Sensing drought- and salinity-imposed stresses on tomato leaves by means of fluorescence techniques

Abstract

In our study, we investigated whether multiple fluorescence indices may be used to sense physiological changes in tomato plants (Solanum lycopersicum L.) caused by salinity and water deficit as single or combined stresses. The fluorescence intensity in the blue (B), red (R) and far-red (FR) spectral regions and the pulse-amplitude-modulated (PAM) chlorophyll fluorescence, were recorded on a weekly basis in the scope of a long-term experiment. The results indicate the coefficient of photochemical quenching (qL), the B to FR fluorescence ratio and the logarithm of the FR fluorescence ratio after R and UV-light excitation as appropriate parameters to sense the response of plants to the imposed stress. The qL revealed the impact of water deficiency, whereas the two multispectral ratios revealed the influence of combined salinity and water shortage. Despite minor changes in the chlorophyll concentration, salinity and water deficit, when combined, had an additive impact on the chlorophyll fluorescence. Overall, the fluorescence signals of ‘Rio Grande’ were more affected by the induced stresses compared to ‘Harzfeuer’. The multiparametric fluorescence technique, confirming the trends obtained with the PAM-method, reveals promising perspectives for the ‘in situ’ evaluation of the physiological status of horticultural crops.

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Abbreviations

AOI:

Area of interest

B:

Blue fluorescence

BFRR_UV:

Blue-to-far-red fluorescence ratio

Chl:

Chlorophyll

ChlF:

Chlorophyll fluorescence

DM:

Dry mass

EC:

Electrical conductivity

FLAV:

Flavonol-Index

FM:

Fresh mass

Fm:

Maximum fluorescence

Fo:

Ground fluorescence

FR:

Far-red

G:

Green fluorescence

Harzfeuer:

Solanum lycopersicum L. F1 hybrid Harzfeuer

NPQ:

Non-photochemical quenching

PAM:

Pulse-amplitude-modulated

PSII:

Photosystem II

qL:

Coefficient of photochemical quenching

R:

Red

Rio Grande:

Solanum lycopersicum L. variety Rio Grande

ψπ :

Osmotic potential

References

  1. Baker NN (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113

    CAS  PubMed  Article  Google Scholar 

  2. Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55:1607–1621

    CAS  PubMed  Article  Google Scholar 

  3. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207

    CAS  Article  Google Scholar 

  4. Belkhodja R, Morales F, Abadía A, Gómez-Aparisi J, Abadía J (1994) Chlorophyll fluorescence as a possible tool for salinity tolerance screening in barley (Hordeum vulgare L). Plant Physiol 104:667–673

    CAS  PubMed Central  PubMed  Google Scholar 

  5. Bilger W, Veit M, Schreiber L, Schreiber U (1997) Measurement of leaf epidermal transmittance of UV radiation by chlorophyll fluorescence. Physiol Plant 101:754–763

    CAS  Article  Google Scholar 

  6. Boureima S, Oukarroum A, Diouf A, Cisse N, Van Damme P (2012) Screening for drought tolerance in mutant germplasm of sesame (Sesamum indicum) probing by chlorophyll a fluorescence. Environ Exp Bot 81:37–43

    CAS  Article  Google Scholar 

  7. Bürling K, Hunsche M, Noga G (2010) Quantum yield of non-regulated energy dissipation in PSII (Y(NO)) for early detection of leaf rust (Puccinia triticina) infection in susceptible and resistant wheat (Triticum aestivum L) cultivars. Precis Agric 11:703–716

    Article  Google Scholar 

  8. Bürling K, Cerovic ZG, Cornic G, Ducruet J-M, Noga G, Hunsche M (2013) Fluorescence-based sensing of drought-induced stress in the vegetative phase of four contrasting wheat genotypes. Environ Exp Bot 89:51–59

    Article  Google Scholar 

  9. Buschmann C (2007) Variability and application of the chlorophyll fluorescence emission ratio red/far-red of leaves. Photosynth Res 92:261–271

    CAS  PubMed  Article  Google Scholar 

  10. Buschmann C, Lichtenthaler HK (1998) Principles and characteristics of multi-colour fluorescence imaging of plants. J Plant Physiol 152:297–314

    CAS  Article  Google Scholar 

  11. Buschmann C, Langsdorf G, Lichtenthaler HK (2000) Imaging of the blue, green, and red fluorescence emission of plants: an overview. Photosynthetica 38:483–491

    CAS  Article  Google Scholar 

  12. Cayuela E, Pérez-Alfocea F, Caro M, Bolarín MC (1996) Priming of seeds with NaCl induces physiological changes in tomato plants grown under salt stress. Physiol Plant 96:231–236

    CAS  Article  Google Scholar 

  13. Cayuela E, Muñoz-Mayor A, Vicente-Agulló F, Moyano E, Garcia-Abellan JO, Estañ MT, Bolarín MC (2007) Drought pretreatment increases the salinity resistance of tomato plants. J Plant Nutr Soil Sci 170:479–484

    CAS  Article  Google Scholar 

  14. Cerovic ZG, Samson G, Morales F, Tremblay N, Moya I (1999) Ultraviolet-induced fluorescence for plant monitoring: present state and prospects. Agronomic 19:543–578

    Article  Google Scholar 

  15. Cerovic ZG, Moise N, Agati G, Latouche N, Ben Ghozlen N, Meyer S (2008) New portable optical sensors for the assessment of winegrape phenolic maturity based on berry fluorescence. J Food Compos Anal 21:650–654

    CAS  Article  Google Scholar 

  16. Cerovic ZG, Masdoumier G, Ben Ghozlen N, Latouche G (2012) A new optical leaf-clip meter for simultaneous non-destructive assessment of leaf chlorophyll and epidermal flavonoids. Physiol Plant 146:251–260

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  17. Chappelle EW, Wood FM, McMurtrey IIIJE, Newcomb WW (1984) Laser-induced fluorescence of green plants 1: a technique for the remote detection of plant stress and species differentiation. Appl Optics 23:134–138

    CAS  Article  Google Scholar 

  18. Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought—from genes to the whole plant. Funct Plant Biol 89:51–59

    Google Scholar 

  19. Chinnusamy V, Zhu J-K (2003) Plant salt tolerance. In: Hirt H, Shinozaki K (eds) Plant responses to abiotic stress. Springer, Berlin Heidelberg, pp 241–270

    Google Scholar 

  20. Claussen W (2005) Proline as a measure of stress in tomato plants. Plant Sci 168:241–248

    CAS  Article  Google Scholar 

  21. Di Ferdinando M, Brunetti C, Fini A, Tattini M (2012) Flavonoids as antioxidants in plants under abiotic stresses. In: Ahmad P, Prasad MNV (eds) Abiotic stress responses in plants: metabolism productivity and sustainability. Springer, New York, pp 159–179

    Google Scholar 

  22. El-Meleigy E-SA, Gabr MF, Mohamed FH, Ismail MA (2004) Responses of NaCl salinity of tomato cultivated and breeding lines differing in salt tolerance in callus cultures. Int J Agric Biol 6:19–26

    CAS  Google Scholar 

  23. Haupt-Herting S, Fock HP (2000) Exchange of oxygen and its role in energy dissipation during drought stress in tomato plants. Physiol Plant 110:489–495

    CAS  Article  Google Scholar 

  24. Hunsche M, Lankes C, Hoffstall H, Noga G (2010) Vegetative performance, leaf water potential, and partitioning of minerals and soluble sugars: traits for ranking the NaCl-tolerance of tomato genotypes? Plant Growth Regul 62:151–162

    CAS  Article  Google Scholar 

  25. Hura T, Grzesiak S, Hura K, Thiemt E, Tokarz K, Wędzony M (2007) Physiological and biochemical tools useful in drought-tolerance detection in genotypes of winter triticale: accumulation of ferulic acid correlates with drought tolerance. Ann-Bot-London 100:767–775

    CAS  Article  Google Scholar 

  26. Juan M, Rivero RM, Romero L, Ruiz JM (2005) Evaluation of some nutritional and biochemical indicators in selecting salt-resistant tomato cultivars. Environ Exp Bot 54:193–201

    CAS  Article  Google Scholar 

  27. Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218

    CAS  PubMed  Article  Google Scholar 

  28. Lang M, Lichtenthaler HK, Sowinska M, Heisel F, Miehé JA (1996) Fluorescence imaging of water and temperature stress in plant leaves. J Plant Physiol 148:613–621

    CAS  Article  Google Scholar 

  29. Leufen G, Noga G, Hunsche M (2013) Physiological response of sugar beet (Beta vulgaris) genotypes to a temporary water deficit, as evaluated with a multiparameter fluorescence sensor. Acta Physiol Plant 35:1763–1774

    CAS  Article  Google Scholar 

  30. Lichtenthaler HK (1996) Vegetation stress: an introduction to the stress concept in plants. Plant Physiol 148:4–14

    CAS  Article  Google Scholar 

  31. Lichtenthaler HK, Babani F (2000) Detection of photosynthetic activity and water stress by imaging the red chlorophyll fluorescence. Plant Physiol Biochem 38:889–895

    CAS  Article  Google Scholar 

  32. Lichtenthaler HK, Schweiger J (1998) Cell wall bound ferulic acid, the major substance of the blue-green fluorescence emission of plants. J Plant Physiol 152:272–282

    CAS  Article  Google Scholar 

  33. Lichtenthaler HK, Buschmann C, Rinderle U, Schmuck G (1986) Application of chlorophyll fluorescence in ecophysiology. Radiat Environ Biophys 25:297–308

    CAS  PubMed  Article  Google Scholar 

  34. Lichtenthaler HK, Subhash N, Wenzel O, Miehé JA (1997) Laser-induced imaging of blue/red and blue/far-red fluorescence ratios, F440/F690 and F440/F740, as a means of early stress detection in plants. Gisci Remote Sens 4:1799–1801

    Google Scholar 

  35. Lichtenthaler HK, Wenzel O, Buschmann C, Gitelson A (1998) Plant stress detection by reflectance and fluorescence. Ann NY Acad Sci 851:271–285

    Article  Google Scholar 

  36. Lichtenthaler HK, Buschmann C, Knapp M (2005) How to correctly determine the different chlorophyll fluorescence parameters and the chlorophyll fluorescence decrease ratio RFD of leaves with the PAM fluorometer. Photosynthetica 43:379–393

    CAS  Article  Google Scholar 

  37. Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158

    CAS  PubMed  Article  Google Scholar 

  38. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    CAS  PubMed  Article  Google Scholar 

  39. Morales F, Cerovic ZG, Moya I (1996) Time-resolved blue-green fluorescence of sugar beet (Beta vulgaris L) leaves. Spectroscopic evidence for the presence of ferulic acid as the main fluorophore of the epidermis. Biochim Biophys Acta 1273:251–262

    Article  Google Scholar 

  40. Morant-Manceau A, Pradier E, Tremblin G (2004) Osmotic adjustment, gas exchange and chlorophyll fluorescence of a hexaploid triticale and its parental species under salt stress. J Plant Physiol 161:25–33

    CAS  PubMed  Article  Google Scholar 

  41. Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching a response to excess light energy. Plant Physiol 125:1558–1566

    PubMed Central  PubMed  Article  Google Scholar 

  42. Müller V, Lankes C, Schmitz-Eiberger M, Noga G, Hunsche M (2013) Estimation of flavonoid and centelloside accumulation in leaves of Centella asiatica L. Urban by multiparametric fluorescence measurements. Environ Exp Bot 93:27–34

    Article  Google Scholar 

  43. Munné-Bosch S, Alegre L (2000) Changes in carotenoids, tocopherols and diterpenes during drought and recovery, and the biological significance of chlorophyll loss in Rosmarinus officinalis plants. Planta 210:925–931

    PubMed  Article  Google Scholar 

  44. Santos CV (2004) Regulation of chlorophyll biosynthesis and degradation by salt stress in sunflower leaves. Sci Hortic-Amsterdam 103:93–99

    CAS  Article  Google Scholar 

  45. Schmuck G, Moya I, Pedrini A, van der Linde D, Lichtenthaler HK, Stober F, Schindler C, Goulas Y (1992) Chlorophyll fluorescence lifetime determination of water stressed C3- and C4-plants. Radiat Environ Biophy 31:141–151

    CAS  Article  Google Scholar 

  46. Schreiber U (2004) Pulse-amplitude-modulation (PAM) fluorometry and saturation pulse method: an overview. In: Papageorgiu GC and Govindjee (eds) Chlorophyll a Fluorescence: a Signature of photosynthesis. Springer, Dordrecht, p 1–42

  47. Stoll A (1936) Zusammenhänge zwischen der Chemie des Chlorophylls und seiner Funktion in der Photosynthese. Naturwissenschaften 4:53–59

    Article  Google Scholar 

  48. Szigeti Z (2008) Physiological status of cultivated plants characterized by multi-wavelength fluorescence imaging. Acta Agron Hung 56:223–234

    CAS  Article  Google Scholar 

  49. Taiz L, Zeiger E (2007) Plant Physiology, 4th edn. Sinauer Associates Inc, Sunderland MA

    Google Scholar 

  50. Walter J, Nagby L, Hein R, Rascher U, Beierkuhnlein C, Willner E, Jentsch A (2011) Do plants remember drought? Hints towards a drought-memory in grasses. Environ Exp Bot 71:34–40

    Article  Google Scholar 

  51. Zribi L, Fatma G, Fatma R, Salwa R, Hassan N, Néjib RM (2009) Application of chlorophyll fluorescence for the diagnosis of salt stress in tomato “Solanum lycopersicum (variety Rio Grande)”. Sci Hortic-Amsterdam 120:367–372

    CAS  Article  Google Scholar 

  52. Zushi K, Matsuzoe N (2009) Seasonal and cultivar differences in salt-induced changes in antioxidant system in tomato. Sci Hortic-Amsterdam 120:181–187

    CAS  Article  Google Scholar 

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Acknowledgments

The authors are grateful to Libeth Schwager for her extensive support in the laboratory activities. The first author acknowledges the University of Bonn for providing Ph.D. scholarship support.

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Correspondence to Mauricio Hunsche.

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Kautz, B., Noga, G. & Hunsche, M. Sensing drought- and salinity-imposed stresses on tomato leaves by means of fluorescence techniques. Plant Growth Regul 73, 279–288 (2014). https://doi.org/10.1007/s10725-014-9888-x

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Keywords

  • Abiotic stresses
  • Chlorophyll fluorescence
  • Laser-induced fluorescence
  • NaCl
  • Solanum lycopersicum
  • Water deficiency