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  • Porcar-Castell, Albert; Malenovsky, Zbynek; Magney, Troy; Van Wittenberghe, Shari; Fernandez-Marin, Beatriz; Maignan, Fabienne; Zhang, Yongguang; Maseyk, Kadmiel; Atherton, Jon; Albert, Loren P.; Robson, Thomas Matthew; Zhao, Feng; Garcia-Plazaola, Jose-Ignacio; Ensminger, Ingo; Rajewicz, Paulina A.; Grebe, Steffen; Tikkanen, Mikko; Kellner, James R.; Ihalainen, Janne A.; Rascher, Uwe; Logan, Barry (2021)
    Remote sensing methods enable detection of solar-induced chlorophyll a fluorescence. However, to unleash the full potential of this signal, intensive cross-disciplinary work is required to harmonize biophysical and ecophysiological studies. For decades, the dynamic nature of chlorophyll a fluorescence (ChlaF) has provided insight into the biophysics and ecophysiology of the light reactions of photosynthesis from the subcellular to leaf scales. Recent advances in remote sensing methods enable detection of ChlaF induced by sunlight across a range of larger scales, from using instruments mounted on towers above plant canopies to Earth-orbiting satellites. This signal is referred to as solar-induced fluorescence (SIF) and its application promises to overcome spatial constraints on studies of photosynthesis, opening new research directions and opportunities in ecology, ecophysiology, biogeochemistry, agriculture and forestry. However, to unleash the full potential of SIF, intensive cross-disciplinary work is required to harmonize these new advances with the rich history of biophysical and ecophysiological studies of ChlaF, fostering the development of next-generation plant physiological and Earth-system models. Here, we introduce the scale-dependent link between SIF and photosynthesis, with an emphasis on seven remaining scientific challenges, and present a roadmap to facilitate future collaborative research towards new applications of SIF.
  • Magney, Troy S.; Frankenberg, Christian; Kohler, Philipp; North, Gretchen; Davis, Thomas S.; Dold, Christian; Dutta, Debsunder; Fisher, Joshua B.; Grossmann, Katja; Harrington, Alexis; Hatfield, Jerry; Stutz, Jochen; Sun, Ying; Porcar-Castell, Albert (2019)
    Novel satellite measurements of solar-induced chlorophyll fluorescence (SIF) can improve our understanding of global photosynthesis; however, little is known about how to interpret the controls on its spectral variability. To address this, we disentangle simultaneous drivers of fluorescence spectra by coupling active and passive fluorescence measurements with photosynthesis. We show empirical and mechanistic evidence for where, why, and to what extent leaf fluorescence spectra change. Three distinct components explain more than 95% of the variance in leaf fluorescence spectra under both steady-state and changing illumination conditions. A single spectral shape of fluorescence explains 84% of the variance across a wide range of species. The magnitude of this shape responds to absorbed light and photosynthetic up/down regulation; meanwhile, chlorophyll concentration and nonphotochemical quenching control 9% and 3% of the remaining spectral variance, respectively. The spectral shape of fluorescence is remarkably stable where most current satellite retrievals occur (far-red, >740nm), and dynamic downregulation of photosynthesis reduces fluorescence magnitude similarly across the 670- to 850-nm range. We conduct an exploratory analysis of hourly red and far-red canopy SIF in soybean, which shows a subtle change in red:far-red fluorescence coincident with photosynthetic downregulation but is overshadowed by longer-term changes in canopy chlorophyll and structure. Based on our leaf and canopy analysis, caution should be taken when attributing large changes in the spectral shape of remotely sensed SIF to plant stress, particularly if data acquisition is temporally sparse. Ultimately, changes in SIF magnitude at wavelengths greater than 740 nm alone may prove sufficient for tracking photosynthetic dynamics. Plain Language Summary Satellite remote sensing provides a global picture of photosynthetic activity-allowing us to see when, where, and how much CO2 plants are assimilating. To do this, satellites measure a small emission of energy from the plants called chlorophyll fluorescence. However, this measurement is typically made across a narrow wavelength range, while the emission spectrum (650-850 nm) is quite dynamic. We show where, why, and to what extent leaf fluorescence spectra change across a diverse range of species and conditions, ultimately informing canopy remote sensing measurements. Results suggest that wavelengths currently used by satellites are stable enough to track the downregulation of photosynthesis resulting from stress, while spectral shape changes respond more strongly to dynamics in canopy structure and chlorophyll concentration.
  • Nichol, Caroline J.; Drolet, Guillaume; Porcar-Castell, Albert; Wade, Tom; Sabater, Neus; Middleton, Elizabeth M.; MacLellan, Chris; Levula, Janne; Mammarella, Ivan; Vesala, Timo; Atherton, Jon (2019)
    Solar induced chlorophyll fluorescence has been shown to be increasingly an useful proxy for the estimation of gross primary productivity (GPP), at a range of spatial scales. Here, we explore the seasonality in a continuous time series of canopy solar induced fluorescence (hereafter SiF) and its relation to canopy gross primary production (GPP), canopy light use efficiency (LUE), and direct estimates of leaf level photochemical efficiency in an evergreen canopy. SiF was calculated using infilling in two bands from the incoming and reflected radiance using a pair of Ocean Optics USB2000+ spectrometers operated in a dual field of view mode, sampling at a 30 min time step using custom written automated software, from early spring through until autumn in 2011. The optical system was mounted on a tower of 18 m height adjacent to an eddy covariance system, to observe a boreal forest ecosystem dominated by Scots pine. (Pinus sylvestris) A Walz MONITORING-PAM, multi fluorimeter system, was simultaneously mounted within the canopy adjacent to the footprint sampled by the optical system. Following correction of the SiF data for O-2 and structural effects, SiF, SiF yield, LUE, the photochemicsl reflectance index (PRI), and the normalized difference vegetation index (NDVI) exhibited a seasonal pattern that followed GPP sampled by the eddy covariance system. Due to the complexities of solar azimuth and zenith angle (SZA) over the season on the SiF signal, correlations between SiF, SiF yield, GPP, and LUE were assessed on SZA <50 degrees and under strictly clear sky conditions. Correlations found, even under these screened scenarios, resulted around similar to r(2) = 0.3. The diurnal responses of SiF, SiF yield, PAM estimates of effective quantum yield (Delta F/Delta F-m(')), and meteorological parameters demonstrated some agreement over the diurnal cycle. The challenges inherent in SiF retrievals in boreal evergreen ecosystems are discussed.
  • Zhang, Chao; Atherton, Jon; Penuelas, Josep; Filella, Iolanda; Kolari, Pasi; Aalto, Juho; Ruhanen, Hanna; Back, Jaana; Porcar-Castell, Albert (2019)
    Chlorophyll a fluorescence (ChlF) is closely related to photosynthesis and can be measured remotely using multiple spectral features as solar-induced fluorescence (SIF). In boreal regions, SIF shows particular promise as an indicator of photosynthesis, in part because of the limited variation of seasonal light absorption in these ecosystems. Seasonal spectral changes in ChlF could yield new information on processes such as sustained nonphotochemical quenching (NPQ(S)) but also disrupt the relationship between SIF and photosynthesis. We followed ChlF and functional and biochemical properties of Pinus sylvestris needles during the photosynthetic spring recovery period to answer the following: (a) How ChlF spectra change over seasonal timescales? (b) How pigments, NPQ(S), and total photosynthetically active radiation (PAR) absorption drive changes of ChlF spectra? (c) Do all ChlF wavelengths track photosynthetic seasonality? We found seasonal ChlF variation in the red and far-red wavelengths, which was strongly correlated with NPQ(S), carotenoid content, and photosynthesis (enhanced in the red), but not with PAR absorption. Furthermore, a rapid decrease in red/far-red ChlF ratio occurred in response to a cold spell, potentially relating to the structural reorganization of the photosystems. We conclude that all current SIF retrieval features can track seasonal photosynthetic dynamics in boreal evergreens, but the full SIF spectra provides additional insight.
  • Bacour, C.; Maignan, F.; MacBean, N.; Porcar-Castell, A.; Flexas, J.; Frankenberg, C.; Peylin, P.; Chevallier, F.; Vuichard, N.; Bastrikov, V. (2019)
    Abstract Over the last few years, solar-induced chlorophyll fluorescence (SIF) observations from space have emerged as a promising resource for evaluating the spatio-temporal distribution of gross primary productivity (GPP) simulated by global terrestrial biosphere models. SIF can be used to improve GPP simulations by optimizing critical model parameters through statistical Bayesian data assimilation techniques. A prerequisite is the availability of a functional link between GPP and SIF in terrestrial biosphere models. Here we present the development of a mechanistic SIF observation operator in the ORCHIDEE (Organizing Carbon and Hydrology In Dynamic Ecosystems) terrestrial biosphere model. It simulates the regulation of photosystem II fluorescence quantum yield at the leaf level thanks to a novel parameterization of non-photochemical quenching as a function of temperature, photosynthetically active radiation, and normalized quantum yield of photochemistry. It emulates the radiative transfer of chlorophyll fluorescence to the top of the canopy using a parametric simplification of the SCOPE (Soil Canopy Observation Photosynthesis Energy) model. We assimilate two years of monthly OCO-2 (Orbiting Carbon Observatory-2) SIF product at 0.5° (2015?2016) to optimize ORCHIDEE photosynthesis and phenological parameters over an ensemble of grid points for all plant functional types. The impact on the simulated GPP is considerable with a large decrease of the global scale budget by 28 GtC/year over the period 1990?2009. The optimized GPP budget (134/136 GtC/year over 1990?2009/2001?2009) remarkably agrees with independent GPP estimates, FLUXSAT (137 GtC/year over 2001?2009) in particular and FLUXCOM (121 GtC/year over 1990?2009). Our results also suggest a biome dependency of the SIF-GPP relationship that needs to be improved for some plant functional types.
  • Wang, Siyu; Lu, Xinchen; Cheng, Xiao; Li, Xianglan; Peichl, Matthias; Mammarella, Ivan (2018)
    Recent efforts have been made to monitor the seasonal metrics of plant canopy variations globally from space, using optical remote sensing. However, phenological estimations based on vegetation indices (VIs) in high-latitude regions such as the pan-Arctic remain challenging and are rarely validated. Nevertheless, pan-Arctic ecosystems are vulnerable and also crucial in the context of climate change. We reported the limitations and challenges of using MODerate-resolution Imaging Spectroradiometer (MODIS) measurements, a widely exploited set of satellite measurements, to estimate phenological transition dates in pan-Arctic regions. Four indices including normalized vegetation difference index (NDVI), enhanced vegetation index (EVI), phenology index (PI), plant phenological index (PPI) and a MODIS Land Cover Dynamics Product MCD12Q2, were evaluated and compared against eddy covariance (EC) estimates at 11 flux sites of 102 site-years during the period from 2000 to 2014. All the indices were influenced by snow cover and soil moisture during the transition dates. While relationships existed between VI-based and EC-estimated phenological transition dates, the R-2 values were generally low (0.01-0.68). Among the VIs, PPI-estimated metrics showed an inter-annual pattern that was mostly closely related to the EC-based estimations. Thus, further studies are needed to develop region-specific indices to provide more reliable estimates of phenological transition dates.
  • Atherton, Jon; Liu, Weiwei; Porcar-Castell, Albert (2019)
    Solar-induced chlorophyll a Fluorescence (SIF), which is distributed over a relatively broad (similar to 200 nm) spectral range, is a signal intricately connected to the efficiency of photosynthesis and is now observable from space. Variants of the Fraunhofer Line Depth/Discriminator (FLD) method are used as the basis of retrieval algorithms for estimating SIF from space. Although typically unobserved directly, recent advances in FLD-based algorithms now facilitate the prediction (by model inversion) of the canopy emitted fluorescence spectrum from the discrete-feature FLD retrievals. Here we present first canopy scale measurements of chlorophyll a fluorescence spectra emitted from Scots pine at two times of year, and also from a lingonberry dominated understory. We used a high power mul-tispectral Light Emitting Diode (LED) array to illuminate the respective canopies at night and measured under standardised conditions using a field spectrometer mounted in the nadir position above the canopy. We refer to the technique, which facilitates the in situ upscaling of a commonly measured leaf scale quantity to the canopy, as nocturnal LED-Induced chlorophyll a Fluorescence (LEDIF). The shape of the LEDIF spectra was dependant on the colour of the excitation light and also on the dominant species. Because we measured pine at two different times of year we were also able to show an increase in the canopy scale apparent quantum yield of fluorescence which was consistent with leaf-level increase in fluorescence yield recorded with a monitoring PAM fluorometer. The automation of the LEDIF technique could be used to estimate seasonal changes in canopy fluorescence spectra and yield from fixed or mobile platforms and provide a window into functional traits across species and architectures. LEDIF could also be used to evaluate FLD and inversion-based retrievals of canopy spectra, as well as different irradiance normalisation schemes typically applied to SIF data to account for the dependence of SIF on ambient light conditions.
  • Zhang, Zhaoying; Zhang, Yongguang; Porcar-Castell, Albert; Joiner, Joanna; Guanter, Luis; Yang, Xi; Migliavacca, Mirco; Ju, Weimin; Sun, Zhigang; Chen, Shiping; Martini, David; Zhang, Qian; Li, Zhaohui; Cleverly, James; Wang, Hezhou; Goulas, Yves (2020)
    Quantifying global photosynthesis remains a challenge due to a lack of accurate remote sensing proxies. Solar-induced chlorophyll fluorescence (SIF) has been shown to be a good indicator of photosynthetic activity across various spatial scales. However, a global and spatially challenging estimate of terrestrial gross primary production (GPP) based on satellite SIF remains unresolved due to the confounding effects of species-specific physical and physiological traits and external factors, such as canopy structure or photosynthetic pathway (C-3 or C-4). Here we analyze an ensemble of far-red SIF data from OCO-2 satellite and ground observations at multiple sites, using the spectral invariant theory to reduce the effects of canopy structure and to retrieve a structure-corrected total canopy SIF emission (SIFtotal). We find that the relationships between observed canopy-leaving SIF and ecosystem GPP vary significantly among biomes. In contrast, the relationships between SIFtotal and GPP converge around two unique models, one for C-3 and one for C-4 plants. We show that the two single empirical models can be used to globally scale satellite SIF observations to terrestrial GPP. We obtain an independent estimate of global terrestrial GPP of 129.56 +/- 6.54 PgC/year for the 2015-2017 period, which is consistent with the state-of-the-art data- and process-oriented models. The new GPP product shows improved sensitivity to previously undetected 'hotspots' of productivity, being able to resolve the double-peak in GPP due to rotational cropping systems. We suggest that the direct scheme to estimate GPP presented here, which is based on satellite SIF, may open up new possibilities to resolve the dynamics of global terrestrial GPP across space and time.