Remote sensing of solar-induced chlorophyll fluorescence (SIF) is a rapidly advancing front in terrestrial vegetation science, with emerging capability in space-based methodologies and diverse application prospects. Although remote sensing of SIF – especially from space – is seen as a contemporary new specialty for terrestrial plants, it is founded upon a multi-decadal history of research, applications, and sensor developments in active and passive sensing of chlorophyll fluorescence. Current technical capabilities allow SIF to be measured across a range of biological, spatial, and temporal scales. As an optical signal, SIF may be assessed remotely using high-resolution spectral sensors in tandem with state-of-the-art algorithms to distinguish the emission from reflected and/or scattered ambient light. Because the red to far-red SIF emission is detectable non-invasively, it may be sampled repeatedly to acquire spatio-temporally explicit information about photosynthetic light responses and steady-state behaviour in vegetation. Progress in this field is accelerating with innovative sensor developments, retrieval methods, and modelling advances. This review distills the historical and current developments spanning the last several decades. It highlights SIF heritage and complementarity within the broader field of fluorescence science, the maturation of physiological and radiative transfer modelling, SIF signal retrieval strategies, techniques for field and airborne sensing, advances in satellite-based systems, and applications of these capabilities in evaluation of photosynthesis and stress effects. Progress, challenges, and future directions are considered for this unique avenue of remote sensing.

Although traditional remote sensing systems based on spectral reflectance can already provide estimates of the "potential" photosynthetic activity of terrestrial vegetation through the quantification of total canopy chlorophyll content or absorbed photosynthetic radiation, the determination of the "actual" photosynthetic activity of terrestrial vegetation requires information about how the absorbed light is used by plants, such as vegetation fluorescence, using very high spectral resolution spectroscopy in the range 650-800 nm. The Fluorescence Explorer (FLEX) mission, selected in November 2015 as the 8th Earth Explorer by the European Space Agency (ESA), carries the FLORIS spectrometer, with a spectral resolution of 0.3 nm and a spatial resolution of 300 m, with a swath of 150 km. The FLEX mission is designed to fly in tandem with the Copernicus Sentinel-3 satellite, in order to provide all the necessary information to disentangle emitted fluorescence from the background reflected radiance, and to allow proper interpretation of the fluorescence spatial and temporal changes in relation to photosynthesis dynamics, accounting for non-photochemical energy dissipation and canopy temperature effects.

In November 2015, the FLuorescence EXplorer (FLEX) was selected as the eighth Earth Explorer mission of the European Space Agency. The tandem mission concept will provide measurements at a spectral and spatial resolution enabling the retrieval and interpretation of the full chlorophyll fluorescence spectrum emitted by the terrestrial vegetation. This paper provides a mission concept overview of the scientific goals, the key objectives related to fluorescence, and the requirements guaranteeing the fitness for purpose of the resulting scientific data set. We present the mission design at the time of selection, i.e., at the end of project phase Phase A/B1, as developed by two independent industrial consortia. The mission concepts both rely on a single payload Fluorescence Imaging Spectrometer, covering the spectral range from 500 to 780 nm. In the oxygen absorption bands, its spectral resolution will be 0.3 nm with a spectral sampling interval of 0.1 nm. The swath width of the spectrometer is 150 km and the spatial resolution will be 300 x 300 m(2). The satellite will fly in tandem with Sentinel-3 providing different and complementary measurements with a temporal collocation of 6 to 15 s. The FLEX launch is scheduled for 2022.

Progress in imaging spectroscopy technology and data processing can enable derivation of the complete sun-induced chlorophyll fluorescence (SIF) emission spectrum. This opens up opportunities to fully exploit the use of the SIF spectrum as an indicator of photosynthetic activity. Simulations performed with the coupled fluorescence–photosynthesis model SCOPE were used to determine how strongly canopy-leaving SIF can be related to net photosynthesis of the canopy (NPC) for various canopy configurations. Regression analysis between SIF retrievals and NPC values produced the following general findings: (1) individual SIF bands that were most sensitive to NPC were located around the first emission peak (SIFred) for heterogeneous canopy configurations (i.e., varying biochemistry, leaf, canopy variables); (2) using two SIF retrieval bands, e.g. O2-B at 687nm and O2-A at 760nm, or the red and NIR emission peaks at 685nm and 740nm, led to stronger correlations than using only one band; (3) using the O2-B and the O2-A SIF retrieval bands was at least as effective as using the two emission peaks; (4) superior correlations were achieved by using the four main SIF retrieval bands (Hα, O2-B, water vapor, O2-A); and (5) further improvements may be obtained by exploiting the full SIF profile and by using an adaptive, nonlinear regression algorithm such as Gaussian processes regression (GPR). Relationships can be due to variation in photosynthetic capacity (Vcmo), but also from variation in leaf optical and canopy structural variables such as chlorophyll content and leaf area index. Overall, modeling results suggest that sampling the SIF profile in at least both O2-B and O2-A bands enables quantification photosynthetic activity of vegetation with high accuracy.

In this study, measurements of solar induced chlorophyll fluorescence (SIF) at 760nm (F760) are combined with hyperspectral reflectance (R) measurements collected in the field over agricultural crops in order to better understand the fluorescence (ChlF) signal of the vegetation. The ‘Soil-Canopy Observation Photosynthesis and Energy fluxes' (SCOPE) model, which combines radiative transfer and enzyme kinetics of photosynthesis with turbulent heat exchange in vegetation canopies, was partly inverted to obtain model parameters from R taken over healthy (unstressed) crops during the growing season. Reflectance spectra between 400 and 900nm obtained at midday on different days in the growing season were used to obtain pigment concentrations, leaf area index and leaf inclination. These parameters were then used to simulate diurnal cycles of half-hourly ChlF spectra, using measured weather variables as input. Three scenarios were simulated: (i) a constant emission efficiency of ChlF (at the photosystem level), (ii) a variable emission efficiency calculated per half hour with an electron transport, photosynthesis and ChlF model for the photosystem, and (iii) a constant emission efficiency that was set to a theoretical maximum value for fully blocked photochemical electron transport of photosystem II and minimal non-photochemical quenching. The simulations of the first two scenarios were compared to ChlF retrieved from field measurements in the O2-A band with the spectral fitting method in unstressed rice and alfalfa. This comparison and a sensitivity analysis showed that SCOPE reproduces most of the seasonal variability of SIF after tuning to R even if the ChlF emission efficiency is kept constant, and F760 values are mostly determined by chlorophyll content, dry matter, senescent material and leaf area and leaf inclination, whereas leaf water and carotenoid content had small effects. Diurnal variations in the ChlF emission efficiency at photosystem level were small in these crops. The simulations of the third scenario were compared to measurements of grass that was treated chemically to block electron transport and to provoke maximum ChlF. This comparison showed that the observed increase in F760 can indeed be explained by a change in the ChlF emission efficiency at the photosystem level. It is concluded that hyperspectral reflectance and the ChlF signal together can reveal both the dynamics of vegetation structure and functioning.

The Fluorescence Explorer (FLEX) mission has been recently selected as the 8th Earth Explorer by the European Space Agency (ESA). It will be the first mission specifically designed to measure from space vegetation fluorescence emission, by making use of very high spectral resolution imaging spectroscopy techniques. Vegetation fluorescence is the best proxy to actual vegetation photosynthesis which can be measurable from space, allowing an improved quantification of vegetation carbon assimilation and vegetation stress conditions, thus having key relevance for global mapping of ecosystems dynamics and aspects related with agricultural production and food security. The FLEX mission carries the FLORIS spectrometer, with a spectral resolution in the range of 0.3 nm, and is designed to fly in tandem with Copernicus Sentinel-3, in order to provide all the necessary spectral / angular information to disentangle emitted fluorescence from reflected radiance, and to allow proper interpretation of the observed fluorescence spatial and temporal dynamics.

Progress in imaging spectroscopy technology and data processing can enable derivation of the complete solarinduced chlorophyll fluorescence (SIF) emission spectrum from 640-800 nm. This opens up opportunities to fully utilize the SIF signal as an indicator of photosynthetic activity. A SCOPE modelling exercise was conducted to determine how strongly canopy-leaving SIF can be related to net photosynthesis of the canopy (NPC) for various simulated canopy configurations. This was done in two ways. First, a variance-based global sensitivity analysis (GSA) for both SIF and NPC was conducted; second, a regression analysis between SIF and NPC was performed. The GSA identified the SCOPE input variables that drive SIF and NPC. Largely the same key variables were identified, which explains why SIF can be related to NPC. Subsequent regression analysis between SIF retrievals and NPC values indicated that for heterogeneous canopy configurations (i.e. varying biochemistry, leaf, canopy variables) individual SIF bands most sensitive to NPC were located around the first emission peak (SIFred).

This study provides insight into the key variables that drive sun-induced chlorophyll fluorescence (SIF) emanating from vegetation canopies, based on a global sensitivity analysis (GSA) of the Soil-Canopy Observation of Photosynthesis and Energy (SCOPE) balance model. An updated version of the SCOPE model was used here (v1.53) which contains novel leaf physiological modules for determination of the steady state fluorescence yield: a photosynthesis model coupled with (a) submodels having empirically derived relationships, identified as TB12 for unstressed and TB12-D for drought conditions and (b) a mechanistic (MD12) submodel based on theoretical relationships. By inspecting Sobol's total order (main effect and all the interactions) sensitivity index (STi) rankings, the influential and non-influential variables were determined. Two experiments were conducted for the different leaf physiology modules in SCOPE considering (1) only vegetation variables, and (2) all SCOPE variables, i.e., including micrometeorological, aerodynamic and geometry variables.Considering TB12-D STi results using only vegetation input variables, the canopy-leaving broadband (641–800nm) SIF variability was determined mainly by leaf optical properties and canopy structural variables. The most important variables were (with decreasing importance) leaf chlorophyll content (Cab), leaf inclination (LIDFa) and leaf area index (LAI). These three variables alone determined 77.9% of the SIF variability. Vcmo, the variable related to photosynthetic capacity, determined 11.4% of overall SIF variability, and its importance declined considerably when moving from the first emission peak (SIFred; with maximal relevance of 17.9% at 676nm) to the second emission peak (SIFNIR; e.g., 9.6% at 740nm). Stronger relationships with Vcmo were obtained when retrieving the full broadband SIF flux and calculating total fluorescence yield (Fyield, determined as the integral of the hemispherical broadband SIF flux divided by the total absorbed PAR), of which 35% of the variability was influenced by Vcmo. Using the TB12 submodel, the major drivers of SIF flux were similar to TB12-D except that Vcmo accounted for very little (<2%) variability. The MD12 submodel identified the components of long-term PSII photoprotection and photodamage as the dominant factors for SIF variability: these two variables alone accounted for 51.4% of the variability of SIF flux and 61% of Fyield, whereas Vcmo explained only 9.7% and 10.9% of variability in SIF flux and Fyield, respectively.Analysis of the relative importance of all SCOPE variables revealed that in addition to the key vegetation variables, micrometeorological variables were important in driving SIF variability, especially incoming shortwave radiation (Rin) and to a lesser extent air temperature (Ta), atmospheric vapor pressure (ea) and atmospheric CO2 concentration (Ca). Their impact further reduced the relative importance of Vcmo.The GSA experiments led to the following conclusions: (1) explicit knowledge of key variables driving the SIF flux is essential in order to achieve unbiased SIF interpretation related to photosynthetic activity at local and global scales; (2) information related to photosynthetic activity is found more in the first emission peak (SIFred) than in the second peak (SIFNIR), and more in the full broadband SIF emission, which allows calculation of Fyield, than in individual wavebands.

Many laboratory studies investigating chlorophyll fluorescence (F) of plants have provided sufficient evidence of the functional link between dynamic changes in photosynthetic activity and F emissions. Far fewer studies, however, have been devoted to detailed analysis of F emission under steady-state conditions, which may be amenable to measurement by passive spectroradiometers onboard airborne or satellite missions. Here, we provide a random-effects meta-analysis of studies using both passively (sun-induced) and actively (e.g. laser-induced) measured steady-state F for detecting stress reactions in terrestrial vegetation. Specifically, we review behaviour of F in red and far-red wavelengths, and also the red to far-red F ratio, for plants physiologically stressed by water deficit, temperature extremes, and nitrogen insufficiency. Results suggest that water stress is, in general, associated with a decline in red and far-red F signal intensity measured at both leaf and canopy levels, whereas the red to far-red F ratio displays an inconsistent behaviour. Chilling, for which only studies with active measurements at the leaf level are available, significantly increased red and far-red F, whereas heat stress produced a less convincing decrease in both F emissions, notably in canopies measured passively. The clearest indicator of temperature stress was the F ratio, which declined significantly and consistently. The F ratio was also the strongest indicator of nitrogen deficiency, revealing a nearly uniformly increasing pattern driven by predominantly declining far-red F. Although significant knowledge gaps were encountered for certain scales and F measurement techniques, the analyses indicate that future airborne or space-borne acquisitions of both red and far-red F signals would be beneficial for timely detection of plant stress events.

This study addresses the question which factors are responsible for reported positive correlations between solar induced fluorescence (SIF) and gross primary production (GPP). A sensitivity analysis of the model SCOPE, which simulates photosynthesis, fluorescence emission and radiative transfer in canopies, has been carried out for four different plant functional types (PFT): tropical rainforest, C4 crops, C3 crops, and tundra, located in distinct climate zones: tropical everwet (Af), tropical with seasonal drought (savannah, Aw), temperate (Cf), and continental tundra (Dfd). Literature values for structural and physiological parameters and climate reanalysis data were used as input. The effect of main driving variables points towards a positive relation between GPP and SIF. For all four climates, the partial derivative of SIF to GPP is higher when irradiance varies than when any other parameter varies. Climate and PFT specific differences occurred, including a hot-spot effect on SIF in the tropics, relatively strong sensitivity of SIF and GPP to carboxylation capacity in the tropics, and a temperature and humidity effect in the tropical seasonal climate.

The potential to measure vegetation fluorescence from space (1) and to derive from it direct information on the gross primary productivity (GPP) of terrestrial ecosystems is probably the most thrilling development in remote sensing and global ecology of recent years, as it moves Earth observation techniques from the detection of canopy biophysics (e.g., fraction of absorbed radiation) and biochemistry (chlorophyll and nitrogen content) to the realm of ecosystem function. The existence of a functional relationship between fluorescence and photosynthesis has been elucidated over the last decade by several laboratories, notably as part of the preliminary studies of the European Space Agency Fluorescence Explorer (FLEX) Earth Explorer Mission. The …

In support of ESA's Earth Explorer 8 candidate mission FLEX (FLuorescence EXplorer), a Photosynthesis Study has been initiated to quantitatively link fluorescence to photosynthesis. This led to the development of A-SCOPE, a graphical user interface software package that integrates multiple biochemical models into the soil-vegetation atmosphere-transfer model SCOPE. Its latest version (v1.53) has been successfully verified and was subsequently evaluated through a global sensitivity analysis. By using the method of Saltelli [4], the relative importance of each input variable to model outputs was quantified through first order and total effect sensitivity indices. Variations in leaf area index (LAI) and chlorophyll content are mostly impacting the reflectance and fluorescence signal. Non-driving variables that can be safely set to default values have been identified and will facilitate consolidating SCOPE into an operational and invertible model.

In this study we performed a random-effects comprehensive meta-analysis of data published by various studies that investigated passively (solar) and actively (artificial light) induced chlorophyll fluorescence (F) in a steady state as an indicator of various stress events. Specifically, we reviewed and analysed behaviour of the steady-state fluorescence in red (684-695 nm, FR) and far-red wavelengths (730-740 nm, FFR), and also their ratio (FR/FFR), for plants physiologically stressed by water deficiency, temperature extremes (chilling and heat) and nitrogen insufficiency. The meta-analysis was followed by systematic investigation of knowledge gaps between actual scientific understanding and potential application of remotely sensed steady-state F as an early indicator of plant stress. The knowledge gap analysis pointed out that the lack of dedicated studies assessing measurement errors caused by the factors interfering with F measurements is currently the weakest point of the chlorophyll fluorescence stress detection discussion. The largest identified gap, common to all three investigated stressors, is potential use of the steady-state F signal acquired at the level of whole ecosystems with complex heterogeneous canopies that are naturally established as mixture of various plant functional types (e.g., grassland with shrubs and trees). The most challenging unknown is behaviour of F under the influence of combined multiple stress impacts and the related temporal aspects. The least is known about the potential use of F emissions as indicators of plant nitrogen insufficiency, due to the multiple roles of nitrogen in plant physiological processes. Systematically coordinated experiments of active F measurements physiologically linked to passively observed F are suggested to bridge the identified gaps. Regular measurements at permanent research sites forming a global network may help us to establish an envelope of plant environmental limits, for which F values are stress indicative. Finally, measurement of both FR and FFR signals can be strongly recommended, as these measurements seem to be complementary rather than redundant and their ratio demonstrated a consistent stress indicating character.

The practical utility of chlorophyll fluorescence to forestry applications is reviewed. Major subjects include a review of past applications, sampling protocols, important fluorescence features, and instrumentation. Applications including the study of various stress effects, seasonal effects, and comparative sun/shade leaf physiology are provided. Chlorophyll fluorescence has been used mainly in applied research, rather than directly in operational forestry, but work has begun in this area. Sampling protocols include the selection and treatment of samples before assessment, and control of environmental conditions during assessment. Instrumentation is evaluated based on accuracy, versatility, ease of operation, and cost. Chlorophyll fluorescence ranks high among stress detection tests in forestry applications, because it is rapid, reliable, non-destructive, quantitative, diagnostic, and the physiological basis of the assessment is understood.

The FLuorescence EXplorer (FLEX) mission proposes to launch a satellite for the global monitoring of steady-state chlorophyll fluorescence in terrestrial vegetation. Fluorescence is a sensitive probe of photosynthetic function in both healthy and physiologically perturbed vegetation, and a powerful non-invasive tool to track the status, resilience, and recovery of photochemical processes and moreover provides important information on overall photosynthetic performance with implications for related carbon sequestration. The early responsiveness of fluorescence to atmospheric, soil and plant water balance, as well as to atmospheric chemistry and human intervention in land usage makes it an obvious biological indicator in improving our understanding of Earth system dynamics. The amenability of fluorescence to remote, even space-basedobservation qualifies it to join the emerging suite of space-based technologies for Earth observation. FLEX would encompass a three-instrument array for measurement of the interrelated features of fluorescence, hyperspectral reflectance, and canopy temperature. FLEX would involve a space and ground-truthing program of 3-years duration and would provide data formats for research and applied science.

The FLuorescence EXplorer (FLEX) mission proposes to launch a satellite for the global monitoring of steady-state chlorophyll fluorescence in terrestrial vegetation. Fluorescence is a sensitive probe of photosynthetic function in both healthy and physiologically perturbed vegetation, and a powerful non-invasive tool to track the status, resilience, and recovery of photochemical processes and moreover provides important information on overall photosynthetic performance with implications for related carbon sequestration. The early responsiveness of fluorescence to atmospheric, soil and plant water balance, as well as to atmospheric chemistry and human intervention in land usage makes it an obvious biological indicator in improving our understanding of Earth system dynamics. The amenability of fluorescence to remote, even space-basedobservation qualifies it to join the emerging suite of space-based technologies for Earth observation. FLEX would encompass a three-instrument array for measurement of the interrelated features of fluorescence, hyperspectral reflectance, and canopy temperature. FLEX would involve a space and ground-truthing program of 3-years duration and would provide data formats for research and applied science.