse.2009.05.003","article-title":"Remote sensing of solar-induced chlorophyll fluorescence: Review of methods and applications","volume":"113","author":"Meroni","year":"2009","journal-title":"Remote Sens. Environ."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1517","DOI":"10.1098\/rstb.2000.0712","article-title":"Photorespiration: Metabolic pathways and their role in stress protection","volume":"355","author":"Wingler","year":"2000","journal-title":"Philos. Trans. R. Soc. Lond."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1016\/j.rse.2010.08.023","article-title":"The photochemical reflectance index (PRI) and the remote sensing of leaf, canopy and ecosystem radiation use efficiencies: A review and meta-analysis","volume":"115","author":"Garbulsky","year":"2011","journal-title":"Remote Sens. Environ."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"4443","DOI":"10.1080\/01431160802575661","article-title":"PRI assessment of long-term changes in carotenoids\/chlorophyll ratio and short-term changes in de-epoxidation state of the xanthophyll cycle","volume":"30","author":"Filella","year":"2009","journal-title":"Int. J. Remote Sens."},{"key":"ref_49","unstructured":"Kolber, Z. (2002, January 11\u201313). Laser Induced Fluorescence Transient (LIFT) Method for Measuring Photosynthetic Performance and Primary Productivity in Terrestrial Ecosystems. Proceedings of the Earth Science Technology Conference, Pasadena, CA, USA."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1093\/treephys\/tpu065","article-title":"Understanding something that is remotely sensible, scaling active chlorophyll fluorescence from leaves to canopies at ranges of ~50 metres","volume":"34","author":"Osmond","year":"2014","journal-title":"Tree Physiol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"3109","DOI":"10.5194\/bg-6-3109-2009","article-title":"An integrated model of soil-canopy spectral radiances, photosynthesis, fluorescence, temperature and energy balance","volume":"6","author":"Verhoef","year":"2009","journal-title":"Biogeosciences"},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Gastellu-Etchegorry, J.P., Lauret, N., Yin, T., Landier, L., Kallel, A., Malenovsk\u00fd, Z., Al Bitar, A., Aval, J., Benhmida, S., and Qi, J. (2017). Recent advances in remote sensing data modeling with atmosphere, polarization, and chlorophyll fluorescence. IEEE J. Sel. Top. Appl. Earth Obs. Remote Sens., in press.","DOI":"10.1109\/JSTARS.2017.2685528"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1016\/j.isprsjprs.2012.01.003","article-title":"Effect of canopy structure on sun-induced chlorophyll fluorescence","volume":"68","author":"Fournier","year":"2012","journal-title":"ISPRS J. Photogramm. Remote Sens."},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Pinto, F., M\u00fcller-Linow, M., Schickling, A., Cendrero-Mateo, M., Ballvora, A., and Rascher, U. (2017). Multiangular Observation of Canopy Sun-Induced Chlorophyll Fluorescence by Combining Imaging Spectroscopy and Stereoscopy. Remote Sens., 9.","DOI":"10.3390\/rs9050415"}],"container-title":["Remote Sensing"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-4292\/9\/6\/604\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T18:39:03Z","timestamp":1760207943000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-4292\/9\/6\/604"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,6,14]]},"references-count":54,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2017,6]]}},"alternative-id":["rs9060604"],"URL":"https:\/\/doi.org\/10.3390\/rs9060604","relation":{},"ISSN":["2072-4292"],"issn-type":[{"type":"electronic","value":"2072-4292"}],"subject":[],"published":{"date-parts":[[2017,6,14]]}}}