Proximal Imaging of Changes in Photochemical Reflectance Index in Leaves Based on Using Pulses of Green-Yellow Light

Plants are affected by numerous environmental factors that influence their physiological processes and productivity. Early revealing of their action based on measuring spectra of reflected light and calculating reflectance indices is an important stage in the protection of agricultural plants. Photochemical reflectance index (PRI) is a widely used parameter related to photosynthetic changes in plants under action of stressors. We developed a new system for proximal imaging of PRI based on using short pulses of measuring light detected simultaneously in green (530 nm) and yellow (570 nm) spectral bands. The system has several advances compared to those reported in literature. Active light illumination and subtraction of the ambient light allow for PRI measurements without periodic calibrations. Short duration of measuring pulses (18 ms) minimizes their influence on plants. Measurements in two spectral bands operated by separate cameras with aligned fields of visualization allow one to exclude mechanically switchable parts like filter wheels thus minimizing acquisition time and increasing durability of the setup. Absolute values of PRI and light-induced changes in PRI (ΔPRI) in pea leaves and changes of these parameters under action of light with different intensities, water shortage, and heating have been investigated using the developed setup. Changes in ΔPRI are shown to be more robust than the changes in the absolute value of PRI which is in a good agreement with our previous studies. Values of PRI and, especially, ΔPRI are strongly linearly related to the energy-dependent component of the non-photochemical quenching and can be potentially used for estimation of this component. Additionally, we demonstrate that the developed system can also measure fast changes in PRI (hundreds of milliseconds and seconds) under leaf illumination by the pulsed green-yellow measuring light. Thus, the developed system of proximal PRI imaging can be used for PRI measurements (including fast changes in PRI) and estimation of stressors-induced photosynthetic changes.

[1]  C. Field,et al.  Canopy near-infrared reflectance and terrestrial photosynthesis , 2017, Science Advances.

[2]  Ekaterina Sukhova,et al.  Relation of Photochemical Reflectance Indices Based on Different Wavelengths to the Parameters of Light Reactions in Photosystems I and II in Pea Plants , 2020, Remote. Sens..

[3]  J. Peñuelas,et al.  Relationship between photosynthetic radiation-use efficiency of barley canopies and the photochemical reflectance index (PRI) , 1996 .

[4]  D. Deamer,et al.  Mechanisms of light-induced structural changes in chloroplasts I. Light-scattering increments and ultrastructural changes mediated by proton transport , 1967 .

[5]  E. Aro,et al.  Low pH‐induced regulation of excitation energy between the two photosystems , 2014, FEBS letters.

[6]  Relationships between photosystem II efficiency and photochemical reflectance index under different levels of illumination: comparison among species grown at high- and low elevations through different seasons , 2012, Trees.

[7]  Josep Peñuelas,et al.  Potential of Photochemical Reflectance Index for Indicating Photochemistry and Light Use Efficiency in Leaves of European Beech and Norway Spruce Trees , 2018, Remote. Sens..

[8]  Majed A. Alotaibi,et al.  Ability of Modified Spectral Reflectance Indices for Estimating Growth and Photosynthetic Efficiency of Wheat under Saline Field Conditions , 2019, Agronomy.

[9]  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 .

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

[11]  C. Frankenberg,et al.  Linking chlorophyll a fluorescence to photosynthesis for remote sensing applications: mechanisms and challenges. , 2014, Journal of experimental botany.

[12]  Anne-Katrin Mahlein Plant Disease Detection by Imaging Sensors - Parallels and Specific Demands for Precision Agriculture and Plant Phenotyping. , 2016, Plant disease.

[13]  K Maxwell,et al.  Chlorophyll fluorescence--a practical guide. , 2000, Journal of experimental botany.

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

[15]  V. Sukhov,et al.  The electrical signal-induced systemic photosynthetic response is accompanied by changes in the photochemical reflectance index in pea. , 2019, Functional plant biology : FPB.

[16]  A. Ruban Nonphotochemical Chlorophyll Fluorescence Quenching: Mechanism and Effectiveness in Protecting Plants from Photodamage1 , 2016, Plant Physiology.

[17]  M. S. Moran,et al.  Remote Sensing for Crop Management , 2003 .

[18]  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.

[19]  Josep Peñuelas,et al.  Assessing Ecosystem Isoprene Emissions by Hyperspectral Remote Sensing , 2018, Remote. Sens..

[20]  J. Serôdio,et al.  Frequently asked questions about in vivo chlorophyll fluorescence: practical issues , 2014, Photosynthesis Research.

[21]  L. Alonso,et al.  In vivo photoprotection mechanisms observed from leaf spectral absorbance changes showing VIS–NIR slow-induced conformational pigment bed changes , 2019, Photosynthesis Research.

[22]  Oksana Sytar,et al.  Evaluation of Hyperspectral Reflectance Parameters to Assess the Leaf Water Content in Soybean , 2019, Water.

[23]  Y. Ibaraki,et al.  Nondestructive evaluation of the photosynthetic properties of micropropagated plantlets by imaging photochemical reflectance index under low light intensity , 2010, In Vitro Cellular & Developmental Biology - Plant.

[24]  Ekaterina Sukhova,et al.  Connection of the Photochemical Reflectance Index (PRI) with the Photosystem II Quantum Yield and Nonphotochemical Quenching Can Be Dependent on Variations of Photosynthetic Parameters among Investigated Plants: A Meta-Analysis , 2018, Remote. Sens..

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

[26]  Paul E. Gessler,et al.  Sensitivity of Ground‐Based Remote Sensing Estimates of Wheat Chlorophyll Content to Variation in Soil Reflectance , 2009 .

[27]  A. Gitelson,et al.  Spectral reflectance changes associated with autumn senescence of Aesculus hippocastanum L. and Acer platanoides L. leaves. Spectral features and relation to chlorophyll estimation , 1994 .

[28]  Majed A. Alotaibi,et al.  Comparative Performance of Spectral Reflectance Indices and Multivariate Modeling for Assessing Agronomic Parameters in Advanced Spring Wheat Lines Under Two Contrasting Irrigation Regimes , 2019, Front. Plant Sci..

[29]  J. Peñuelas,et al.  Correction of PRI for carotenoid pigment pools improves photosynthesis estimation across different irradiance and temperature conditions , 2020, Remote Sensing of Environment.

[30]  O. Sytar,et al.  Nondestructive detection and biochemical quantification of buckwheat leaves using visible (VIS) and near-infrared (NIR) hyperspectral reflectance imaging , 2017 .

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

[32]  J. Peñuelas,et al.  Photochemical reflectance index as an indirect estimator of foliar isoprenoid emissions at the ecosystem level , 2013, Nature Communications.

[33]  Josep Peñuelas,et al.  Photochemical Reflectance Index (PRI) for Detecting Responses of Diurnal and Seasonal Photosynthetic Activity to Experimental Drought and Warming in a Mediterranean Shrubland , 2017, Remote. Sens..

[34]  W. Bilger,et al.  Light-induced spectral absorbance changes in relation to photosynthesis and the epoxidation state of xanthophyll cycle components in cotton leaves. , 1989, Plant physiology.

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

[36]  M. Feng,et al.  Assessment of plant water status in winter wheat (Triticum aestivum L.) based on canopy spectral indices , 2019, PloS one.

[37]  Y. Ibaraki,et al.  Time course of the photochemical reflectance index during photosynthetic induction: its relationship with the photochemical yield of photosystem II. , 2018, Physiologia plantarum.

[38]  J. Peñuelas,et al.  Estimation of plant water concentration by the reflectance Water Index WI (R900/R970) , 1997 .

[39]  Anne-Katrin Mahlein,et al.  Hyperspectral Sensors and Imaging Technologies in Phytopathology: State of the Art. , 2018, Annual review of phytopathology.

[40]  V. Sukhov,et al.  Burning-induced electrical signals influence broadband reflectance indices and water index in pea leaves , 2020, Plant signaling & behavior.

[41]  V. Sukhov,et al.  Influence of electrical signals on pea leaf reflectance in the 400–800-nm range , 2019, Plant signaling & behavior.

[42]  U. Schreiber,et al.  New accessory for the DUAL-PAM-100: The P515/535 module and examples of its application , 2008 .

[43]  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 .

[44]  U. Steiner,et al.  Spectral signatures of sugar beet leaves for the detection and differentiation of diseases , 2010, Precision Agriculture.

[45]  John A Gamon,et al.  Three causes of variation in the photochemical reflectance index (PRI) in evergreen conifers. , 2015, The New phytologist.

[46]  Stefan Jansson,et al.  A pigment-binding protein essential for regulation of photosynthetic light harvesting , 2000, Nature.

[47]  Ekaterina Sukhova,et al.  Complex Analysis of the Efficiency of Difference Reflectance Indices on the Basis of 400-700 nm Wavelengths for Revealing the Influences of Water Shortage and Heating on Plant Seedlings , 2021, Remote. Sens..

[48]  V. Sukhov,et al.  A light-induced decrease in the photochemical reflectance index (PRI) can be used to estimate the energy-dependent component of non-photochemical quenching under heat stress and soil drought in pea, wheat, and pumpkin , 2020, Photosynthesis Research.

[49]  W. Bilger,et al.  Relationships among violaxanthin deepoxidation, thylakoid membrane conformation, and nonphotochemical chlorophyll fluorescence quenching in leaves of cotton (Gossypium hirsutum L.) , 1994, Planta.

[50]  Josep Peñuelas,et al.  A remotely sensed pigment index reveals photosynthetic phenology in evergreen conifers , 2016, Proceedings of the National Academy of Sciences.

[51]  Continuous ECS-indicated recording of the proton-motive charge flux in leaves , 2013, Photosynthesis Research.

[52]  Low-cost photochemical reflectance index measurements of micropropagated plantlets using image analysis , 2010 .

[53]  K. Hikosaka,et al.  Physiological validation of photochemical reflectance index (PRI) as a photosynthetic parameter using Arabidopsis thaliana mutants. , 2018, Biochemical and biophysical research communications.

[54]  Ekaterina Sukhova,et al.  Analysis of Light-Induced Changes in the Photochemical Reflectance Index (PRI) in Leaves of Pea, Wheat, and Pumpkin Using Pulses of Green-Yellow Measuring Light , 2019, Remote. Sens..

[55]  Ismael Moya,et al.  A new instrument for passive remote sensing: 2. Measurement of leaf and canopy reflectance changes at 531 nm and their relationship with photosynthesis and chlorophyll fluorescence , 2004 .

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

[57]  V. Sukhov,et al.  Analysis of Changes in Photochemical Reflectance Index (PRI) in Relation to the Acidification of the Lumen of the Chloroplasts of Pea and Geranium Leaves under a Short-Term Illumination , 2019, Biochemistry (Moscow), Supplement Series A: Membrane and Cell Biology.

[58]  Mathias Disney,et al.  Can we measure terrestrial photosynthesis from space directly, using spectral reflectance and fluorescence? , 2007 .

[59]  L. Packer,et al.  PROTONATION AND CHLOROPLAST MEMBRANE STRUCTURE , 1970, The Journal of cell biology.

[60]  Jingjue Jiang,et al.  Assessing leaf photoprotective mechanisms using terrestrial LiDAR: towards mapping canopy photosynthetic performance in three dimensions. , 2014, The New phytologist.

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

[62]  Josep Peñuelas,et al.  Affecting Factors and Recent Improvements of the Photochemical Reflectance Index (PRI) for Remotely Sensing Foliar, Canopy and Ecosystemic Radiation-Use Efficiencies , 2016, Remote. Sens..

[63]  Josep Peñuelas,et al.  Leaf and stand-level carbon uptake of a Mediterranean forest estimated using the satellite-derived reflectance indices EVI and PRI , 2012 .

[64]  G. A. Blackburn,et al.  Quantifying Chlorophylls and Caroteniods at Leaf and Canopy Scales: An Evaluation of Some Hyperspectral Approaches , 1998 .

[65]  D. Kramer,et al.  Modulation of energy-dependent quenching of excitons in antennae of higher plants. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[66]  J. Peñuelas,et al.  The reflectance at the 950–970 nm region as an indicator of plant water status , 1993 .

[67]  Josep Peñuelas,et al.  Photochemical reflectance index (PRI) and remote sensing of plant CO₂ uptake. , 2011, The New phytologist.

[68]  B. Gao NDWI—A normalized difference water index for remote sensing of vegetation liquid water from space , 1996 .