Reflectance indices as nondestructive indicators of the physiological status of Ceratonia siliqua seedlings under varying moisture and temperature regimes
Júlio Osório A C , Maria Leonor Osório B and Anabela Romano BA Institute of Mediterranean Agricultural and Environmental Sciences, Faculty of Sciences and Technology, University of Algarve, Ed. 8, Campus de Gambelas, 8005-139 Faro, Portugal.
B Institute for Biotechnology and Bioengineering, Centre of Genomics and Biotechnology, Faculty of Sciences and Technology, University of Algarve, Ed. 8, Campus de Gambelas, 8005-139 Faro, Portugal.
C Corresponding author. Email: josorio@ualg.pt
Functional Plant Biology 39(7) 588-597 https://doi.org/10.1071/FP11284
Submitted: 19 December 2011 Accepted: 16 May 2012 Published: 29 June 2012
Abstract
We investigated the use of spectral reflectance techniques to monitor the physiological responses of Ceratonia siliqua L. seedlings exposed to different levels of water availability under normal (25 : 18°C, day : night) and elevated (32 : 21°C, day : night) temperatures. Three spectral reflectance indices (photochemical reflectance index, PRI; water index, WI; red edge position, REP) were measured along with water status, chlorophyll fluorescence and chlorophyll concentration variables in the leaves of well watered, moderately stressed, severely stressed and rehydrated plants under each temperature regime. The PSII effective photochemical efficiency (φ2) and the intrinsic efficiency of open PSII centres (F′v/F′m) correlated significantly with PRI, and these three variables loaded heavily onto the same principal component of a three-factor principal component analysis solution. Water concentration (WC) and the succulence index (SI) were more strongly correlated with WI than either water potential (ΨPD) or relative water content (RWC). Accordingly, WI, WC and SI were combined in the second principal component, and ΨPD and RWC in the third. Our results provide clear evidence for interaction between water availability and temperature in the WI and the PRI response segments of the reflectance curves. Elevated temperature inhibited the recovery of WI spectral segments more than that of the PRI segments in SS plants. REP showed a strongly positive linear relationship with leaf total chlorophyll concentration across all water and temperature treatment combinations. PRI, WI and REP are therefore reliable markers that can be used to monitor φ2, WC and total chlorophyll concentration, respectively, in C. siliqua seedlings under drought and temperature stress.
Additional keywords: chlorophyll a fluorescence, photochemical reflectance index, red edge position, temperature stress, water index, water stress.
References
Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Australian Journal of Biological Sciences 15, 413–428.Busch F, Hüner NPA, Ensminger I (2009) Biochemical constrains limit the potential of the photochemical reflectance index as a predictor of effective quantum efficiency of photosynthesis during the winter spring transition in Jack pine seedlings. Functional Plant Biology 36, 1016–1026.
| Biochemical constrains limit the potential of the photochemical reflectance index as a predictor of effective quantum efficiency of photosynthesis during the winter spring transition in Jack pine seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlOgs7rE&md5=640c50d32c6839f70f9dfe261fa80887CAS |
Carter GA (1993) Responses of leaf spectral reflectance to plant stress. American Journal of Botany 80, 239–243.
| Responses of leaf spectral reflectance to plant stress.Crossref | GoogleScholarGoogle Scholar |
Cornic G (1994) Drought stress and high light effects on leaf photosynthesis. In ‘Photoinhibition of photosynthesis: from molecular mechanisms to the field’. (Eds NR Baker, JR Bowyer) pp. 297–313. (BIOS Scientific Publishers: Oxford)
Curran PJ, Dungan JL, Gholz HL (1990) Exploring the relationship between reflectance red edge and chlorophyll content in slash pine. Tree Physiology 7, 33–48.
Curran PJ, Windham WR, Gholz HL (1995) Exploring the relationship between reflectance red edge and chlorophyll concentration in slash pine leaves. Tree Physiology 15, 203–206.
Dawson TP, Curran PJ (1998) A new technique for interpolating the reflectance red edge position. International Journal of Remote Sensing 19, 2133–2139.
| A new technique for interpolating the reflectance red edge position.Crossref | GoogleScholarGoogle Scholar |
Demmig-Adams B, Adams WW (1992) Photoprotection and other responses of plants to light stress. Annual Review of Plant Physiology and Plant Molecular Biology 43, 599–626.
| Photoprotection and other responses of plants to light stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xks1Knu70%3D&md5=1f76b6236cf17e7a01e4821f54804c2cCAS |
Demmig-Adams B, Adams WW (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends in Plant Science 1, 21–26.
| The role of xanthophyll cycle carotenoids in the protection of photosynthesis.Crossref | GoogleScholarGoogle Scholar |
Filella I, Peñuelas J (1994) The red edge position and shape as indicators of plant chlorophyll content, biomass potential for land applications. International Journal of Remote Sensing 15, 1459–1470.
| The red edge position and shape as indicators of plant chlorophyll content, biomass potential for land applications.Crossref | GoogleScholarGoogle Scholar |
Gamon JA, Surfus JS (1999) Assessing leaf pigment content and activity with a reflectometer. New Phytologist 143, 105–117.
| Assessing leaf pigment content and activity with a reflectometer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlvFSgsbc%3D&md5=dff4c0cd9d56c07381711c4b34b1c0a1CAS |
Gamon JA, Field CB, Bilger W, Björkman O, Fredeen AL, Peñuelas J (1990) Remote sensing of the xanthophyll cycle and chlorophyll fluorescence in sunflower leaves and canopies. Oecologia 85, 1–7.
| Remote sensing of the xanthophyll cycle and chlorophyll fluorescence in sunflower leaves and canopies.Crossref | GoogleScholarGoogle Scholar |
Gamon JA, Peñuelas J, Field CB (1992) A narrow-waveband spectral index that tracks diurnal changes in photosynthetic efficiency. Remote Sensing of Environment 41, 35–44.
| A narrow-waveband spectral index that tracks diurnal changes in photosynthetic efficiency.Crossref | GoogleScholarGoogle Scholar |
Garbulsky MF, Peñuelas J, Gamon J, Inoue Y, Filella I (2011) The photochemical reflectance index (PRI) and the remote sensing of leaf, canopy and ecosystem radiation use efficiencies. A review and meta-analysis. Remote Sensing of Environment 115, 281–297.
| The photochemical reflectance index (PRI) and the remote sensing of leaf, canopy and ecosystem radiation use efficiencies. A review and meta-analysis.Crossref | GoogleScholarGoogle Scholar |
Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87–92.
| The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXhsFWntL4%3D&md5=b1e6f4f065fb1987a8ebc6ee811cafe8CAS |
Gitelson AA, Merzlyak MN, Lichtenthaler HK (1996) Detection of red edge position and chlorophyll content by reflectance measurements near 700 nm. Journal of Plant Physiology 148, 501–508.
| Detection of red edge position and chlorophyll content by reflectance measurements near 700 nm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjslWjsLg%3D&md5=c8e6e96c25722d18ec24b7e03018d1a8CAS |
Govender M, Dye PJ, Weiersbye IM, Witkowski ETF, Ahmed F (2009) Review of commonly used remote sensing and ground-based technologies to measure plant water stress. Water S.A. 35, 741–752.
| Review of commonly used remote sensing and ground-based technologies to measure plant water stress.Crossref | GoogleScholarGoogle Scholar |
Horler DNH, Dockray M, Barber J (1983) The red edge of plant leaf reflectance. International Journal of Remote Sensing 4, 273–288.
| The red edge of plant leaf reflectance.Crossref | GoogleScholarGoogle Scholar |
Jackson RD (1986) Remote sensing of biotic and abiotic plant stress. Annual Review of Phytopathology 24, 265–287.
| Remote sensing of biotic and abiotic plant stress.Crossref | GoogleScholarGoogle Scholar |
Jago RA, Cutler MEJ, Curran PJ (1999) Estimating canopy chlorophyll concentration from field and airborne spectra. Remote Sensing of Environment 68, 217–224.
| Estimating canopy chlorophyll concentration from field and airborne spectra.Crossref | GoogleScholarGoogle Scholar |
Leone AP, Menenti M, Buondonno A, Letizia A, Maffei C, Sorrentino G (2007) A field experiment on spectrometry of crop response to soil salinity. Agricultural Water Management 89, 39–48.
| A field experiment on spectrometry of crop response to soil salinity.Crossref | GoogleScholarGoogle Scholar |
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology 148, 350–382.
| Chlorophylls and carotenoids: pigments of photosynthetic biomembranes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXhs1Cgu78%3D&md5=46881071f2fd7b31c9d89c1d4bdb8a57CAS |
Lichtenthaler HK, Gitelson A, Lang M (1996) Non-destructive determination of chlorophyll content of leaves of a green and an aurea mutant of tobacco by reflectance measurements. Journal of Plant Physiology 148, 483–493.
| Non-destructive determination of chlorophyll content of leaves of a green and an aurea mutant of tobacco by reflectance measurements.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjslWjsLo%3D&md5=40451fb9ef94f94776ea93c1e2a32931CAS |
Mariotti M, Ercoli L, Masoni A (1996) Spectral properties of iron-deficient corn and sunflower leaves. Remote Sensing of Environment 58, 282–288.
| Spectral properties of iron-deficient corn and sunflower leaves.Crossref | GoogleScholarGoogle Scholar |
Méthy M (2000) Analysis of photosynthetic activity at the leaf and canopy levels from reflectance measurements: a case study. Photosynthetica 38, 505–512.
| Analysis of photosynthetic activity at the leaf and canopy levels from reflectance measurements: a case study.Crossref | GoogleScholarGoogle Scholar |
Montgomery RA, Goldstein G, Givnish TJ (2008) Photoprotection of PSII in Hawaiian lobeliads from diverse light environments. Functional Plant Biology 35, 595–605.
| Photoprotection of PSII in Hawaiian lobeliads from diverse light environments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVSrsrrL&md5=1c79a39c4cb20bc6ec2a94bda0ff1829CAS |
Munden R, Curran PJ, Catt JA (1994) The relationship between red edge and chlorophyll concentration in the Broadbalk winter wheat experiment at Rothamsted. International Journal of Remote Sensing 15, 705–709.
| The relationship between red edge and chlorophyll concentration in the Broadbalk winter wheat experiment at Rothamsted.Crossref | GoogleScholarGoogle Scholar |
Omae H, Kumar A, Kashiwaba K, Shono M (2007) Assessing drought tolerance of snap bean (Phaseolus vulgaris) from genotypic differences in leaf water relations, shoot growth and photosynthetic parameters. Plant Production Science 10, 28–35.
| Assessing drought tolerance of snap bean (Phaseolus vulgaris) from genotypic differences in leaf water relations, shoot growth and photosynthetic parameters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitlyitrs%3D&md5=4338baf26d6c695fbcc9c920a97015daCAS |
Osório ML, Osório J, Vieira AC, Gonçalves S, Romano A (2011) Influence of enhanced temperature on photosynthesis, photooxidative damage, and antioxidant strategies in Ceratonia siliqua L. seedlings subjected to water deficit and rewatering. Photosynthetica 49, 3–12.
| Influence of enhanced temperature on photosynthesis, photooxidative damage, and antioxidant strategies in Ceratonia siliqua L. seedlings subjected to water deficit and rewatering.Crossref | GoogleScholarGoogle Scholar |
Panigada C, Rossini M, Meroni M, Marzuoli R, Gerosa G, Colombo R (2009) Indicators of ozone effects on Fagus sylvatica L. by means of spectroradiometric measurements. Italian Journal of Remote Sensing 41, 3–20.
Peguero-Pina JJ, Morales F, Flexas J, Gil-Pelegrín E, Moya I (2008) Photochemistry, remotely sensed physiological reflectance index and de-epoxidation state of the xanthophyll cycle in Quercus coccifera under intense drought. Oecologia 156, 1–11.
| Photochemistry, remotely sensed physiological reflectance index and de-epoxidation state of the xanthophyll cycle in Quercus coccifera under intense drought.Crossref | GoogleScholarGoogle Scholar |
Peñuelas J, Filella I (1998) Visible and near-infrared reflectance techniques for diagnosing plant physiological status. Trends in Plant Science 3, 151–156.
| Visible and near-infrared reflectance techniques for diagnosing plant physiological status.Crossref | GoogleScholarGoogle Scholar |
Peñuelas J, Inoue Y (1999) Reflectance indices indicative of changes in water and pigment contents of peanut and wheat leaves. Photosynthetica 36, 355–360.
| Reflectance indices indicative of changes in water and pigment contents of peanut and wheat leaves.Crossref | GoogleScholarGoogle Scholar |
Peñuelas J, Filella I, Biel C, Serrano L, Savé R (1993a) The reflectance at the 950–970 nm region as an indicator of plant water status. International Journal of Remote Sensing 14, 1887–1905.
| The reflectance at the 950–970 nm region as an indicator of plant water status.Crossref | GoogleScholarGoogle Scholar |
Peñuelas J, Gamon JA, Griffin KL, Field CB (1993b) Assessing community type, plant biomass, pigment composition, and photosynthetic efficiency of aquatic vegetation from spectral reflectance. Remote Sensing of Environment 46, 110–118.
| Assessing community type, plant biomass, pigment composition, and photosynthetic efficiency of aquatic vegetation from spectral reflectance.Crossref | GoogleScholarGoogle Scholar |
Peñuelas J, Gamon JA, Fredeen AL, Merino J, Field CB (1994) Reflectance indices associated with physiological changes in nitrogen- and water-limited sunflower leaves. Remote Sensing of Environment 48, 135–146.
| Reflectance indices associated with physiological changes in nitrogen- and water-limited sunflower leaves.Crossref | GoogleScholarGoogle Scholar |
Peñuelas J, Filella I, Gamon JA (1995) Assessment of plant photosynthetic radiation-use efficiency with spectral reflectance. New Phytologist 131, 291–296.
| Assessment of plant photosynthetic radiation-use efficiency with spectral reflectance.Crossref | GoogleScholarGoogle Scholar |
Peñuelas J, Llusia J, Pinol J, Filella I (1997a) Photochemical reflectance index and leaf photosynthetic radiation-use-efficiency assessment in Mediterranean trees. International Journal of Remote Sensing 18, 2863–2868.
| Photochemical reflectance index and leaf photosynthetic radiation-use-efficiency assessment in Mediterranean trees.Crossref | GoogleScholarGoogle Scholar |
Peñuelas J, Pinol J, Ogaya R, Filella I (1997b) Estimation of plant water concentration by the reflectance water index WI (R900/R970). International Journal of Remote Sensing 18, 2869–2875.
| Estimation of plant water concentration by the reflectance water index WI (R900/R970).Crossref | GoogleScholarGoogle Scholar |
Peñuelas J, Munné-Bosch S, Llusià J, Filella I (2004) Leaf reflectance and photo- and antioxidant protection in field-grown summer-stressed Phillyrea angustifolia. Optical signals of oxidative stress? New Phytologist 162, 115–124.
| Leaf reflectance and photo- and antioxidant protection in field-grown summer-stressed Phillyrea angustifolia. Optical signals of oxidative stress?Crossref | GoogleScholarGoogle Scholar |
Pinar A, Curran PJ (1996) Grass chlorophyll and the reflectance red edge. International Journal of Remote Sensing 17, 351–357.
| Grass chlorophyll and the reflectance red edge.Crossref | GoogleScholarGoogle Scholar |
Rascher U, Nichol CJ, Small C, Hendricks L (2007) Monitoring spatio-temporal dynamics of photosynthesis with a portable hyperspectral imaging system. Photogrammetric Engineering and Remote Sensing 73, 45–56.
Richardson AD, Duigan SP, Berlyn GP (2002) An evaluation of noninvasive methods to estimate foliar chlorophyll content. New Phytologist 153, 185–194.
| An evaluation of noninvasive methods to estimate foliar chlorophyll content.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xns1yrsQ%3D%3D&md5=d2334265e6edeafd79a093e79389779eCAS |
Ripullone F, Rivelli AR, Baraldi R, Guarini R, Guerrieri R, Magnani F, Peñuelas J, Raddi S, Borghetti M (2011) Effectiveness of the photochemical reflectance index to track photosynthetic activity over a range of forest tree species and plant water statuses. Functional Plant Biology 38, 177–186.
| Effectiveness of the photochemical reflectance index to track photosynthetic activity over a range of forest tree species and plant water statuses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjvVOjsbs%3D&md5=8cec25ddd1a8e1dad2b5ec0e766ec337CAS |
Serrano L, Gonzalez-Flor C, Gorchs G (2010) Assessing vineyard water status using the reflectance based water index. Agriculture Ecosystems & Environment 139, 490–499.
| Assessing vineyard water status using the reflectance based water index.Crossref | GoogleScholarGoogle Scholar |
Sims DA, Gamon JA (2002) Relationships between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages. Remote Sensing of Environment 81, 337–354.
| Relationships between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages.Crossref | GoogleScholarGoogle Scholar |
Smith KL, Steven MD, Colls JJ (2004) Use of hyperspectral derivative ratios in the red-edge region to identify plant stress responses to gas leak. Remote Sensing of Environment 92, 207–217.
| Use of hyperspectral derivative ratios in the red-edge region to identify plant stress responses to gas leak.Crossref | GoogleScholarGoogle Scholar |
Stylinski CD, Gamon JA, Oechel WC (2002) Seasonal patterns of reflectance indices, carotenoid pigments and photosynthesis of evergreen chaparral species. Oecologia 131, 366–374.
| Seasonal patterns of reflectance indices, carotenoid pigments and photosynthesis of evergreen chaparral species.Crossref | GoogleScholarGoogle Scholar |
Wangxia W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218, 1–14.
| Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance.Crossref | GoogleScholarGoogle Scholar |
Weng JH, Chen YN, Liao TS (2006a) Relationships between chlorophyll fluorescence parameters and photochemical reflectance index of tree species adapted to different temperature regimes. Functional Plant Biology 33, 241–246.
| Relationships between chlorophyll fluorescence parameters and photochemical reflectance index of tree species adapted to different temperature regimes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhvFCqsrk%3D&md5=972df1dddf07864dd72577624acec024CAS |
Weng JH, Jhaung LH, Jiang JY, Lai GM, Liao TS (2006b) Down-regulation of photosystem 2 efficiency and spectral reflectance in mango leaves under very low irradiance and varied chilling treatments. Photosynthetica 44, 248–254.
| Down-regulation of photosystem 2 efficiency and spectral reflectance in mango leaves under very low irradiance and varied chilling treatments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjvFSnsbY%3D&md5=fecc91eb1fda48f36044d56f05e08359CAS |
Weng JH, Liao TS, Hwang MY, Chung CC, Lin CP, Chu CH (2006c) Seasonal variation in photosystem II efficiency and photochemical reflectance index of evergreen trees and perennial grasses growing at low and high elevations in subtropical Taiwan. Tree Physiology 26, 1097–1104.
| Seasonal variation in photosystem II efficiency and photochemical reflectance index of evergreen trees and perennial grasses growing at low and high elevations in subtropical Taiwan.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xot1ygsrw%3D&md5=defd03c0ef88924c315f9bf7fc93acf1CAS |
Weng JH, Lai KM, Liao TS, Hwang MY, Chen YN (2009) Relationships of photosynthetic capacity to PSII efficiency and to photochemical reflectance index of Pinus taiwanensis through different seasons at high and low elevations of subtropical Taiwan. Trees – Structure and Function 23, 347–356.
| Relationships of photosynthetic capacity to PSII efficiency and to photochemical reflectance index of Pinus taiwanensis through different seasons at high and low elevations of subtropical Taiwan.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivFSms78%3D&md5=61454be06cc94f48d9c9fc703bcb5bbaCAS |