Plant and Soil

, Volume 354, Issue 1–2, pp 45–55 | Cite as

Effects of salinity on physiological responses and the photochemical reflectance index in two co-occurring coastal shrubs

Regular Article


Background and aims

The photochemical reflectance index (PRI) is correlated to photosynthetic efficiency and has been successfully applied at multiple scales for remote estimation of physiological functioning. However, interpretation of the PRI signal can be confounded by many different variables including declines in photochemical pigments. Our study was aimed at investigating PRI in response to salinity stress, and evaluating physiological and pigment responses of two co-occurring shrubs, Baccharis halimifolia and Myrica cerifera in laboratory studies.


Photosynthesis, water relations, chlorophyll fluorescence, hyperspectral reflectance and leaf pigment contents were measured following salinity treatment.


Physiological measurements indicated that both species exhibit adaptations which protect PSII during periods of stress. Chlorophyll fluorescence parameters were affected in both species, but indicated that other photochemical reactions (e.g. photorespiration) were important for energy dissipation in absence of chlorophyll changes. After many days of reduced photosynthesis, photochemical changes were detectable using PRI indicating chronic stress.


Variations in PRI were not related to changes in pigments but strongly related to tissue chlorides indicating salinity effects on the PRI signal. Thus, PRI is an indicator of salinity stress in these coastal species and may be as an early signal for increasing salt exposure associated with rising sea-level and climate change.


Chlorophyll fluorescence Chlorophyll pigments Gas exchange Photosystem II photochemistry PRI Remote sensing Salinity treatment 



The authors thank Donald R Young for thorough review and comments on an earlier draft of this manuscript. This research was supported by internal basic research program funds from the U.S. Army Corps of Engineers/Engineer Research and Development Center (ERDC) and (in part) by the U.S. Army RDECOM ARL Army Research Office under grant W911NF-06-1-0074.


  1. Abdelkader AF, Aronsson H, Solymosi K, Böddi B, Sundqvist C (2007) High salt stress induces swollen prothylakoids in dark-grown wheat and alters both prolamellar body transformation and reformation after irradiation. J Exp Bot 58:2553–2564PubMedCrossRefGoogle Scholar
  2. Atkinson MJ, Bingman C (1997) Elemental composition of commercial seasalts. J Aquaricult Aquat Sci 8:39–43Google Scholar
  3. Barton CVM, North PRJ (2001) Remote sensing of canopy light use efficiency using the photochemical reflectance index. Remote Sens Environ 78:264–273CrossRefGoogle Scholar
  4. Bilger W, Björkman O (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth Res 25:173–185CrossRefGoogle Scholar
  5. Bilger W, Schreiber U (1986) Energy dependent quenching of dark-level chlorophyll fluorescence in intact leaves. Photosynth Res 10:303–308CrossRefGoogle Scholar
  6. Blackburn GA (2007) Hyperspectral remote sensing of plant pigments. J Exp Bot 58:855–867PubMedCrossRefGoogle Scholar
  7. Chaves MM, Pereira JS, Maroco J, Rodrigues ML, Ricardo CPP, Osόrio ML, Carvalho I, Faria T, Pinheiro C (2002) How plants cope with water stress in the field: photosynthesis and growth. Ann Bot-London 89:907–916CrossRefGoogle Scholar
  8. Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560PubMedCrossRefGoogle Scholar
  9. Downton WJS, Loveys BR, Grant WJR (1990) Salinity effects on the stomatal behavior of grapevine. New Phytol 116:499–503CrossRefGoogle Scholar
  10. Ehrenfeld JG (1990) Dynamics and processes of barrier island vegetation. Rev Aquat Sci 2:437–480Google Scholar
  11. Filella I, Llusià J, Piñol J, Peñuelas J (1998) Leaf gas exchange and fluorescence of Phillyrea latifolia, Pistacia lentiscus and Quercus ilex saplings in severe drought and high temperature conditions. Environ Exp Bot 39:213–220CrossRefGoogle Scholar
  12. Filella I, Porcar-Castell A, Munné-Bosch S, Bäck J, Garbulsky MF, Peñuelas J (2009) PRI assessment of long-term changes in carotenoids/chlorophyll ratio and short-term changes in de-epoxidation state of the xanthophyll cycle. Int J Remote Sens 30:4443–4455CrossRefGoogle Scholar
  13. Gamon JA, Peñuelas J, Field CB (1992) A narrow-waveband spectral index that tracks diurnal changes in photosynthetic efficiency. Remote Sens Environ 41:35–44CrossRefGoogle Scholar
  14. Gamon JA, Serrano L, Surfus JS (1997) The photochemical reflectance index: an optical indicator of photosynthetic radiation use efficiency across species, functional types, and nutrient levels. Oecologia 112:492–501CrossRefGoogle Scholar
  15. 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. Remote Sens Environ 115:281–297CrossRefGoogle Scholar
  16. Garrity SR, Eitel JUH, Vierling LA (2010) Disentangling the relationships between plant pigments and the photochemical reflectance index reveals a new approach for remote estimation of carotenoid content. Remote Sens Environ 115:628–635CrossRefGoogle Scholar
  17. Geissler N, Hussin S, Koyro HW (2009) Elevated atmospheric CO2 concentration ameliorates effects of NaCl salinity on photosynthesis and leaf structure of Aster tripolium L. J Exp Bot 60:137–151PubMedCrossRefGoogle Scholar
  18. Gitelson AA, Chivkunova OB, Merzlyak MM (2009) Nondestructive estimation of anthocyanins and chlorophylls in anthocyanic leaves. Am J Bot 96:1861–1868PubMedCrossRefGoogle Scholar
  19. Hassine AB, Ghanem ME, Bouzid S, Lutts S (2008) An inland and a coastal population of the Mediterranean xero-halophyte species Atriplex halimus L. differ in their ability to accumulate proline and glycinebetaine in response to salinity and water stress. J Exp Bot 59:1315–1326PubMedCrossRefGoogle Scholar
  20. Huynh H, Feldt LS (1976) Estimation of the box correction for degrees of freedom for sample data in randomized block and split plot designs. J Educ Stat 1:69–82CrossRefGoogle Scholar
  21. Krause G, Vernotte C, Briantais J (1982) Photoinduced quenching of chlorophyll fluorescence in intact chloroplasts and algae. Resolution into two components. Biochim Biophys Acta 679:116–124CrossRefGoogle Scholar
  22. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. In: Colowick P, Kaplan NO (eds) Methods in enzymology, vol 148. Academic, San Diego, pp 350–382Google Scholar
  23. Lu C, Qiu N, Wang B, Zhang J (2003) Salinity treatment shows no effects on photosystem II photochemistry, but increases the resistance of photosystem II to heat stress in halophyte Suaeda salsa. J Exp Bot 54:851–860PubMedCrossRefGoogle Scholar
  24. Mateos-Naranjo E, Redondo-Gómez S, Álavarez R, Cambrollé J, Gandullo J, Figueroa ME (2010) Synergic effect of salinity and CO2 enrichment on growth and photosynthetic responses of the invasive cordgrass Spartina densiflora. J Exp Bot 61:1643–1654PubMedCrossRefGoogle Scholar
  25. Morales F, Abadía A, Abadía J (2006) Photoinhibition and photoprotection under nutrient deficiencies, drought and salinity. In: Demmig-Adams B, Adams WW, Mattoo AK (eds) Photoprotection, photoinhibition, gene regulation, and environment. Springer, DordrechtGoogle Scholar
  26. Nakaji T, Oguma H, Fujinuma Y (2006) Seasonal changes in the relationship between photochemical reflectance index and photosynthetic light use efficiency of Japanese larch needles. Int J Remote Sens 27:493–509CrossRefGoogle Scholar
  27. Naumann JC, Young DR, Anderson JE (2008) Leaf fluorescence, reflectance, and physiological response of freshwater and saltwater flooding in the evergreen shrub, Myrica cerifera. Environ Exp Bot 63:402–409CrossRefGoogle Scholar
  28. Naumann JC, Young DR, Anderson JE (2009) Spatial variations in salinity stress across a coastal landscape using vegetation indices derived from hyperspectral imagery. Plant Ecol 202:285–297CrossRefGoogle Scholar
  29. Nichol CJ, Rascher U, Matsubara S, Osmond B (2006) Assessing photosynthetic efficiency in an experimental mangrove canopy using remote sensing and chlorophyll fluorescence. Trees 20:9–15CrossRefGoogle Scholar
  30. Ogaya R, Peñuelas J (2003) Comparative field study of Quercus ilex and Phillyrea latifolia: photosynthetic response to experimental drought conditions. Environ Exp Bot 50:137–148CrossRefGoogle Scholar
  31. Oosting HJ, Billings WD (1942) Factors effecting vegetational zonation on coastal dunes. Ecology 23:131–141CrossRefGoogle Scholar
  32. 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 156:1–11PubMedCrossRefGoogle Scholar
  33. Peñuelas J, Filella I, Llusià J, Siscart D, Piñol J (1998) Compartive field study of spring and summer leaf gas exhange and photobiology of the meidterranean trees Quercus ilex and Phillyrea latifolia. J Environ Exp Bot 319:229–238CrossRefGoogle Scholar
  34. Ranjbarfordoei A, Samson R, van Damme P (2006) Chlorophyll fluorescence performance of sweet almond [Prunus dulcis (Miller) D. Webb] in response to salinity stress induced by NaCl. Photosynthetica 44:513–522CrossRefGoogle Scholar
  35. Redondo-Gomez S, Wharmby C, Castillo JM, Mateos-Naranjo E, Luque C, de Cires A, Luque T, Davy AJ, Figueroa ME (2006) Growth and photosynthetic responses to salinity in an extreme halophyte, Sarcocornia fruticosa. Physiol Plantarum 128:116–124CrossRefGoogle Scholar
  36. 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 Sens Environ 81:337–354CrossRefGoogle Scholar
  37. Stalter R, Odum WE (1993) Maritime communities. In: Martin WM, Boyce SG, Echternacht C (eds) Biodiversity of the Southeastern United States: Lowland Terrestrial Communities. John Wiley and Sons, New YorkGoogle Scholar
  38. Stępień P, Kłobus G (2006) Water relations and photosynthesis in Cucumis sativus L. leaves under salt stress. Biol Plantarum 50:610–616CrossRefGoogle Scholar
  39. Stylinski CD, Gamon JA, Oechel WC (2002) Seasonal patterns of reflectance indices, carotenoid pigments and photosynthesis of evergreen chaparral species. Oecologia 131:366–374CrossRefGoogle Scholar
  40. Suárez L, Zarco-Tejada PJ, Sepulcre-Cantó G, Pérez-Priego O, Miller JR, Jiménez-Muñoz JC, Sobrino J (2008) Assessing canopy PRI for water stress detection with diurnal airborne imagery. Remote Sens Environ 112:560–575CrossRefGoogle Scholar
  41. Tolliver KS, Martin DW, Young DR (1997) Freshwater and saltwater flooding response for woody species common to barrier island swales. Wetlands 17:10–18CrossRefGoogle Scholar
  42. Tuffers A, Naidoo G, von Willert DJ (2001) Low salinities adversely affect photosynthetic performance of the mangrove, Avicennia marina. Wetl Ecol Manag 9:225–232CrossRefGoogle Scholar
  43. Ustin SL, Gitelson AA, Jacquemond S, Schaepman M, Asner GP, Gamon JA, Zarco-Tejada P (2009) Retrieval of foliar information about plant pigment systems from high resolution spectroscopy. Remote Sens Environ 113:S67–S77CrossRefGoogle Scholar
  44. von Ende CN (1993) Repeated-measures analysis: growth and other time-dependent measures. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Chapman & Hall, New York, pp 113–137Google Scholar
  45. Yeo AR (1998) Molecular biology of salt tolerance in the context of whole-plant physiology. J Exp Bot 49:915–929CrossRefGoogle Scholar
  46. Young DR, Erickson DL, Semones SW (1994) Salinity and the small-scale distribution of three barrier island shrubs. Can J Botany 72:1365–1372CrossRefGoogle Scholar
  47. Zar JH (1999) Biostatistical analysis. Prentice Hall, Inc, Upper Saddle RiverGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. (outside the USA) 2011

Authors and Affiliations

  • Julie C Zinnert
    • 1
    • 2
  • Jean D Nelson
    • 1
    • 2
  • Ava M Hoffman
    • 2
  1. 1.US Army ERDC, Fluorescence Spectroscopy LabAlexandriaUSA
  2. 2.Department of BiologyVirginia Commonwealth UniversityRichmondUSA

Personalised recommendations