European Journal of Plant Pathology

, Volume 142, Issue 3, pp 625–632 | Cite as

Metabolic responses of avocado plants to stress induced by Rosellinia necatrix analysed by fluorescence and thermal imaging

  • Espen Granum
  • María Luisa Pérez-BuenoEmail author
  • Claudia E. Calderón
  • Cayo Ramos
  • Antonio de Vicente
  • Francisco M. Cazorla
  • Matilde Barón


One of the most important soilborne diseases affecting avocado (Persea americana Mill.) crops is white root rot, caused by the fungus Rosellinia necatrix. In this study we investigated the metabolic responses elicited by white root rot in the aerial part of the plant with special focus on the potential applications of imaging technique (including chlorophyll fluorescence (Chl-F), blue-green fluorescence and thermography) in early detection of the disease on leaves. The results show that leaf metabolism was significantly affected by the infection only when symptoms started to appear, which was probably related to the loss of root functionality. However, changes in some Chl-F parameters provided early indications of stress even prior to the development of symptoms. We suggest that the combinatorial analysis of several Chl-F parameters could be used as a method for early detection of stress related to white root rot, and might prove useful as a general indicator of biotic and abiotic stress in avocado plants.


Rosellinia necatrix White root rot Avocado Fluorescence imaging Thermal imaging Plant stress 



This work was supported by grants from CICE-Junta de Andalucía (Proyectos de Excelencia P08-CVI-03475, P10-AGR-5797 and P12-AGR-0370), Plan Nacional de I + D + I del Ministerio de Ciencia e Innovación, Spain (AGL2011-30354C0201) cofinanced by FEDER, EU and RECUPERA 2020/20134R060 (Ministerio de Economía y Competitividad-CSIC, Feder funds). E. Granum was recipient of a JAE-Doc contract funded by CSIC, Spain. C. E. Calderón was supported by a grant from FPI, Ministerio de Ciencia e Innovación, Spain.

Compliance with Ethical Standards

The Authors declare that the present manuscript complies with the Ethical Rules of good scientific practice applicable for the European Journal of Plant Pathology.

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

10658_2015_640_Fig1_ESM.gif (68 kb)
Suppl. Fig 1

Average values of Chl-F parameters FM/F0 (a), F’M/F’0 (b), F’V/F’M (c) and F’V/F’0 (d) in leaves of R. necatrix-infected avocado plants (R) and non-infected control plants (C) throughout the infection; means ± sd, n = 5. (GIF 68 kb)

10658_2015_640_MOESM1_ESM.tif (270 kb)
High resolution image (TIFF 270 kb)


  1. Bilger, W., Johnsen, T., & Schreiber, U. (2001). UV-excited chlorophyll fluorescence as a tool for the assessment of UV-protection by the epidermis of plants. Journal of Experimental Botany, 52, 2007–2014.CrossRefPubMedGoogle Scholar
  2. Buschmann, C., & Lichtenthaler, H. K. (1998). Principles and characteristics of multi-colour fluorescence imaging of plants. Journal of Plant Physiology, 152, 297–314.CrossRefGoogle Scholar
  3. Calderón, C. E., Pérez-García, A., de Vicente, A., & Cazorla, F. M. (2013). The dar genes of Pseudomonas chlororaphis PCL1606 are crucial for biocontrol activity via production of the antifungal compound 2-hexyl, 5-propyl resorcinol. Molecular Plant-Microbe Interactions, 26, 554–565.CrossRefPubMedGoogle Scholar
  4. Cazorla, F. M., Duckett, S. B., Bergström, E. T., Noreen, S., Odijk, R., Lugtenberg, B. J. J., et al. (2006). Biocontrol of avocado Dematophora root rot by antagonistic Pseudomonas fluorescens PCL1606 correlates with the production of 2-hexyl 5-propyl resorcinol. Molecular Plant-Microbe Interactions, 19, 418–428.CrossRefPubMedGoogle Scholar
  5. Cerovic, Z. G., Samson, G., Morales, F., Tremblay, N., & Moya, I. (1999). Ultraviolet-induced fluorescence for plant monitoring: present state and prospects. Agronomie, 19, 543–578.CrossRefGoogle Scholar
  6. Chaerle, L., & Van der Straeten, D. (2000). Imaging techniques and the early detection of plant stress. Trends in Plant Science, 5, 495–501.CrossRefPubMedGoogle Scholar
  7. Chartzoulakis, K., Patakas, A., Kofidis, G., Bosabalidis, A., & Nastou, A. (2002). Water stress affects leaf anatomy, gas exchange, water relations and growth of two avocado cultivars. Scientia Horticulturae, 95, 39–50.CrossRefGoogle Scholar
  8. Freeman, S., Sztejnberg, A., & Chet, I. (1986). Evaluation of Trichoderma as a biocontrol agent for Rosellinia necatrix. Plant and Soil, 94, 163–170.CrossRefGoogle Scholar
  9. Glenn, D. M. (2012). Infrared and chlorophyll fluorescence imaging methods for stress evaluation. HortScience, 47, 697–698.Google Scholar
  10. Gorbe, E., & Calatayud, A. (2012). Applications of chlorophyll fluorescence imaging technique in horticultural research: a review. Scientia Horticulturae, 138, 24–35.CrossRefGoogle Scholar
  11. Gutiérrez-Barranquero, J. A., Pliego, C., Bonilla, N., Calderón, C. E., Pérez-García, A., de Vicente, A., et al. (2012). Sclerotization as a long-term preservation method for Rosellinia necatrix strains. Mycoscience, 53, 460–465.CrossRefGoogle Scholar
  12. Kanadani, G., Date, H., & Nasu, H. (1998). Effect of fluazinam soil-drench on white root rot of grapevine. Japanese Journal of Phytopathology, 64, 139–141.CrossRefGoogle Scholar
  13. Kondo, H., Kanematsu, S., & Suzuki, N. (2013). Viruses of the white root rot fungus, Rosellinia necatrix. In A. G. Said (Ed.), Advances in virus research (pp. 177–214). USA: Academic.Google Scholar
  14. López-Herrera, C. J., Pérez-Jiménez, R. M., Zea-Bonilla, T., Basallote-Ureba, M. J., & Melero-Vara, J. M. (1998). Soil solarization in established avocado trees for control of Dematophora necatrix. Plant Disease, 82, 1088–1092.CrossRefGoogle Scholar
  15. Mahlein, A. K., Oerke, E. C., Steiner, U., & Dehne, H. W. (2012). Recent advances in sensing plant diseases for precision crop protection. European Journal of Plant Pathology, 133, 197–209.CrossRefGoogle Scholar
  16. Pérez-Bueno, M. L., Pineda, M., Díaz-Casado, M. E., & Barón, M. (2014). Spatial and temporal dynamics of primary and secondary metabolism in Phaseolus vulgaris challenged by Pseudomonas syringae. Physiologia Plantarum, 153, 161–174.CrossRefPubMedGoogle Scholar
  17. Pérez-Jiménez, R. M. (2006). A review of the biology and pathogenicity of rosellinia necatrix – the cause of white root rot disease of fruit trees and other plants. Journal of Phytopathology, 154, 257–266.CrossRefGoogle Scholar
  18. Pliego, C., Cazorla, F. M., González-Sánchez, M. A., Pérez-Jiménez, R. M., de Vicente, A., & Ramos, C. (2007). Selection for biocontrol bacteria antagonistic toward Rosellinia necatrix by enrichment of competitive avocado root tip colonizers. Research in Microbiology, 158, 463–70.CrossRefPubMedGoogle Scholar
  19. Pliego, C., de Weert, S., Lamers, G., de Vicente, A., Bloemberg, G., Cazorla, F. M., et al. (2008). Two similar enhanced root-colonizing Pseudomonas strains differ largely in their colonization strategies of avocado roots and Rosellinia necatrix hyphae. Environmental Microbiology, 10, 3295–304.CrossRefPubMedGoogle Scholar
  20. Pliego, C., Kanematsu, S., Ruano-Rosa, D., de Vicente, A., López-Herrera, C., Cazorla, F. M., et al. (2009). GFP sheds light on the infection process of avocado roots by Rosellinia necatrix. Fungal Genetics and Biology, 46, 137–45.CrossRefPubMedGoogle Scholar
  21. Pliego, C., López-Herrera, C., Ramos, C., & Cazorla, F. M. (2012). Developing tools to unravel the biological secrets of Rosellinia necatrix, an emergent threat to woody crops. Molecular Plant Pathology, 13, 226–39.CrossRefPubMedGoogle Scholar
  22. Ploetz, R., & Schaffer, B. (1989). Effects of flooding and phytophthora root rot on net gas exchange and growth of avocado. Phytopathology, 79, 204–208.CrossRefGoogle Scholar
  23. Rolfe, S. A., & Scholes, J. D. (2010). Chlorophyll fluorescence imaging of plant-pathogen interactions. Protoplasma, 247, 163–75.CrossRefPubMedGoogle Scholar
  24. Ruano-Rosa, D., Cazorla, F. M., Bonilla, N., Martín-Pérez, R., Vicente, A., & López-Herrera, C. J. (2014). Biological control of avocado white root rot with combined applications of Trichoderma spp. and rhizobacteria. European Journal of Plant Pathology, 138, 751–762.CrossRefGoogle Scholar
  25. Sade, N., Gebremedhin, A., & Moshelion, M. (2012). Risk-taking plants. Plant Signaling & Behavior, 7, 767–770.CrossRefGoogle Scholar
  26. Sztejnberg, A., & Madar, Z. (1980). Host range of Dematophora necatrix, the cause of white root rot disease in fruit trees. Plant Disease, 64, 662–664.CrossRefGoogle Scholar
  27. ten Hoopen, G. M., & Krauss, U. (2006). Biology and control of Rosellinia bunodes, Rosellinia necatrix and Rosellinia pepo: A review. Crop Protection, 25, 89–107.CrossRefGoogle Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2015

Authors and Affiliations

  • Espen Granum
    • 1
  • María Luisa Pérez-Bueno
    • 1
    Email author
  • Claudia E. Calderón
    • 2
  • Cayo Ramos
    • 3
  • Antonio de Vicente
    • 2
  • Francisco M. Cazorla
    • 2
  • Matilde Barón
    • 1
  1. 1.Departamento de Bioquímica, Biología Celular y Molecular de PlantasEstación Experimental del Zaidín. Consejo Superior de Investigaciones CientíficasGranadaSpain
  2. 2.Departamento de Microbiología, Facultad de CienciasInstituto de Hortofruticultura Subtropical y Mediterránea La Mayora. Universidad de Málaga, Consejo Superior de Investigaciones CientíficasMálagaSpain
  3. 3.Área de Genética, Facultad de CienciasInstituto de Hortofruticultura Subtropical y Mediterránea La Mayora. Universidad de Málaga, Consejo Superior de Investigaciones CientíficasMálagaSpain

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