Explaining the variability of the photochemical reflectance index (PRI) at the canopy-scale: Disentangling the effects of phenological and physiological changes.

Assessing photosynthesis rates at the ecosystem scale and over large regions is important for tracking the global carbon cycle and remote sensing has provided new and useful approaches for performing this assessment. The photochemical reflectance index (PRI) is a good estimator of short-term light-use efficiency (LUE) at the leaf scale; however, confounding factors appear at larger temporal and spatial scales. In this study, canopy-scale PRI variability was investigated for three species (Fagus sylvatica L., Quercus robur L. and Pinus sylvestris L.) growing under contrasting soil moisture conditions. Throughout the growing season, no significant differences in chlorophyll content and in violaxanthin, antheraxanthin and zeaxanthin were found between species or treatments. The daily PRI vs PAR (photosynthetically active radiation) relationships were determined using continuous measurements obtained at high frequency throughout the entire growing season, from early spring budburst to later autumn senescence, and were used to deconvolute the physiological PRI variability related to LUE variations due to phenological variability and related to temporal changes in the biochemical and structural canopy attributes. The PRI vs PAR relationship is used to show that the canopy-scale PRI measured at low radiation depends on the chlorophyll content of the canopy. The range of PRI variations at an intra-daily scale and the dynamics of the xanthophyll pool do not vary between days, which suggests that the PRI responds to a xanthophyll ratio. The PAR values at PRI saturation are mainly related to the canopy chlorophyll content during budburst and senescence and to the soil moisture content when the chlorophyll content is no longer a limiting factor. This parameter is significantly lower in the oak species that experience less stress from variations in soil moisture and is species dependant. These results provide new insights regarding the analysis and the meaning of PRI variability as a proxy for LUE at the canopy scale.

[1]  A. Huete,et al.  Overview of the radiometric and biophysical performance of the MODIS vegetation indices , 2002 .

[2]  O. Björkman,et al.  Leaf Xanthophyll content and composition in sun and shade determined by HPLC , 1990, Photosynthesis Research.

[3]  Pablo J. Zarco-Tejada,et al.  Assessing Canopy PRI for Water Stress detection with Diurnal Airborne Imagery , 2008 .

[4]  Kenji Takizawa,et al.  The thylakoid proton motive force in vivo. Quantitative, non-invasive probes, energetics, and regulatory consequences of light-induced pmf. , 2007, Biochimica et biophysica acta.

[5]  EVIDENCE FOR A HETEROGENOUS ORGANIZATION OF VIOLAXANTHIN IN THYLAKOID MEMBRANES , 1984 .

[6]  A. Isoda,et al.  Adaptive Responses of Soybean and Cotton to Water Stress II. Changes in CO2 Assimilation Rate, Chlorophyll Fluorescence and Photochemical Reflectance Index in Relation to Leaf Temperature , 2005 .

[7]  Abduwasit Ghulam,et al.  Characterizing Crop Responses to Background Ozone in Open-Air Agricultural Field by Using Reflectance Spectroscopy , 2015, IEEE Geoscience and Remote Sensing Letters.

[8]  Albert Porcar-Castell,et al.  Physiology of the seasonal relationship between the photochemical reflectance index and photosynthetic light use efficiency , 2012, Oecologia.

[9]  B. Palsson,et al.  UPLC-UV-MSE analysis for quantification and identification of major carotenoid and chlorophyll species in algae , 2012, Analytical and Bioanalytical Chemistry.

[10]  Hiroyuki Oguma,et al.  Seasonal changes in the relationship between photochemical reflectance index and photosynthetic light use efficiency of Japanese larch needles , 2006 .

[11]  John A. Gamon,et al.  Monitoring seasonal and diurnal changes in photosynthetic pigments with automated PRI and NDVI sensors , 2015 .

[12]  W. Oechel,et al.  FLUXNET: A New Tool to Study the Temporal and Spatial Variability of Ecosystem-Scale Carbon Dioxide, Water Vapor, and Energy Flux Densities , 2001 .

[13]  P. North,et al.  Remote sensing of canopy light use efficiency using the photochemical reflectance index , 2001 .

[14]  John A. Gamon,et al.  Assessing leaf pigment content and activity with a reflectometer , 1999 .

[15]  K. Soudani,et al.  Relationship between photochemical reflectance index and leaf ecophysiological and biochemical parameters under two different water statuses: towards a rapid and efficient correction method using real-time measurements. , 2014, Plant, cell & environment.

[16]  W. Cleveland Robust Locally Weighted Regression and Smoothing Scatterplots , 1979 .

[17]  Govindjee,et al.  Chlorophyll a Fluorescence: A Signature of Photosynthesis , 2006 .

[18]  T. A. Black,et al.  The use of remote sensing in light use efficiency based models of gross primary production: a review of current status and future requirements. , 2008, The Science of the total environment.

[19]  J. Peñuelas,et al.  Assessment of photosynthetic radiation‐use efficiency with spectral reflectance , 1995 .

[20]  L. Alegre,et al.  Changes in carotenoids, tocopherols and diterpenes during drought and recovery, and the biological significance of chlorophyll loss in Rosmarinus officinalis plants , 2000, Planta.

[21]  C. Field,et al.  A narrow-waveband spectral index that tracks diurnal changes in photosynthetic efficiency , 1992 .

[22]  J. Gamon,et al.  The photochemical reflectance index: an optical indicator of photosynthetic radiation use efficiency across species, functional types, and nutrient levels , 1997, Oecologia.

[23]  Pablo J. Zarco-Tejada,et al.  Simple reflectance indices track heat and water stress-induced changes in steady-state chlorophyll fluorescence at the canopy scale , 2005 .

[24]  Gwendal Latouche,et al.  A new optical leaf-clip meter for simultaneous non-destructive assessment of leaf chlorophyll and epidermal flavonoids , 2012, Physiologia plantarum.

[25]  B. Demmig‐Adams,et al.  Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among higher plant species , 1996, Planta.

[26]  K. Winter,et al.  Light Response of CO(2) Assimilation, Dissipation of Excess Excitation Energy, and Zeaxanthin Content of Sun and Shade Leaves. , 1989, Plant physiology.

[27]  J. Peñuelas,et al.  PRI assessment of long-term changes in carotenoids/chlorophyll ratio and short-term changes in de-epoxidation state of the xanthophyll cycle , 2009 .

[28]  Josep Peñuelas,et al.  Relationship between light use efficiency and photochemical reflectance index in soybean leaves as affected by soil water content , 2006 .

[29]  P. Haldimann,et al.  Photosynthetic performance and water relations in young pubescent oak (Quercus pubescens) trees during drought stress and recovery. , 2007, The New phytologist.

[30]  Josep Peñuelas,et al.  The photochemical reflectance index (PRI) and the remote sensing of leaf, canopy and ecosystem radiation use efficiencies: A review and meta-analysis , 2011 .

[31]  Jan U.H. Eitel,et al.  Disentangling the relationships between plant pigments and the photochemical reflectance index reveals a new approach for remote estimation of carotenoid content , 2011 .

[32]  H. Yamamoto Functional roles of the major chloroplast lipids in the violaxanthin cycle , 2006, Planta.

[33]  W. W. Adams,et al.  Carotenoid composition in sun and shade leaves of plants with different life forms , 1992 .

[34]  K. Omasa,et al.  Relationships between the photochemical reflectance index (PRI) and chlorophyll fluorescence parameters and plant pigment indices at different leaf growth stages , 2012, Photosynthesis Research.

[35]  A. K. Mitchell,et al.  Differentiation among effects of nitrogen fertilization treatments on conifer seedlings by foliar reflectance: a comparison of methods. , 2000, Tree physiology.

[36]  B. Demmig‐Adams,et al.  Survey of Thermal Energy Dissipation and Pigment Composition in Sun and Shade Leaves , 1998 .

[37]  Steven M. Driever,et al.  Photochemical reflectance index as a mean of monitoring early water stress , 2010 .

[38]  D. Sims,et al.  Relationships between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages , 2002 .

[39]  Ulrike Groemping,et al.  Relative Importance for Linear Regression in R: The Package relaimpo , 2006 .

[40]  B. Demmig‐Adams,et al.  Regulation of Photosynthetic Light Energy Capture, Conversion, and Dissipation in Leaves of Higher Plants , 1994 .

[41]  Iolanda Filella,et al.  Reflectance assessment of seasonal and annual changes in biomass and CO2 uptake of a Mediterranean shrubland submitted to experimental warming and drought , 2004 .

[42]  L. Alonso,et al.  Remote sensing of sunlight-induced chlorophyll fluorescence and reflectance of Scots pine in the boreal forest during spring recovery , 2005 .

[43]  B. Demmig‐Adams,et al.  The role of xanthophyll cycle carotenoids in the protection of photosynthesis , 1996 .

[44]  J. Abadía,et al.  Seasonal changes in xanthophyll composition and photosynthesis of cork oak (Quercus suber L.) leaves under mediterranean climate , 1997 .

[45]  R. J. Porra,et al.  Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy , 1989 .

[46]  J. García-Plazaola,et al.  Photoprotection mechanisms in European beech (Fagus sylvatica L.) seedlings from diverse climatic origins , 2000, Trees.

[47]  John A. Gamon,et al.  Facultative and constitutive pigment effects on the Photochemical Reflectance Index (PRI) in sun and shade conifer needles , 2012 .

[48]  G. Liakopoulos,et al.  The photoprotective role of epidermal anthocyanins and surface pubescence in young leaves of grapevine (Vitis vinifera). , 2006, Annals of botany.

[49]  K. Soudani,et al.  Deconvolution of pigment and physiologically related photochemical reflectance index variability at the canopy scale over an entire growing season. , 2015, Plant, cell & environment.

[50]  Christopher B. Field,et al.  Remote sensing of the xanthophyll cycle and chlorophyll fluorescence in sunflower leaves and canopies , 1990, Oecologia.

[51]  W. Oechel,et al.  Seasonal patterns of reflectance indices, carotenoid pigments and photosynthesis of evergreen chaparral species , 2002, Oecologia.