Skip to main content
Log in

Monitoring cashew seedlings during interactions with the fungus Lasiodiplodia theobromae using chlorophyll fluorescence imaging

  • Original Papers
  • Published:
Photosynthetica

Abstract

The chlorophyll (Chl) fluorescence imaging technique was applied to cashew seedlings inoculated with the fungus Lasiodiplodia theobromae to assess any disturbances in the photosynthetic apparatus of the plants before the onset of visual symptoms. Two-month-old cashew plants were inoculated with mycelium of L. theobromae isolate Lt19 or Lt32. Dark-adapted and light-acclimated whole plants or previously labelled, single, mature leaf from each plant were evaluated weekly for Chl fluorescence parameters. From 21 to 28 days, inoculation with both isolates resulted in the significantly lower maximal photochemical quantum yield of PSII (Fv/Fm) than those for control samples, decreasing from values of 0.78 to 0.62. In contrast, the time response of the measured fluorescence transient curve from dark-acclimated plants increased in both whole plants and single mature leaves in inoculated plants compared with controls. The Fv/Fm images clearly exhibited photosynthetic perturbations 14 days after inoculation before any visual symptoms appeared. Additionally, decays in the effective quantum yield of PSII photochemistry and photochemical quenching coefficient were also observed over time. However, nonphotochemical quenching increased during the evaluation period. We conclude that Fv/Fm images are the effective way of detecting early metabolic perturbations in the photosynthetic apparatus of cashew seedlings caused by gummosis in both whole plants and single leaves and could be potentially employed in larger-scale screening systems.

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

Abbreviations

Chl:

chlorophyll

F0 :

minimal Chl fluorescence of dark-acclimated plants

F0′:

minimum fluorescence during light exposure treatment

Fm :

maximal Chl fluorescence of dark-acclimated plants

Fv/Fm :

maximal photochemical quantum yield of PSII

Fm′:

maximal fluorescence during light treatment

Fv :

variable fluorescence

LED:

light-emitting diode

NPQ:

nonphotochemical fluorescence quenching

QA :

quinone A

qP :

coefficient of photochemical fluorescence quenching

ΦPSII :

effective quantum yield of PSII photochemistry

τTR :

time response of the measured fluorescence transient curve from dark-acclimated plants

References

  • Baker, N.R.: Chlorophyll Fluorescence: A probe of photosynthesis in vivo. — Annu. Rev. Plant Biol. 59: 89–113, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Bezerra, M.A., Cardoso, J.E., Santos, A.A. et al.: [Effect of gummosis in the photosynthesis of the precocious dwarf cashew.] — Bol. Pesq. Desenvol. Emb. Agroind. Trop. 8: 1–12, 2003. [In Portuguese]

    Google Scholar 

  • Bilger, W., Björkman, O. 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: 173–185, 1990.

    Article  CAS  PubMed  Google Scholar 

  • Björkman, O., Demmig, B.: Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. — Planta 170: 489–504, 1987.

    Article  PubMed  Google Scholar 

  • Blaikie, S.J.; Chacko, E.K.: Sap flow, leaf gas exchange and chlorophyll fluorescence of container-grown cashew (Anacardium occidentale L.) trees subjected to repeated cycles of soil drying. — Aust. J. Exp. Agri. 38: 305–311, 1998.

    Article  Google Scholar 

  • Cardoso, J.E., Bezerra, M.A., Viana, F.M.P. et al.: [Endophyte occurrence of Lasiodiplodia theobromae in cashew tissues and its transmission by vegetative propagules.] — Summa Phytopathol. 35: 262–266, 2009. [In Portuguese]

    Article  Google Scholar 

  • Cardoso, J.E., Cavalcanti, J.J.V., Cysne, A.Q. et al.: [Effect of cashew clone used as rootstocks and scions on gummosis incidence in cashew plants.] — Rev. Bras. Frutic. 32: 847–854, 2010. [In Portuguese]

    Article  Google Scholar 

  • Cavalcanti Junior, A.T., Correa, D., Bueno, D.: [Propagation.] — In: Barros, L.M. (ed.): [Cashew production: technical aspects.] Pp. 43–48. Emb. Agroind. Trop., Fortaleza 2002. [In Portuguese]

    Google Scholar 

  • Chaerle, L., Hagenbeek, D., De Bruyne, E. et al.: Thermal and chlorophyll-fluorescence imaging distinguish plant-pathogen interactions at an early stage. — Plant Cell Physiol. 45: 887–896, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Chaerle, L., Leinonen, I., Jones, H.G., Van der Straeten, D.: Monitoring and screening plant populations with combined thermal and chlorophyll fluorescence imaging. — J. Exp.Bot. 58: 773–784, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Chou, H.M., Bundock, N., Rolfe, S.A., Scholes, J.D.: Infection of Arabidopsis thaliana leaves with Albugo candida (white blister rust) causes a reprogramming of host metabolism. — Mol. Plant Pathol. 1: 99–113, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Cséfalvay, L., Di Gaspero, G., Matouš, K., Bellin, D., Ruperti, B., Olejníčková, J.: Pre-symptomatic detection of Plasmopara viticola infection in grapevine leaves using chlorophyll fluorescence imaging. — Eur. J. Plant Pathol. 125: 291–302, 2009.

    Article  Google Scholar 

  • de Souza, R.P., Ribeiro, R.V., Machado, E.C. et al.: [Photosynthetic responses of young cashew plants to varying environmental conditions.] — Pesqui. Agropecu. Bras. 40: 735–744, 2005. [In Portuguese]

    Google Scholar 

  • FAOSTAT. Rome 2011. Available on http://faostat.fao.org/. Access on 17 Mai 2011.

  • Guidi, L., Mori, S., Degl’Innocenti, E., Pecchia, S.: Effects of ozone exposure or fungal pathogen on white lupin leaves as determined by imaging of chlorophyll a fluorescence. — Plant Physiol. Bioch. 45: 851–857, 2007.

    Article  CAS  Google Scholar 

  • Hoagland, D.R., Arnon, D.A.: The water-culture method of growing plants without soil. — Circ. Calif. Agr. Exp. Sta. 347: 1–39, 1950.

    Google Scholar 

  • IBGE. SIDRA, 2011. [Aggregate database.] Table 1613. Available on 〈http://www.sidra.ibge.gov.br/bda/tabela/listabl.asp?c=1613&z=t&o=11〉. Access on 9 Nov. 2011. [In Portuguese]

  • IBRAF, 2011. [Brazilian exportations of processed fruits 2009/2010.] Available on 〈www.ibraf.org.br/estatisticas/est_processadas.asp〉. Access on 9 Nov. 2011. [In Portuguese]

  • Lazar, D., Susila, P., Naus, J.: Early detection of plant stress from changes in distributions of chlorophyll a fluorescence parameters measured with fluorescence imaging. — J. Fluoresc. 16: 173–176, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Maxwell, K.; Johnson, G.N. Chlorophyll fluorescence — a practical guide. — J. Exp. Bot. 51: 659–668, 2000.

    Article  CAS  PubMed  Google Scholar 

  • McElrone, A.J., Hamilton, J.G., Krafnick, A.J. et al.: Combined effects of elevated CO2 and natural climatic variation on leaf spot diseases of redbud and sweetgum trees. — Environ. Pollut. 158: 108–114, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Muniz, C.R., Freire, F.C.O., Viana, F.M.P. et al.: Colonization of cashew plant by Lasiodiplodia theobromae: Microscopical features. — Micron 42: 419–428, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Muniz, C.R., Freire, F.C.O., Viana, F.M.P. et al.: Polyclonal antibody-based ELISA in combination with specific PCR amplification of internal transcribed spacer regions for the detection and quantitation of Lasiodiplodia theobromae, causal agent of gummosis in cashew nut plants. — Ann. Appl. Biol. 160: 217–224, 2012.

    Article  CAS  Google Scholar 

  • Nedbal, L., Whitmarsh, J.: Chlorophyll fluorescence imaging of leaves and fruits. — In: Papageorgiou, G.C., Govindjee (ed.): Chlorophyll Fluorescence: a Signature of Photosynthesis Pp. 279–319. Springer, Dordrecht 2004.

    Google Scholar 

  • Oxborough, K., Baker, N.R.: Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photo-chemical and non-photochemical components-calculation of qP and Fv′/Fm′ without measuring F0′. — Photosynth. Res. 54: 135–142, 1997.

    Article  CAS  Google Scholar 

  • Prokopová, J., Špundová, M., Sedlářová et al.: Photosynthetic responses of lettuce to downy mildew infection and cytokinin treatment. — Plant Physiol. Bioch. 48: 716–723, 2010.

    Article  Google Scholar 

  • Roháček, K.: Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. — Photosynthetica 40: 13–29, 2002.

    Article  Google Scholar 

  • Rolfe, S.A., Scholes, J.D.: Chlorophyll fluorescence imaging of plant-pathogen interactions. — Protoplasma 247: 163–175, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Scholes, J.D., Rolfe, S.A.: Photosynthesis in localised regions of oat leaves infected with crown rust (Puccinia coronata): quantitative imaging of chlorophyll fluorescence. — Planta 199: 573–582, 1996.

    Article  CAS  Google Scholar 

  • Scholes, J.D., Rolfe, S.A.: Chlorophyll fluorescence imaging as a tool for understanding the impact of fungal diseases on plant performance: a phenomics perspective. — Funct. Plant Biol. 36: 880–892, 2009.

    Article  Google Scholar 

  • Segarra, G., Casanova, E., Avilés, M., Trillas, I.: Trichoderma asperellum strain T34 controls fusarium wilt disease in tomato plants in soilless culture through competition for iron. — Microbial Ecol. 59: 141–149, 2010.

    Article  Google Scholar 

  • Taylor, A.; Hardy, G.E.S.; Wood, P.; Burgess, T.: Identification and pathogenicity of Botryosphaeriaceae species associated with grapevine decline in Western Australia. — Australas. Plant Path. 34: 187–195, 2005.

    Article  Google Scholar 

  • Úrbez-Torres, J.R.; Leavitt, G.M.; Guerrero, J.C. et al.: Identification and pathogenicity of Lasiodiplodia theobromae and Diplodia seriata, the causal agentes of bot canker disease of grapevines in Mexico. — Plant Dis. 92: 519–529, 2008.

    Article  Google Scholar 

  • van Kooten, O., Snell, J.F.H.: The use of chlorophyll fluorescence nomenclature in plant stress physiology. — Photosynth. Res. 25: 147–150, 1990.

    Article  PubMed  Google Scholar 

  • Wolpert, T.J., Dunkle, L.D., Ciuffetti, L.M.: Host-selective toxins and avirulence determinants: what’s in a name? — Annu. Rev. Phytopathol. 40: 251–285, 2002.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to C. R. Muniz.

Additional information

Acknowledgments: We would like to thank CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) for granting scholarships through the “Adding value to Brazilian Tropical fruits: MIPS (Multiple Imaging Plant Stress) and TRS (Time Resolved Spectroscopy) applications to assure uniform quality of papaya and mango” project, coordinated by Dr. H. Filgueiras and Dr. M. Teixeira de Souza Junior for his support through Embrapa LABEX Europe.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Muniz, C.R., Freire, F.C.O., Viana, F.M.P. et al. Monitoring cashew seedlings during interactions with the fungus Lasiodiplodia theobromae using chlorophyll fluorescence imaging. Photosynthetica 52, 529–537 (2014). https://doi.org/10.1007/s11099-014-0061-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11099-014-0061-6

Additional key words

Navigation