Skip to main content
Log in

Laser-induced fluorescence spectroscopy for early disease detection in grapefruit plants

  • Paper
  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

Abstract

Biotic and abiotic stress both cause a considerable decrease in the chlorophyll content in plant leaves, which provides a means for the early diagnosis of diseases in plants. The emergence of diseases affects the fluorescence of phenolic compounds and chlorophyll, which have emissions located at 530, 686 and 735 nm. Herein, it was found that the intensity of the emission band of phenolic compounds at 530 nm increased and that of chlorophyll at 735 nm decreased with the onset of diseases. Statistical analysis through principal component analysis (PCA) and partial least squares regression (PLSR) was performed, which differentiated between apparently healthy leaf sites and diseased leaves, providing a basis for the detection of diseases in the early stages. The PLSR model was validated through the coefficient of determination (R2), standard error of prediction (SEP) and standard error of calibration (SEC) with the values of 0.99, 0.394 and 0.0.401, respectively, which authenticated the model. The prediction accuracy of the model was evaluated through root mean square error in prediction (RMSEP), with a value of 0.14, by predicting 22 unknown emission spectra of different leaf sites. Both the PCA and PLSR models produced similar results, proving that fluorescence spectroscopy is an excellent tool for early disease detection in plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. J. M. Alston, J. M. Beddow and P. G. Pardey, Agricultural Research, Productivity, and Food Prices in the Long Run, Science, 2009, 325, 1209–1210.

    Article  CAS  Google Scholar 

  2. H. C. J. Godfray, J. R. Beddington, I. R. Crute, L. Haddad, D. Lawrence, J. F. Muir, J. Pretty, S. Robinson, S. M. Thomas and C. Toulmin, Food Security: The Challenge of Feeding 9 Billion People, Science, 2010, 327, 812–818.

    Article  CAS  Google Scholar 

  3. R. Pedrós, I. Moya, Y. Goulas and S. Jacquemoud, Chlorophyll fluorescence emission spectrum inside a leaf, Photochem. Photobiol. Sci., 2008, 7, 498–502.

    Article  Google Scholar 

  4. K. Maxwell and G. N. Johnson, Chlorophyll fluorescence - a practical guide, J. Exp. Bot., 2000, 51, 659–668.

    Article  CAS  Google Scholar 

  5. B. Anderson, P. K. Buah-Bassuah and J. P. Tetteh, Using violet laser-induced chlorophyll fluorescence emission spectra for crop yield assessment of cowpea (Vigna unguiculata (L) Walp) varieties, Meas. Sci. Technol., 2004, 15, 1255–1265.

    Article  CAS  Google Scholar 

  6. M. Pérez-Patricio, J. L. Camas-Anzueto, A. Sanchez-Alegría, A. Aguilar-González, F. Gutiérrez-Miceli, E. Escobar-Gómez, Y. Voisin, C. Rios-Rojas and R. Grajales-Coutiño, Optical method for estimating the chlorophyll contents in plant leaves, Sensors, 2018, 18, 650.

    Article  Google Scholar 

  7. H. Wang, X. Qian, L. Zhang, S. Xu, H. Li, X. Xia, L. Dai, L. Xu, J. Yu and X. Liu, Detecting crop population growth using chlorophyll fluorescence imaging, Appl. Opt., 2017, 56, 9762–9769.

    Article  CAS  Google Scholar 

  8. L. Nedbal and J. Whitmarsh, Chlorophyll Fluorescence Imaging of Leaves and Fruits, in Chlorophyll a Fluorescence, Springer, 2004, pp. 389–407.

  9. A. Friedrichs, J. A. Busch, H. J. van der Woerd and O. Zielinski, SmartFluo: A method and affordable adapter to measure chlorophyll a fluorescence with smartphones, Sensors, 2017, 17, 1–14.

    Article  Google Scholar 

  10. S. Lenk, L. Chaerle, E. E. Pfündel, G. Langsdorf, D. Hagenbeek, H. K. Lichtenthaler, D. Van Der Straeten and C. Buschmann, Multispectral fluorescence and reflectance imaging at the leaf level and its possible applications, J. Exp. Bot., 2007, 58, 807–814.

    Article  CAS  Google Scholar 

  11. H. K. Lichtenthale and J. A. Miehe, Fluorescence imaging as a diagnostic tool for plant stress, Trends Plant Sci., 1997, 2, 316–320.

    Article  Google Scholar 

  12. H. Wang, X. Qian, L. Zhang, S. Xu, H. Li, X. Xia, L. Dai, L. Xu, J. Yu and X. Liu, A Method of High Throughput Monitoring Crop Physiology Using Chlorophyll Fluorescence and Multispectral Imaging, Front. Plant Sci., 2018, 9, 1–12.

    Article  Google Scholar 

  13. N. Tremblay, Z. Wang and Z. G. Cerovic, Sensing crop nitrogen status with fluorescence indicators. A review, Agron. Sustainable Dev., 2012, 32, 451–464.

    Article  CAS  Google Scholar 

  14. J. Yang, L. Du, W. Gong, S. Shi, J. Sun and B. Chen, Potential of vegetation indices combined with laser-induced fluorescence parameters for monitoring leaf nitrogen content in paddy rice, PLoS One, 2018, 13, 1–15.

    Google Scholar 

  15. J. Cubero, J. H. Graham and T. R. Gottwald, Quantitative PCR Method for Diagnosis of Citrus Bacterial Canker, Appl. Environ. Microbiol., 2001, 67, 2849–2852.

    Article  CAS  Google Scholar 

  16. J. D. Scholes and S. A. Rolfe, Chlorophyll fluorescence imaging as tool for understanding the impact of fungal diseases on plant performance: a phenomics perspective, Funct. Plant Biol., 2009, 36, 880.

    Article  Google Scholar 

  17. L. Chaerle, D. Hagenbeek, E. De Bruyne, R. Valcke and D. Van Der Straeten, Thermal and Chlorophyll-Fluorescence Imaging Distinguish Plant-Pathogen Interactions at an Early Stage, Plant Cell Physiol., 2004, 45, 887–896.

    Article  CAS  Google Scholar 

  18. F. M. V. Pereira, D. M. B. P. Milori, E. R. Pereira-Filho, A. L. Venâncio, M. de S. T. Russo, M. C. do B. Cardinali, P. K. Martins and J. Freitas-Astúa, Laser-induced fluorescence imaging method to monitor citrus greening disease, Comput. Electron. Agric., 2011, 79, 90–93.

    Article  Google Scholar 

  19. J. Belasque Jr., M. C. G. Gasparoto and L. G. Marcassa, Detection of mechanical and disease stresses in citrus plants by fluorescence spectroscopy, Appl. Opt., 2008, 47, 1922.

    Article  Google Scholar 

  20. E. C. Lins, J. Belasque and L. G. Marcassa, Detection of citrus canker in citrus plants using laser induced fluorescence spectroscopy, Precis. Agric., 2009, 10, 319–330.

    Article  Google Scholar 

  21. C. B. Wetterich, R. F. de O. Belasque, N. José and L. G. Marcassa, Detection of citrus canker and Huanglongbing using fluorescence imaging spectroscopy and support vector machine technique, Appl. Opt., 2016, 55, 400–407.

    Article  CAS  Google Scholar 

  22. P. F. Daley, Chlorophyll fluorescence analysis and imaging in plant stress and disease, Can. J. Plant Pathol., 1995, 17, 167–173.

    Article  Google Scholar 

  23. R. Hull and R. Hull, Assay, Detection, and Diagnosis of Plant Viruses, in Plant Virology, Elsevier, 2014, pp. 755–808.

  24. B. M. Atta, M. Saleem, H. Ali, H. M. I. Arshad and M. Ahmed, Chlorophyll as a biomarker for early disease diagnosis, Laser Phys., 2018, 28, 065607.

    Article  Google Scholar 

  25. M. D. Brooks and K. K. Niyogi, Use of a Pulse-Amplitude Modulated Chlorophyll Fluorometer to Study the Efficiency of Photosynthesis in Arabidopsis Plants, in Methods in molecular biology, Springer, 2011, vol. 775, pp. 299–310.

  26. U. Schreiber, Pulse-Amplitude-Modulation (PAM) Fluorometry and Saturation Pulse Method: An Overview, in Chlorophyll a Fluorescence, Springer, 2004, pp. 279–319.

  27. T. Dong, J. Shang, J. M. Chen, J. Liu, B. Qian, B. Ma, M. J. Morrison, C. Zhang, Y. Liu, Y. Shi, H. Pan and G. Zhou, Assessment of Portable Chlorophyll Meters for Measuring Crop Leaf Chlorophyll Concentration, Remote Sens., 2019, 11, 2706.

    Article  Google Scholar 

  28. Y. Goulas, Z. G. Cerovic, A. Cartelat and I. Moya, Dualex: A new instrument for field measurements of epidermal ultraviolet absorbance by chlorophyll fluorescence, Appl. Opt., 2004, 43, 4488–4496.

    Article  CAS  Google Scholar 

  29. F. M. Padilla, M. Gallardo, M. T. Peña-Fleitas, R. de Souza and R. B. Thompson, Proximal Optical Sensors for Nitrogen Management of Vegetable Crops: A Review, Sensors, 2018, 18, 2083.

    Article  Google Scholar 

  30. F. M. Padilla, R. de Souza, M. T. Peña-Fleitas, M. Gallardo, C. Giménez and R. B. Thompson, Different Responses of Various Chlorophyll Meters to Increasing Nitrogen Supply in Sweet Pepper, Front. Plant Sci., 2018, 9, 1752.

    Article  Google Scholar 

  31. Y. Li and M. Chen, Novel chlorophylls and new directions in photosynthesis research, Funct. Plant Biol., 2015, 42, 493–501.

    Article  Google Scholar 

  32. J. P. Palta, Leaf chlorophyll content, Remote Sens. Rev., 1990, 5, 207–213.

    Article  Google Scholar 

  33. A. V. Ruban, Nonphotochemical chlorophyll fluorescence quenching: Mechanism and effectiveness in protecting plants from photodamage, Plant Physiol., 2016, 170, 1903–1916.

    Article  CAS  Google Scholar 

  34. M. Lang, F. Stober and H. K. Lichtenthaler, Fluorescence emission spectra of plant leaves and plant constituents, Radiat. Environ. Biophys., 1991, 30, 333–347.

    Article  CAS  Google Scholar 

  35. J. M. Harnly, S. Bhagwat and L. Z. Lin, Profiling methods for the determination of phenolic compounds in foods and dietary supplements, Anal. Bioanal. Chem., 2007, 389, 47–61.

    Article  CAS  Google Scholar 

  36. A. A. Gitelson, C. Buschmann and H. K. Lichtenthaler, Leaf chlorophyll fluorescence corrected for re-absorption by means of absorption and reflectance measurements, J. Plant Physiol., 1998, 152, 283–296.

    Article  CAS  Google Scholar 

  37. A. A. Gitelson, C. Buschmann and H. K. Lichtenthaler, The Chlorophyll Fluorescence Ratio F735/F700 as an Accurate Measure of the Chlorophyll Content in Plants, Remote Sens. Environ., 1999, 69, 296–302.

    Article  Google Scholar 

  38. K. Yu, G. Leufen, M. Hunsche, G. Noga, X. Chen and G. Bareth, Investigation of Leaf Diseases and Estimation of Chlorophyll Concentration in Seven Barley Varieties Using Fluorescence and Hyperspectral Indices, Remote Sens., 2013, 6, 64–86.

    Article  Google Scholar 

  39. G. Agati, P. Mazzinghi, F. Fusi and I. Ambrosini, The F685/F730 Chlorophyll Fluorescence Ratio as a Tool in Plant Physiology: Response to Physiological and Environmental Factors, J. Plant Physiol., 1995, 145, 228–238.

    Article  CAS  Google Scholar 

  40. E. V. Thomas and D. M. Haaland, Comparison of multivariate calibration methods for quantitative spectral analysis, Anal. Chem., 1990, 62, 1091–1099.

    Article  CAS  Google Scholar 

  41. S. N. Jha and R. Garg, Non-destructive prediction of quality of intact apple using near infrared spectroscopy, J. Food Sci. Technol., 2010, 47, 207–213.

    Article  CAS  Google Scholar 

  42. S. L. Cantor, S. W. Hoag, C. D. Ellison, M. A. Khan and R. C. Lyon, NIR spectroscopy applications in the development of a compacted multiparticulate system for modified release, AAPS PharmSciTech, 2011, 12, 262–278.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. Saleem.

Additional information

Electronic supplementary information (ESI) available. See DOI: 10.1039/c9pp00368a

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Saleem, M., Atta, B.M., Ali, Z. et al. Laser-induced fluorescence spectroscopy for early disease detection in grapefruit plants. Photochem Photobiol Sci 19, 713–721 (2020). https://doi.org/10.1039/c9pp00368a

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/c9pp00368a

Navigation