Skip to main content

Advertisement

SpringerLink
Log in

Virus-induced changes in photosynthetic parameters and peroxidase isoenzyme contents in tomato (Solanum lycopersicum L.) plants

  • Published:
Photosynthetica

Abstract

Tomato samples were collected from the field of Absheron peninsula in Azerbaijan in order to evaluate the incidence of main Tobamoviruses. According to results of serological and molecular tests, Tomato mosaic virus (ToMV), Tobacco mosaic virus (TMV), and Pepper mild mottle virus (PMMoV) were detected as single and mixed infections (TMV + PMMoV; ToMV + PMMoV) in various tomato samples. It was found that Tobamovirus infection caused an increase in the content of malondialdehyde, alterations in the activities of peroxidase enzymes and quantitative and qualitative changes in their molecular isoforms. A comparison of thylakoid membrane polypeptides from virus-infected leaves indicated a decrease in the content of the thylakoid membrane polypeptides with molecular masses of 123, 55, 47, 33, 28–24, 17, and 15 kD. PSII efficiency and the content of chlorophylls (a and b) were significantly lower in the virus-infected leaves.

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

Similar content being viewed by others

Abbreviations

APO:

ascorbate peroxidase

BPO:

benzidine-type peroxidase

Chl:

chlorophyll

CMV:

Cucumber mosaic virus

F0 :

initial values of chlorophyll fluorescence

Fm :

maximal values of chlorophyll fluorescence

Fv/Fm :

maximal quantum efficiency of PSII

GPO:

guaiacol-type peroxidase

LPO:

lipid peroxidation

PMMoV:

Pepper mild mottle virus

ROS:

reactive oxygen species

TMV:

Tobacco mosaic virus

ToMV:

Tomato mosaic virus

TSWV:

Tomato spotted wilt virus

References

  • Aliyev J., Suleymanov S., Guseinova I. et al.: Effect of specific translation inhibitors on polypeptide composition and spectral characteristics of wheat thylakoid membrane.–Biochemistry 57: 679–686, 1992.

    Google Scholar 

  • Bertamini M., Grando M.S., Muthuchelian K. et al.: Effect of phytoplasmal infection on PSII efficiency and thylakoid membrane protein changes in field grown apple (Malus Pumila) leaves.–Physiol. Mol. Plant Pathol. 61: 349–356, 2003.

    Article  CAS  Google Scholar 

  • Blancard D., Laterrot H., Marchoux G. et al.: A Colour Handbook–Tomato Diseases: Identification, Biology and Control. Pp. 688. Manson Publishing Limited, London 2012.

    Book  Google Scholar 

  • Bradford M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein using the principles of dyebinding.–Anal. Biochem. 72: 143–147, 1976.

    Article  Google Scholar 

  • Broadbent L.: Epidemiology and control of tomato mosaic virus.–Annu. Rev. Phytopathol. 14: 75–96, 1976.

    Article  Google Scholar 

  • Christov I., Stefanov D., Velinov T. et al.: The symptomless leaf infection with grapevine leafroll associated virus 3 in grown in vitro plants as a simple model system for investigation of viral effects on photosynthesis.–Plant Physiol. 164: 1124–1133, 2005.

    Article  CAS  Google Scholar 

  • Clarke S.F., Guy P.L., Burritt D.J. et al.: Changes in the activities of antioxidant enzymes in response to virus infection and hormone treatment.–Plant Physiol. 114: 157–164, 2002.

    Article  CAS  Google Scholar 

  • Cuypers A., Vangronsveld J., Ciijsters H.: Peroxidases in roots and primary leaves of Pharsalus vulgaris copper and zinc phytotoxicity: a comparison.–Plant Physiol. 159: 869–876, 2002.

    Article  CAS  Google Scholar 

  • Da Costa M., Huang B.: Changes in antioxidant enzyme activities and lipid peroxidation for bent grass species in response to drought stress.–J. Am. Soc. Hortic. Sci. 132: 319–326, 2007.

    Google Scholar 

  • Davis B.: Disc electrophoresis. I. Method and application to human serum proteins.–Ann. NY Acad. Sci. 121: 404–427, 1964.

    Article  PubMed  CAS  Google Scholar 

  • De Gara L., De Pinto M.C., Tommasi F.: The antioxidant systems vis-à-vis reactive oxygen species during plant–pathogen interaction.–Plant Physiol. Bioch. 41: 863–870, 2003.

    Article  CAS  Google Scholar 

  • Díaz-Vivancos P., Clemente-Moreno M.J., Rubio M. et al.: Alteration in the chloroplast metabolism leads to ROS accumulation in pea plants in response to plum pox virus.–J. Exp. Bot. 59: 2147–2160, 2008.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Díaz-Vivancos P., Rubio M., Mesonero V. et al.: The apoplastic antioxidant system in Prunus: response to plum pox virus.–J. Exp. Bot. 57: 3813–3824, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Gechev T., Gadjiev I., van Breusegem E. et al.: Hydrogen peroxide protects tobacco from oxidative stress by inducing a set of antioxidant enzymes.–Cell Mol. Life Sci. 59: 708–714, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Gullner G., Künstler A., Király L. et al.: Up-regulated expression of lipoxygenase and divinyl ether synthase genes in pepper leaves inoculated with Tobamoviruses.–Physiol. Mol. Plant Pathol. 74: 387–393, 2010.

    Article  CAS  Google Scholar 

  • Heath RL., Packer L.: Photoperoxidation in isolated chloroplast. I. Kinetics and stoichiometry of fatty acid peroxidation.–Arch. Physiol. Biochem. 125: 189–198, 1968.

    Article  CAS  Google Scholar 

  • Helepciuca F.E., Mitoia M.E., Manole-Paunescua A. et al.: Induction of plant antioxidant system by interaction with beneficial and/or pathogenic microorganisms.–Roman. Biotech. Lett. 19: 9366–9375, 2014.

    Google Scholar 

  • Hernández J.A., Díaz-Vivancos P., Rubio M. et al.: Long-term PPV infection produces an oxidative stress in a susceptible apricot cultivar but not in a resistant cultivar.–Physiol. Plantarum 126: 140–152, 2006.

    Article  CAS  Google Scholar 

  • Huseynova I.M. Sultanova N.F., Aliyev J.A.: Histochemical visualization of ROS and antioxidant response to viral infections of vegetable crops grown in Azerbaijan.–Plant Physiol. Bioch. 81: 26–35, 2014.

    Article  CAS  Google Scholar 

  • Huseynova I.M., Aliyeva D.R., Mammadov A.Ch. et al.: Hydrogen peroxide generation and antioxidant enzyme activities in the leaves and roots of wheat cultivars subjected to long-term soil drought stress.–Photosynth. Res. 125: 279–289, 2015.

    Article  PubMed  CAS  Google Scholar 

  • Klimov V.V., Allakhverdiev S.I., Shuvalov V.A. et al.: Effect of extraction and re-addition of manganese on light reactions of Photosystem II preparations.–FEBS Lett. 148: 307–312, 1982.

    Article  PubMed  CAS  Google Scholar 

  • Kumar G., Knowles N.: Changes in lipid peroxidation and lipolytic and free-radical scavenging enzyme during aging and sprouting of potato (Solanum tuberosum L.) seed-tubers.–Plant Physiol. 102: 115–124, 1993.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Laemmli U.K.: Cleavage of structural proteins during the assembly of the head of bacteriophage T4.–Nature 227: 680–685, 1970.

    Article  PubMed  CAS  Google Scholar 

  • Lucas J.A.: Plant Pathology and Plant Pathogens, 3rd ed. Pp. 151. Blackwell Science, Oxford 1998.

    Google Scholar 

  • Mahalingam R., Shah N., Scrymgeour A. et al.: Temporal evolution of the Arabidopsis oxidative stress response.–Plant Mol. Biol. 57: 709–730, 2005.

    Article  PubMed  CAS  Google Scholar 

  • McKinney G.: Absorption of light by chlorophyll solutions.–Biol. Chem. 140: 315–322, 1941.

    Google Scholar 

  • Mittler R., Zilinskas B.A.: Detection of ascorbate peroxidase activity in native gels by inhibition of the ascorbate-dependent reduction of nitroblue tetrazolium.–Anal. Biochem. 212: 540–546, 1993.

    Article  PubMed  CAS  Google Scholar 

  • Mydlarz L.D., Harvell C.D.: Peroxidase activity and inducibility in the see fan coral exposed to a fungal pathogen.–Comp. Biochem. Phys. A 146: 54–62, 2007.

    Article  CAS  Google Scholar 

  • Nakano Y., Asada K.: Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts.–Plant Cell. Physiol. 22: 867–880, 1981.

    CAS  Google Scholar 

  • Nath K., Jajoo A., Sharma R. et al.: Towards a critical understanding of the photosystem II repair mechanism and its regulation during stress conditions.–FEBS Lett. 587: 3372–3381, 2013.

    Article  PubMed  CAS  Google Scholar 

  • Oliveira J.T.A., Barreto A.L.H., Vasconcelos I.M. et al.: Role of antioxidant enzymes, hydrogen peroxide and PR proteins in the compatible and incompatible interactions of cowpea (Vigna unguiculata) genotypes with the fungus colletotrichum gloeosporioides.–J. Plant Physiol. Pathol. 2: 3, 2014.

    Google Scholar 

  • Onda Y.: Oxidative protein-folding systems in plant cells.–Int. J. Cell Biol. 2013: 44–59, 2013.

    Article  CAS  Google Scholar 

  • Pandey H.C., Baig M.J., Chandra A. et al.: Drought stress induced changes in lipid peroxidation and antioxidant system in genus Avena.–J. Environ. Biol. 31: 435–440, 2010.

    PubMed  CAS  Google Scholar 

  • Pérez-Bueno M.L., Ciscato M., VandeVen M. et al.: Imaging viral infection. Studies on Nicotiana benthamiana plants infected with the Pepper mild mottle tobamovirus.–Photosynth. Res. 90: 11–24, 2006.

    Google Scholar 

  • Pineda M., Sajnani C., Barón M.: Changes induced by the pepper mild mottle tobamovirus on the chloroplast proteome of Nicotiana benthamiana.–Photosynth. Res. 103: 31–45, 2010.

    Article  PubMed  CAS  Google Scholar 

  • Radotic K., Ducic T., Mutavdžić D.: Changes in peroxidase activity and isoenzymes in spruce needles after exposure to different concentrations of cadmium.–Environ. Exp. Bot. 44: 105–113, 2000.

    Article  PubMed  CAS  Google Scholar 

  • Radwan D.E.M., Fayez K.A., Mahmoud S.Y. et al.: Physiological and metabolic changes of Cucurbita pepo leaves in response to Zucchini yellow mosaic virus (ZYMV) infection and salicylic acid treatments.–Plant Physiol. Bioch. 45: 480–489, 2007.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Rao G.S., Rao Reddy N.N., Surekha C.: Induction of plant systemic resistance in legumes Cajanus cajan, Vigna radiata, Vigna mingo against plant pathogens Fusarium oxysporum and Alternaria altermata–a Trichoderma viride mediated reprogramming of plant defense mechanism.–Int. J. Recent Sci. Res. 6: 4270–4280, 2015.

    Google Scholar 

  • Riedle-Bauer M.: Role of reactive oxygen species and antioxidant enzymes in systemic virus infections of plants.–J. Phytopathol. 148: 297–302, 2000.

    Article  CAS  Google Scholar 

  • Roca M., Minguez-Mosquera M.I.: Involvement of chlorophyllase in chlorophyll metabolism in olive varieties with high and low chlorophyll content.–Physiol. Plantarum 117: 459–466, 2003.

    Article  CAS  Google Scholar 

  • Rys M., Juhász C., Surówka E. et al.: Comparison of a compatible and an incompatible pepper-tobamovirus interaction by biochemical and non-invasive techniques: chlorophyll a fluorescence, isothermal calorimetry and FTRaman spectroscopy.–Plant Physiol. Bioch. 83: 267–278, 2014.

    Article  CAS  Google Scholar 

  • Sairam R.K., Deshmukh P.S., Shukla D.S.: Tolerance of drought and temperature stress in relation to increased antioxidant enzyme activity in wheat.–J. Agron. Crop Sci. 178: 171–178, 1997.

    Article  CAS  Google Scholar 

  • Sajnani C., Zurita J.Z., Roncel M. et al.: Changes in photosynthetic metabolism induced by tobamovirus infection in Nicotiana benthamiana studied in vivo by chlorophyll thermoluminescence.–New Phytol. 175: 120–130, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Sofy A.R., Mahfouze S.A., El-Enany M.A.M.: Isozyme markers for response of wild potato species to potato spindle tuber viroid Egyptian isolate.–World Appl. Sci. J. 27: 1010–1022, 2013.

    CAS  Google Scholar 

  • Takahashi S., Murata N.: How do environmental stresses accelerate photoinhibition?–Trend. Plant Sci. 13: 178–182, 2008.

    Article  CAS  Google Scholar 

  • Torres M.A., Jones J.D.G., Dangl J.L.: Reactive oxygen species signaling in response to pathogens.–Plant Physiol. 141: 373–378, 2006.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yi S., Yu S., Choi D.: Involvement of hydrogen peroxide in repression of catalase in TMV-infected resistant tobacco.–Mol. Cells 15: 364–369, 2003.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Molecular Biology and Biotechnology, Azerbaijan National Academy of Sciences, 2A Matbuat Avenue, Baku, AZ1073, Azerbaijan

    I. M. Huseynova, S. M. Mirzayeva, N. F. Sultanova, D. R. Aliyeva, N. Sh. Mustafayev & J. A. Aliyev

Authors
  1. I. M. Huseynova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. M. Mirzayeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. F. Sultanova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. D. R. Aliyeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. N. Sh. Mustafayev
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. J. A. Aliyev
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to I. M. Huseynova.

Additional information

Acknowledgment: This work was supported by the Science Development Foundation under the President of the Republic of Azerbaijan — Grant № EIF-2014-9(24)-KETPL-14/11/3 and Grant № EIF/GAM-3-2014-6(21)-24/15/3.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huseynova, I.M., Mirzayeva, S.M., Sultanova, N.F. et al. Virus-induced changes in photosynthetic parameters and peroxidase isoenzyme contents in tomato (Solanum lycopersicum L.) plants. Photosynthetica 56, 841–850 (2018). https://doi.org/10.1007/s11099-017-0737-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11099-017-0737-9

Additional key words

Search

Navigation