Correction of PRI for carotenoid pigment pools improves photosynthesis estimation across different irradiance and temperature conditions
Introduction
The usefulness of a photochemical reflectance index (PRI) approach to link plant photosynthetic CO2 uptake efficiency in changing light (light use efficiency, LUE) and remotely sensed data has been widely reported (Garbulsky et al., 2008; Peñuelas et al., 2011). PRI is based on our understanding of the photoprotective role of xanthophyll cycle pigments within plants. When plants absorb more light energy than can be used by chlorophyll to produce glucose, excessive light energy is either transferred to xanthophyll molecules and emitted as heat or emitted as fluorescence (Gamon et al., 1992; Rascher et al., 2009). Variations in xanthophyll cycle pigment concentrations and conversions produce reflectance changes at a wavelength of 531 nm. Comparing this reflectance with a reference wavelength (typically 570 nm) can be used to detect stress (Gamon et al., 1997, Gamon et al., 1992; Peñuelas et al., 1995). Examination of empirical work has determined a fundamental relationship between plant photochemistry and PRI that is based on the responsiveness of photosynthesis to irradiance.
The variability of factors that may affect canopy-measured PRI can produce confusion in interpreting PRI, in addition to the desirable effects introduced by changing pigments. In field applications, sun–canopy–sensor geometry can exert a strong effect on the resulting PRI values, as light fields may vary in complex ways with canopy structure (Middleton et al., 2009; Sims et al., 2006). Wu et al. (2015) examined crops and found the structural dependence of PRI on leaf area index (LAI). In addition, these authors proposed a solution for removal of the structural signal, and their results imply that LAI change as a consequence of a change in the illumination angle can impact the measured PRI of the canopy. The results reported by Wu et al. (2015) and Gitelson et al. (2017) suggest that canopy structure-related LAI interferences should be considered when evaluating PRI responses between canopies with lower LAI.
The foliar ratio of chlorophylls to carotenoids (Chla+b/Carx+c) has a strong impact on the observed PRI variability (Filella et al., 2009). Decreasing Chla+b/Carx+c may be related to photosynthesis downregulation in stressed plants, but the changes in pigments may also cause impairment of the PRI–LUE relationship over the long term. Attempts have been made to eliminate the Chla+b/Carx+c variability in the measured signal by deconvoluting the influence of pigments. Gamon and Surfus (1999) have shown an opportunity to detract the extent of xanthophyll cycle pigment conversions by subtracting measured PRI value from the starting PRI value in introduced ΔPRI (ΔPRI = PRI0 – PRI). Following this work, Gamon and Berry (2012) characterized differences in ΔPRI between sun and shade leaves as induced with pigment changes. This study has shown that PRI0 represents a PRI state to which PRI values can be related if the comparison of diurnal changes and plant groups is required. Ideally, PRI0 is measured at low irradiance on leaves with inactivated protective functions to isolate the slow changing component of PRI most likely related to Chla+b/Carx+c and the concentration of lutein pigments. Magney et al. (2016) determined that the ΔPRI does respond to diurnal physiological changes resulting from changes in VPD, air temperature, and stomatal conductance and suggested that these changes may be dependent on the observed pigment dynamics. Nitrogen availability affecting amounts of chlorophylls was considered a primary driver of ΔPRI sensitivity in this study, defining the slope of the observed dependency. ΔPRI yields better correlations in nutrient-deficient plots, thereby indicating the importance of carotenoid levels in observed relationships. There are several good examples showing the opportunity to better estimate LUE from PRI measured at the top of the canopy, if the value of PRI is corrected to the morning PRI0 (Hmimina et al., 2015, Hmimina et al., 2014; Ripullone et al., 2011; Soudani et al., 2014). The presented studies often involve drought stress in the experimental design as the main factor driving photosynthesis declines and the magnitude of PRI response (Magney et al., 2016). We intend to further study the basics of the improved relationship between photosynthetic LUE and ΔPRI, and the desirable role of changing pigments in developing these relationships under conditions involving induced changes in irradiance and temperature.
Differences in the sensitivity of photosynthetic processes to light and temperature stress among species suggest the occurrence of interactive effects on photosynthetic pigments. An insufficient understanding of the associated reflectance signature in relation to the measure of photosynthesis is consequential (Ollinger, 2011; Sims and Gamon, 2002). The co-variation of environmental drivers in the upper canopy suggests that leaves in the upper canopy are often exposed to greater stress originating from exposure of leaves to direct light (Niinemets and Valladares, 2004). Upper canopy leaves may suffer from a variety of additional stresses, among which temperature stress may play a particularly substantial role (Williams et al., 1996). The upper canopy crown, usually accounted for in spectrometric measurements, may represent a substantial portion of the canopy involved in the observed gas exchange (Coops et al., 2017). However, the functional trait attributes of plants may not be the only features able to explain changes in PRI in a given environment. It may also be necessary to account for the PRI variations with changing Chla+b/Carx+c that determines the constitutive (slow-changing) component of the PRI. It has been suggested that the finer definition of the facultative process (fast-changing with xanthophyll cycle) can help to detect LUE and responses to summer stress, such as heat and drought (Gamon and Bond, 2013). Our previous development provided elementary knowledge of PRI changes in relation to dynamic fluctuations of photosynthetically active radiation (PAR) and temperature (Kováč et al., 2018). This study suggests large improvement in estimating LUE from ΔPRI, with measurements of PRI0 that correspond to the xanthophyll cycle pigment conversion state in the dark. Changes in PRI–LUE and ΔPRI–LUE relationships have yet to be investigated with dynamic irradiance increases and temperature changes occurring on a daily scale.
We aimed to study further the sensitivity of both PRI and ΔPRI to decreasing and increasing photosynthesis in fluctuating environments. In this study, we focused on observations of the effect of mutual interactions among the plant pigments and overall canopy LAI on the developing relationship between PRI and LUE in changing temperature conditions. Understanding the aspects of LUE estimations using PRI would improve the applicability of PRI measurements in remote-sensing applications. We aimed to overcome the canopy structural effect on measured PRI by fixing the illumination–observation setup of the measurement by measuring canopies within the closed environment of a growth chamber. We thus compared responses in photosynthesis, pigments and PRI of tree species with distinctive sensitivities to low and high temperatures. Norway spruce trees, which prefer cold regions and higher altitudes, were compared with European beech trees, which show tolerance to higher temperatures and grow at lower altitudes. We established four regimes that varied in their daily sum of irradiance income even as the trees were undergoing similar periodic changes in temperature on a daily scale. We measured how the changes in pigments within these regimes affected the observed PRI–LUE relationship and examined the role of established pigment concentrations in the developing sensitivity of PRI and ΔPRI to LUE.
Section snippets
Setup of the experiment
For the study, we selected two tree species with different habitat preferences: European beech (Fagus sylvatica) and Norway spruce (Picea abies). These species are widespread within the Czech Republic and the Central European region, with a distribution generally occurring according to their contrasting climate and temperature demands. Saplings of the selected tree species aged 3–4 years old (0.5–0.6 m tall) were grown in pots in the garden of the Global Change Research Institute from early
Relationships among environmental, optical, and physiological variables
Principal component 1 (PC1) explained 37.6% of the total variation in European beech and 38.9% of the total variation in Norway spruce data (Fig. 3). The functional traits responded significantly to PAR. PAR determines the positions of individual values on the variable factor map, with individual data points measured at low irradiances situated towards the bottom, negative part of the axis, whereas data measured under high irradiances (1500 μmol m−2 s−1) are situated towards the opposite end of
Discussion
The advantage of using ΔPRI over applying simply measured PRI for the purpose of extracting LUE has been examined in this study. The presented work confirmed that the de-epoxidation cycle of leaf pigments involved in NPQ has a general effect of decreasing the reflectance magnitude at wavelengths around 531 nm (Gamon et al., 1990) with increasing light. The dynamics of PRI in our experimental regimes of heating and cooling furthermore indicated that PRI shows an ability to track photosynthesis
Conclusion
The results showed that photosynthesis estimation using PRI over periods longer than days may be limited by changing dynamics of the foliar Chla+b/Carx+c ratio with stress from irradiance. The extent of the Chla+b/Carx+c limitation in our measurements was dependent on the leaf area index of the measured trees; we recorded greater interference from Chla+b/Carx+c in beech saplings with a lower LAI. An improved assessment of dynamic changes in photosynthetic activity induced with changes in
CRediT authorship contribution statement
Daniel Kováč: Conceptualization, Supervision, Formal analysis, Writing - original draft, Methodology. Barbora Veselá: Data curation, Formal analysis, Methodology. Karel Klem: Formal analysis, Writing - review & editing. Kristýna Večeřová: Data curation, Methodology. Zuzana Materová Kmecová: Data curation, Methodology. Josep Peñuelas: Writing - review & editing. Otmar Urban: Writing - review & editing, Project administration.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This work was supported by the Ministry of Education, Youth, and Sports of the Czech Republic within the National Infrastructure for Carbon Observations-CzeCOS (No. LM2015061) and SustES – Adaptation strategies for sustainable ecosystem services and food security under adverse environmental conditions (CZ.02.1.01/0.0/0.0/16_019/0000797). JP also acknowledges funding from European Research Council Synergy grant ERC-SyG-2013-610028 IMBALANCE-P.
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