Skip to main content
SpringerLink
Log in

Early detection of bean infection by Pseudomonas syringae in asymptomatic leaf areas using chlorophyll fluorescence imaging

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Chlorophyll fluorescence imaging has been used to analyse the response elicited in Phaseolus vulgaris after inoculation with Pseudomonas syringae pv. phaseolicola 1448A (compatible interaction) and P. syringae pv. tomato DC3000 (incompatible interaction). With the aim of modulating timing of symptom development, different cell densities were used to inoculate bean plants and the population dynamics of both bacterial strains was followed within the leaf tissue. Fluorescence quenching analysis was carried out and images of the different chlorophyll fluorescence parameters were obtained for infected as well as control plants at different timepoints post-infection. Among the different parameters analysed, we observed that non-photochemical quenching maximised the differences between the compatible and the incompatible interaction before the appearance of visual symptom. A decrease in non-photochemical quenching, evident in both infiltrated and non-infiltrated leaf areas, was observed in P. syringae pv. phaseolicola-infected plants as compared with corresponding values from controls and P. syringae pv. tomato-infected plants. No photoinhibitory damage was detected, as the maximum photosystem II quantum yield remained stable during the infection period analysed.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

Chl-F:

Chlorophyll fluorescence

Chl-FI:

Chlorophyll fluorescence imaging

cfu:

Colony forming units

dpi:

Days post-inoculation

ΦPSII :

Effective PSII quantum yield

ΦPSII5 :

Effective PSII quantum yield at 5 s during the fluorescence induction kinetics

FM′:

Maximum fluorescence in the light-adapted state

FM :

Maximum fluorescence in the dark-adapted state

F0 :

Initial fluorescence

Ft :

Actual fluorescence any time during illumination with actinic light

HR:

Hypersensitive response

IF:

Infiltrated area

LB:

Luria Bertani medium

NIF:

Non-infiltrated area

NPQ:

Non-photochemical quenching

NPQ20 :

Non-photochemical quenching at 20 s during the fluorescence induction kinetics

Pph:

Pseudomonas syringae pv. phaseolicola

Pst:

Pseudomonas syringae pv. tomato

PSII:

Photosystem II

R :

Resistance genes

RCI:

Real-colour images

References

  • Balachandran S, Hurry VM, Kelley SE, Osmond CB, Robinson SA, Rohozinski J, Seaton GGR, Sims DA (1997) Concepts of plant biotic stress. Some insights into the stress physiology of virus-infected plants, from the perspective of photosynthesis. Physiol Plant 100:203–213

    Article  CAS  Google Scholar 

  • Berger S, Papadopoulos M, Schreiber U, Kaiser W, Roitsch T (2004) Complex regulation of gene expression, photosynthesis and sugar levels by pathogen infection in tomato. Physiol Plant 122:419–428

    Article  CAS  Google Scholar 

  • Berger S, Benediktyová Z, Matouš K, Bonfig K, Mueller MJ, Nedbal L, Roitsch T (2007) Visualization of dynamics of plant–pathogen interaction by novel combination of chlorophyll fluorescence imaging and statistical analysis: differential effects of virulent an avirulent strains of P. syringae and of oxylipins on A. thaliana. J Exp Bot 58:797–806

    Google Scholar 

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

    Article  Google Scholar 

  • Bonfig KB, Schreiber U, Gabler A, Roitsch T, Berger S (2006) Infection with virulent and avirulent P. syringae strains differentially effects photosynthesis and sink metabolism in Arabidopsis leaves. Planta 225:1–12

    Article  PubMed  CAS  Google Scholar 

  • Chaerle L, Pineda M, Romero-Aranda R, Van Der Straeten D, Barón M (2006) Robotized thermal and chlorophyll-fluorescence imaging of pepper mild mottle virus infection in Nicotiana benthamiana. Plant Cell Physiol 47:1323–1336

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Cuppels DA (1986) Generation and characterization of Tn5 insertion mutations in Pseudomonas syringae pv. tomato. Appl Environ Microb 51:323–327

    CAS  Google Scholar 

  • Fillingham AJ, Wood J, Bevan JR, Crute IR, Mansfield JW, Taylor JD, Vivian A (1992) Avirulence genes from Pseudomonas syringae pathovars phaseolicola and pisi confer specificity towards both host and non-host species. Physiol Mol Plant Pathol 40:1–15

    Article  Google Scholar 

  • Fouts DE, Badel JL, Ramos AR, Rapp RA, Collmer A (2003) A Pseudomonas syringae pv. tomato DC3000 Hrp (Type III Secretion) deletion mutant expressing the Hrp system of bean pathogen P. syringae pv. syringae 61 retains normal host specificity for tomato. Mol Plant-Microbe Interact 16:43–52

    Article  PubMed  CAS  Google Scholar 

  • Hirano SS, Upper CD (2000) Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae-a pathogen, ice nucleus and epiphyte. Microbiol Mol Biol Rev 64:624–653

    Article  PubMed  CAS  Google Scholar 

  • Ireland CR, Long SP, Baker NR (1984) The relationship between carbon dioxide fixation and chlorophyll a fluorescence during induction of photosynthesis in maize leaves at different temperatures and carbon dioxide concentrations. Planta 160:550–558

    Article  CAS  Google Scholar 

  • Jones AME, Thomas V, Bennett MH, Mansfield JW, Grant M (2006) Modifications to the Arabidopsis defense proteome occur prior to significant transcriptional change in response to inoculation with Pseudomonas syringae 1[W][OA]. Plant Physiol 142:1603–1620

    Article  PubMed  CAS  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  PubMed  CAS  Google Scholar 

  • Karpinski S, Gabrys H, Mateo A, Karpinska B, Mullineaux PM (2003) Light perception in plant disease defence signalling. Curr Opin Plant Biol 6:390–396

    Article  PubMed  CAS  Google Scholar 

  • Lohaus G, Heldt HW, Osmond CB (2000) Infection with phloem limited abutilon mosaic virus causes localized carbohydrate accumulation in leaves of Abutilon striatum: relationships to symptom development and effects on chlorophyll fluorescence quenching during photosynthetic induction. Plant Biol 2:161–167

    Article  CAS  Google Scholar 

  • Matouš K, Benediktyova Z, Berger S, Roitsch T, Nedbal L (2006) Case study of combinatorial imaging: what protocol and what chlorophyll fluorescence image to use when visualizing infection of Arabidopsis thaliana by Pseudomonas syringae? Photosynth Res 90:243–253

    Article  PubMed  Google Scholar 

  • Meyer S, Saccardt AK, Rizza F, Genty B (2001) Inhibition of photosynthesis by Colletotrichum lindemuthianum in bean determined by chlorophyll fluorescence imaging. Plant Cell Environ 24:947–955

    Article  CAS  Google Scholar 

  • Nedbal L, Soukupová J, Kaftan D, Whitmarsh J, Trtílek M (2000) Kinetic imaging of chlorophyll fluorescence using modulated light. Photosynth Res 66:3–12

    Article  PubMed  CAS  Google Scholar 

  • Pérez-Bueno ML, Rahoutei J, Sajnani C, García-Luque I, Barón M (2004) Proteomic analysis of the oxygen-evolving complex of photosystem II under biotic stress: studies on Nicotiana benthamiana infected with tobamoviruses. Proteomics 4:418–425

    Article  PubMed  Google Scholar 

  • Pérez-Bueno ML, Ciscato M, vandeVen M, García-Luque I, Valcke R, Barón M (2006) Imaging viral infection: studies on Nicotiana benthamiana plants infected with the pepper mild mottle tobamovirus. Photosynth Res 90:111–123

    Article  PubMed  Google Scholar 

  • Rahoutei J, García-Luque I, Barón M (2000) Inhibition of photosynthesis by viral infection: effect on PSII structure and function. Physiol Plant 110:286–292

    Article  CAS  Google Scholar 

  • Repka V (2002) Chlorophyll-deficient mutant in oak (Quercus petrea L.) displays an accelerated hypersensitive-like cell death and enhanced resistance to powdery mildew disease. Photosynthetica 40:183–193

    Article  CAS  Google Scholar 

  • Sajnani C, Zurita J L, Roncel M, Ortega J M, Barón M, Ducruet JM (2007) Changes in photosynthetic metabolism induced by tobamovirus infection in Nicotiana benthamiana studied in vivo by chlorophyll thermoluminescence. New Phytol 175:120–130

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Soukupová J, Smatanová S, Nedbal L, Jegorov A (2003) Plant response to destruxins visualized by imaging of chlorophyll fluorescence. Physiol Plant 118:1–8

    Article  Google Scholar 

  • Staskawicz BJ, Ausubel FM, Baker BJ, Ellis JG, Jones JDG (1995) Molecular genetics of plant disease resistance. Science 268:661–667

    Article  PubMed  CAS  Google Scholar 

  • Tao Y, Xie Z, Chen W, Glazebrook J, Chang HS, Han B, Zhu T, Zou G, Katagiri F (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15:317–330

    Article  PubMed  CAS  Google Scholar 

  • Truman W, Torres de Zabala M, Grant M (2006) Type III effectors orchestrate a complex interplay between transcriptional networks to modify basal defence responses during pathogenesis and resistance. Plant J 46:14–33

    Article  PubMed  CAS  Google Scholar 

  • Whalen MC, Innes RW, Bent AF, Staskawicz BJ (1991) Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. Plant Cell 3:49–59

    Article  PubMed  CAS  Google Scholar 

  • Wilhelmová N, Procházková D, Sindelárová M, Sindelar L (2005) Photosynthesis in leaves of Nicotiana tabacum L. infected with tobacco mosaic virus. Photosynthetica 43:597–602

    Article  Google Scholar 

  • Zou J, Rodriguez-Zas S, Aldea M, Li M, Zhu J, Gonzalez D, Vodkin L, DeLucia E, Clough S (2005) Expression profiling soybean response to Pseudomonas syringae reveals new defence-related genes and rapid HR-specific downregulation of photosynthesis. Mol Plant Microbe Interact 18:1161–1174

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This project was supported by Spanish MEC grants AGL2002-02214 and BIO2004-04968-C02-02 to C.R. and M. B., respectively. The cooperation between the Spanish and the Czech groups was carried out in the frame of the Exchange Programme CSIC/Czech Academy of Sciences (projects 2003CZ0011 and 2004CZ0016). J. S. was supported by the Czech Ministry of Education, Sports and Youth (grant MSM6007665808) and the Czech Academy of Sciences (grant AVOZ60870520).

Author information

Authors and Affiliations

  1. Área de Genética, Facultad de Ciencias, Universidad de Málaga, 29071, Malaga, Spain

    Luis Rodríguez-Moreno, Alberto P. Macho, Carmen R. Beuzón & Cayo Ramos

  2. Department of Biochemistry, Molecular and Cell Biology of Plants, Estación Experimental del Zaidín, CSIC, 18008, Granada, Spain

    Mónica Pineda & Matilde Barón

  3. Institute of Systems Biology and Ecology, Academy of Sciences of Czech Republic, Zámek 136, Nove Hrady, 37333, Czech Republic

    Julia Soukupová

  4. Institute of Physical Biology, University of South Bohemia, Zámek 136, Nove Hrady, 37333, Czech Republic

    Julia Soukupová

Authors
  1. Luis Rodríguez-Moreno
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mónica Pineda
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Julia Soukupová
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alberto P. Macho
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Carmen R. Beuzón
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Matilde Barón
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Cayo Ramos
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Matilde Barón.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rodríguez-Moreno, L., Pineda, M., Soukupová, J. et al. Early detection of bean infection by Pseudomonas syringae in asymptomatic leaf areas using chlorophyll fluorescence imaging. Photosynth Res 96, 27–35 (2008). https://doi.org/10.1007/s11120-007-9278-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-007-9278-6

Keywords

Search

Navigation