Skip to main content
SpringerLink
Log in

Nitric oxide modulates redox-mediated defense in potato challenged with Phytophthora infestans

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

In our experimental approach we investigated how post-infection nitric oxide-dependent signaling activated in potato leaves was related to defense against avirulent (avr) and virulent (vr) races of Phytophthora infestans. Results revealed that only in an incompatible response, early NO and superoxide (O2 •-) generation led to peroxynitrite (ONOO−) formation and together with hydrogen peroxide (H2O2) production synchronized with SOD activity induced effective defense against avr pathogen. Early oxidative and nitrosative bursts triggered an imbalance in redox homeostasis in inoculated tissue. To counteract that effect, a total antioxidative capacity, ascorbate and sulfhydryl (-SH) group compounds increased both synergistically and markedly, confirming the precise mechanism of redox re-adjustment in avr oomycete -potato interaction. Moreover, the NO-coded message was stored and converted into an enhanced total SNO pool and particular S-nitrosylation of targeted proteins. Overall, we identified 104 proteins typed for S-nitrosylation in mock- or P. infestans-inoculated potato leaves. The S-nitrosoproteome structure comprised a wide repertoire of proteins, i.e. defense- and redox-related. Finally, only in the incompatible interaction, NO-based signal was re-written on the rapid PR-1 gene and PR-2 protein activation and was tuned with a limitation of late blight disease symptoms.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abat, J. K., Mattoo, A. K., & Deswal, R. (2008). S-nitrosylated proteins of a medicinal CAM plant Kalanchoe pinnata- ribulose-1,5-bisphosphate carboxylase/oxygenase activity targeted for inhibition. FEBS Journal, 275, 2862–2872.

    Article  CAS  PubMed  Google Scholar 

  • Abeles, F., & Forrence, L. (1970). Temporal and Hormonal Control of β-1,3-Glucanase in Phaseolus vulgaris L. Plant Physiology, 45, 395–400.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Able, A. J., Guest, D. I., & Sutherland, M. W. (1998). Use of a new tetrazolium-based assay to study the production of superoxide radicals by tobacco cell cultures challenged with avirulent zoospores of Phytophthora parasitica var nicotianae. Plant Physiology, 117, 491–499.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Arasimowicz-Jelonek, M., & Floryszak-Wieczorek, J. (2011). Understanding the fate of peroxynitrite in plant cells–from physiology to pathophysiology. Phytochemistry, 72, 681–688.

    Article  CAS  PubMed  Google Scholar 

  • Arasimowicz-Jelonek, M., & Floryszak-Wieczorek, J. (2014). Nitric oxide: an effective weapon of the plant or the pathogen? Molecular Plant Patholology, 15(4), 406–416.

    Article  CAS  Google Scholar 

  • Arasimowicz-Jelonek, M., Floryszak-Wieczorek, J., Drzewiecka, K., Chmielowska-Bąk, J., Abramowski, D., & Izbiańska, K. (2014a). Aluminum induces cross-resistance of potato to Phytophthora infestans. Planta, 239, 679–694.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Arasimowicz-Jelonek, M., Floryszak-Wieczorek, J., Abramowski, D., Izbiańska, K. (2014b) Nitric oxide and reactive nitrogen species. In: nitric oxide in plants: metabolism and role ins tress physiology. Springer International Publishing, pp 165–184.

  • Astier, J., Rasul, S., Koen, E., Manzoor, H., Besson-Bard, A., Lamotte, O., Jeandroz, S., Durner, J., Lindermayr, C., & Wendehenne, D. (2011). S-nitrosylation: an emerging post-translational protein modification in plants. Plant Science: An International Journal of Experimental Plant Biology, 181, 527–533.

    Article  CAS  Google Scholar 

  • Barroso, J. B., Corpas, F. J., Carreras, A., Rodríguez-Serrano, M., Esteban, F. J., Fernández-Ocaňa, A., Chaki, M., Romero-Puertas, M. C., Valderrama, R., Sandalio, L. M., & del Río, L. A. (2006). Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under cadmium stress. Journal of Experimental Botany, 57, 1785–1793.

    Article  CAS  PubMed  Google Scholar 

  • Beauchamp, C., & Fridovich, I. (1971). Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry, 44, 276–287.

    Article  CAS  PubMed  Google Scholar 

  • Becana, M., Aparicio-Tejo, P., Irigoyen, J. J., & Sanchez-Diaz, M. (1986). Some enzymes of hydrogen peroxide metabolism in leaves and root nodules of Medicago sativa. Plant Physiology, 82, 1169–1171.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bennett, M., Mehta, M., & Grant, M. (2005). Biophoton imaging: a nondestructive method for assaying R gene responses. Molecular Plant-Microbe Interactions, 18, 95–102.

    Article  CAS  PubMed  Google Scholar 

  • Besson-Bard, A., Griveau, S., Bedioui, F., & Wendehenne, D. (2008). Real-time electrochemical detection of extracellular nitric oxide in tobacco cells exposed to cryptogein, an elicitor of defence responses. Journal of Experimental Botany, 59, 3407–3414.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chaki M., Lindermayr C. (2014) S-Nitrosoglutathione Reductase: Key Regulator of Plant Development and Stress Response. In: Khan MN, Mobin M, Mohammad F, Corpas FJ (eds) Nitric oxide in plants: metabolism and role in stress physiology. Springer International Publishing, pp 139–151.

  • Chaki, M., Fernández-Ocaňa, A. M., Valderrama, R., Carreras, A., Esteban, F. J., Luque, F., Gómez-Rodrígez, M. V., Begara-Morales, J. C., Corpas, F. J., & Barroso, J. B. (2009). Involvement of reactive nitrogen and oxygen species (RNS and ROS) in sunflower-mildew interaction. Plant and Cell Physiology, 50, 265–279.

    Article  CAS  PubMed  Google Scholar 

  • Chomcznski, P., & Sacchi, N. (1987). Single-step method of RNA isolation by acid quanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry, 162, 156.

    Google Scholar 

  • Corpas, F. J., Palma, J. M., Del Río, L. A., & Barroso, J. B. (2013). Protein tyrosine nitration in higher plants grown under natural and stress conditions. Frontiers in Plant Science, 4, 29.

    PubMed Central  PubMed  Google Scholar 

  • Delledonne, M., Xia, Y., Dixon, R. A., & Lamb, C. (1998). Nitric oxide functions as a signal in plant disease resistance. Nature, 394, 585–588.

    Article  CAS  PubMed  Google Scholar 

  • Delledonne, M., Zeier, J., Marocco, A., & Lamb, C. (2001). Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proceedings of the National Academy of Sciences, 98, 13454–13459.

    Article  CAS  Google Scholar 

  • Doke, N. (1983). Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiologial Plant Pathology, 23, 345–357.

    Article  CAS  Google Scholar 

  • Dubreuil-Maurizi, C., Vitecek, J., Marty, L., Branciard, L., Frettinger, P., Wendehenne, D., Meyer, A. J., Mauch, F., & Poinssot, B. (2011). Glutathione deficiency of the Arabidopsis mutant pad2-1 affects oxidative stress-related events, defense gene expression, and the hypersensitive response. Plant Physiology, 157, 2000–2012.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fares, A., Rossignol, M., & Peltier, J. B. (2011). Proteomics investigation of endogenous S-nitrosylation in Arabidopsis. Biochemical and Biophysical Research Communications, 416(3-4), 331–336.

    Article  CAS  PubMed  Google Scholar 

  • Fares, A., Nespoulous, C., Rossignol, M., & Peltier, J.-B. (2014). Simultaneous identification and quantification of nitrosylation sites by combination of biotin switch and ICAT labeling. Methods in Molecular Biology, 1072, 609–620.

    Article  CAS  PubMed  Google Scholar 

  • Feechan, A., Kwon, E., Yun, B.-W., Wang, Y., Pallas, J. A., & Loake, G. J. (2005). A central role for S-nitrosothiols in plant disease resistance. Proceedings of the National Academy of Sciences of the United States of America, 102(22), 8054–8059.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Floryszak-Wieczorek, J., Górski, W., & Arasimowczi-Jelonek, M. (2011). Functional imaging of biophoton responses of plants to fungal infection. European Journal of Plant Pathology, 130, 249–258.

    Article  Google Scholar 

  • Floryszak-Wieczorek, J., Arasimowicz-Jelonek, M., Milczarek, G., Janus, L., Pawlak-Sprada, S., Abramowski, D., Deckert, J., & Billert, H. (2012). Nitric oxide–mediated stress imprint in potato as an effect of exposure to a priming agent. Molecular Plant-Microbe Interactions, 25, 1469–1477.

    Article  CAS  PubMed  Google Scholar 

  • Floryszak-Wieczorek J., Arasimowicz-Jelonek M., Abramowski D. (2013) Redox-sensing responses in the potato-Phtophthora infestans system. Oxidative stress and cell death in plants: mechanisms and implications Florence, Italy, p. 53.

  • Groß, F., Durner, J., & Gaupels, F. (2013). Nitric oxide, antioxidants and prooxidants in plant defence responses. Frontiers in Plant Science, 4, 419.

    Article  PubMed Central  PubMed  Google Scholar 

  • Hoang, C. V., & Chapman, K. D. (2002). Biochemical and molecular inhibition of plastidial carbonic anhydrase reduces the incorporation of acetate into lipids in cotton embryos and tobacco cell suspensions and leaves. Plant Physiology, 128, 1417–1427.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Holzmeister, C., Gaupels, F., Geerlof, A., Sarioglu, H., Sattler, M., Durner, J., & Lindermayr, C. (2015). Differential inhibition of Arabidopsis superoxide dismutases by peroxynitrite-mediated tyrosine nitration. Journal of Experimental Botany, 66(3), 989–999.

    Article  PubMed Central  PubMed  Google Scholar 

  • Huang, J., Li, D., Diao, J., Hou, J., Yuan, J., & Zou, G. (2007). A novel fluorescent method for determination of peroxynitrite using folic acid as a probe. Talanta, 72, 1283–1287.

    Article  CAS  PubMed  Google Scholar 

  • James, W. C. (1971). An illustrated series of assessment keys for plant diseases, their preparation and usage. Canadian Plant Disease Survey, 51, 39–65.

    Google Scholar 

  • Janus, Ł., Milczarek, G., Arasimowicz-Jelonek, M., Abramowski, D., Billert, H., & Floryszak-Wieczorek, J. (2013). Normoergic NO-dependent changes, triggered by a SAR inducer in potato, create more potent defense responses to Phytophthora infestans. Plant Science, 211, 23–34.

    Article  CAS  PubMed  Google Scholar 

  • Kato, H., Takemoto, D., & Kawakita, K. (2013). Proteomic analysis of S-nitrosylated proteins in potato plant. Physiologia Plantarum, 148, 371–386.

    Article  CAS  PubMed  Google Scholar 

  • Kovacs, I., & Lindermayr, C. (2013). Nitric oxide-based protein modification: formation and site-specificity of protein S-nitrosylation. Frontiers in Plant Science, 4, 137.

    PubMed Central  PubMed  Google Scholar 

  • Lim, M. H., Xu, D., & Lippard, S. J. (2006). Visualization of nitric oxide in living cells by a copper-based fluorescent probe. Nature Chemical Biology, 2, 375–380.

    Article  CAS  PubMed  Google Scholar 

  • Lindermayr, C., Saalbach, G., & Durner, J. (2005). Proteomic Identification of S-Nitrosylated Proteins in Arabidopsis. Plant Physiology, 137, 921–930.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Malik, S. I., Hussain, A., Yun, B.-W., Spoel, S. H., & Loake, G. J. (2011). GSNOR-mediated de-nitrosylation in the plant defence response. Plant Science, 181, 540–544.

    Article  CAS  PubMed  Google Scholar 

  • Mukherjee, S. P., & Choudhuri, M. A. (1983). Implications of water stress-induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. Physiologia Plantarum, 58, 166–170.

    Article  CAS  Google Scholar 

  • Mur, L. A. J., Santosa, I. E., Laarhoven, L. J. J., Holton, N. J., Harren, F. J. M., & Smith, A. R. (2005). Laser photoacoustic detection allows in planta detection of nitric oxide in tobacco following challenge with avirulent and virulent Pseudomonas syringae Pathovars. Plant Physiology, 138, 1247–1258.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Noctor, G., Mhamdi, A., Chaouch, S., Han, Y., Neukermans, J., Marquez-Garcia, B., Queval, G., & Foyer, C. H. (2012). Glutathione in plants: an integrated overview. Plant, Cell & Environment, 35, 454–484.

    Article  CAS  Google Scholar 

  • Noirot, E., Der, C., Lherminier, J., Robert, F., Moricova, P., Kieu, K., Leborgne-Castel, N., Simon-Plas, F., & Bouhidel, K. (2014). Dynamic changes in the subcellular distribution of the tobacco ROS-producing enzyme RBOHD in response to the oomycete elicitor cryptogein. Journal of Experimental Botany, 65, 5011–5022.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Noritake, T., Kawakita, K., & Doke, N. (1996). Nitric oxide induces phytoalexin accumulation in potato tuber tissues. Plant Cell Physiology, 37, 113–116.

    Article  CAS  Google Scholar 

  • Ortega-Galisteo, A. P., Rodriguez-Serrano, M., Pazmino, D. M., Gupta, D. K., Sandalio, L. M., & Romero-Puertas, M. C. (2012). S-Nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: changes under abiotic stress. Journal of Experimental Botany, 63, 2089–2103.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Palmieri, M. C., Lindermayr, C., Bauwe, H., Steinhauser, C., & Durner, J. (2010). Regulation of plant glycine decarboxylase by s-nitrosylation and glutathionylation. Plant Physiology, 152(3), 1514–1528.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pauly, M., Andersen, L. N., Kauppinen, S., Kofod, L. V., York, W. S., Albersheim, P., & Darvill, A. (1999). A xyloglucan-specific endo-beta-1,4-glucanase from Aspergillus aculeatus: expression cloning in yeast, purification and characterization of the recombinant enzyme. Glycobiology, 9, 93–100.

    Article  CAS  PubMed  Google Scholar 

  • Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research, 29, 2004–2007.

    Article  Google Scholar 

  • Re, R., Pellegrini, N., Proteggente, A., Pannala, A., Yang, M., & Rice-Evans, C. (1999). Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biology & Medicine, 26, 1231–1237.

    Article  CAS  Google Scholar 

  • Rice-Evans, C. A., Diplock, A. T., & Symons, M. C. R. (1991). Techniques in free radical research. Laboratory Techniques in Biochemistry and Molecular Biology, 22, 143–147.

    Google Scholar 

  • Romero-Puertas, M. C., Laxa, M., Matte, A., Zaninotto, F., Finkemeier, I., Jones, A. M. E., Perazzolli, M., Vandelle, E., Dietz, K.-J., & Delledonne, M. (2007). S-Nitrosylation of peroxiredoxin ii e promotes peroxynitrite-mediated tyrosine nitration. The Plant Cell, 19, 4120–4130.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rustérucci, C., Espunya, M. C., Díaz, M., Chabannes, M., & Martínez, M. C. (2007). S-Nitrosoglutathione reductase affords protection against pathogens in Arabidopsis, both locally and systemically. Plant Physiology, 143, 1282–1292.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sehrawat A., Abat J.K., Deswal R. (2013) RuBisCO depletion improved proteome coverage of cold responsive S-nitrosylated targets in Brassica juncea. Frontiers in Plant Science, 4, doi:10.3389/fpls.2013.00342.

  • Spadaro, D., Yun, B.-W., Spoel, S. H., Chu, C., Wang, Y.-Q., & Loake, G. J. (2010). The redox switch: dynamic regulation of protein function by cysteine modifications. Physiologia Plantarum, 138, 360–371.

    Article  CAS  PubMed  Google Scholar 

  • Stefano, M., Vandelle, E., Polverari, A., Ferrarini, A., & Delledonne, M. (2006). Nitric oxide-mediated signaling functions during the plant hypersensitive response. In L. Lamattina & J. C. Polacco (Eds.), Nitric oxide in plant growth (pp. 207–222). Berlin, Heidelberg: Development and Stress Physiology. Springer Berlin Heidelberg.

    Chapter  Google Scholar 

  • Tada, Y., Spoel, S. H., Pajerowska-Mukhtar, K., Mou, Z., Song, J., Wang, C., Zuo, J., & Dong, X. (2008). Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins. Science, 321, 952–956.

    Article  CAS  PubMed  Google Scholar 

  • Tanou, G., Job, C., Rajjou, L., Arc, E., Belghazi, M., Diamantidis, G., Molassiotis, A., & Job, D. (2009). Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant Journal, 60(5), 795–804.

    Article  CAS  PubMed  Google Scholar 

  • Tanou, G., Job, C., Belghazi, M., Molassiotis, A., Diamantidis, G., & Job, D. (2010). Proteomic signatures uncover hydrogen peroxide and nitric oxide cross-talk signaling network in citrus plants. Journal of Proteome Research, 2010(11), 5994–6006.

    Article  CAS  Google Scholar 

  • Vanzo, E., Ghirardo, A., Merl-Pham, J., Lindermayr, C., Heller, W., Hauck, S. M., Durner, J., & Schnitzler, J.-P. (2014). S-Nitroso-proteome in poplar leaves in response to acute ozone stress. PLoS ONE, 9(9), e106886. doi:10.1371/journal.pone.0106886.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vleeshouwers, V. G. A. A., & Oliver, R. P. (2014). Effectors as tools in disease resistance breeding against biotrophic, hemibiotrophic, and necrotrophic plant pathogens. Molecular Plant-Microbe Interactions, 27, 196–206.

    Article  CAS  PubMed  Google Scholar 

  • Vleeshouwers, V. G., van Dooijeweert, W., Govers, F., Kamoun, S., & Colon, L. T. (2000). The hypersensitive response is assiociated with host and non-host resistance to Phytophthora infestans. Planta, 210, 853–864.

    Article  CAS  PubMed  Google Scholar 

  • Wang, X., El Hadrami, A., Adam, L. R., & Daayf, F. (2008a). Differential activation and suppression of potato defence responses by Phytophthora infestans isolates representing US-1 and US-8 genotypes. Plant Pathology, 57, 1026–1037.

    Article  CAS  Google Scholar 

  • Wang, Y.-Q., Feechan, A., Yun, B.-W., Shafiei, R., Hofmann, A., Taylor, P., Xue, P., Yang, F.-Q., Xie, Z.-S., Pallas, J. A., Chu, C.-C., & Loake, G. J. (2008b). S-Nitrosylation of AtSABP3 antagonizes the expression of plant immunity. Journal of Biological Chemistry, 284, 2131–2137.

    Article  CAS  PubMed  Google Scholar 

  • Wilson, U. E., Coffey M. D. (1980). Cytological evaluation of general resistance to Phytophthora infestans in potato foliage. Annals of Botany, 45, 81–90.

  • Xiong, Y., DeFraia, C., Williams, D., Zhang, X., & Mou, Z. (2009). Characterization of Arabidopsis 6-phosphogluconolactonase T-DNA insertion mutants reveals an essential role for the oxidative section of the plastidic pentose phosphate pathway in plant growth and development. Plant & Cell Physiology, 50, 1277–1291.

    Article  CAS  Google Scholar 

  • Ye, J., Coulouris, G., Zaretskaya, I., Cutcutache, I., Rozen, S., & Madden, T. L. (2012). Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics, 13, 134.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yu, M., Lamattina, L., Spoel, S. H., & Loake, G. J. (2014). Nitric oxide function in plant biology: a redox cue in deconvolution. New Phytologist, 202, 1142–1156.

    Article  CAS  PubMed  Google Scholar 

  • Yun, B.-W., Feechan, A., Yin, M., Saidi, N. B. B., Le Bihan, T., Yu, M., Moore, J. W., Kang, J.-G., Kwon, E., Spoel, S. H., Pallas, J. A., & Loake, G. J. (2011). S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature, 478, 264–268.

    Article  CAS  PubMed  Google Scholar 

  • Zhao, S., & Fernald, R. D. (2005). Comprehensive algorithm for quantitative real-time polymerase chain reaction. Journal of Computational Biology, 12, 1047–1064.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This study was funded from the National Science Centre (Preludium - grant number 2011/03/N/NZ9/00290). D. Abramowski would like to thank Dr. Christian Lindermayr, Institute of Biochemical Plant Pathology, Helmholtz Zentrum München, for advice in the biotin-switch assay.

Conflict of Interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Plant Physiology, Poznan University of Life Sciences, Wolynska 35, 60 637, Poznan, Poland

    Dariusz Abramowski & Jolanta Floryszak-Wieczorek

  2. Department of Plant Ecophysiology, Adam Mickiewicz University, Umultowska 89, 61 614, Poznan, Poland

    Magdalena Arasimowicz-Jelonek & Karolina Izbiańska

  3. Department of Experimental Anaesthesiology, Poznan University of Medical Sciences, Sw. Marii Magdaleny 14, 60 861, Poznan, Poland

    Hanna Billert

Authors
  1. Dariusz Abramowski
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Magdalena Arasimowicz-Jelonek
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Karolina Izbiańska
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hanna Billert
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jolanta Floryszak-Wieczorek
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dariusz Abramowski.

Appendixes

Appendixes

Fig. 5
figure 5

Late blight disease progress in potato leaves-excised discs inoculated with avr and vr P. infestans. Average area of P. infestans mycelium growth was 2.98 ± 0.17 % in avr P. infestans-treated potato; and 20.1 ± 1.6 % in vr P. infestans-treated potato. Values represent the average of data ± SD of six independent experiments with maintained randomization

Full size image
Fig. 6
figure 6

Identification of S-nitrosylation targets in potato leaves: a immunodetection of S-nitrosylated proteins with the indication of the bands subjected to densytometric analysis, b negative and positive controls in BST, c protein content visualization using Coomassie blue staining, d functional categorization of the 104 identified S-nitrosylated proteins in potato leaves

Full size image
Table 1 The list of S-nitrosylation targets in potato leaves subjected to P. infestans inoculation
Full size table

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abramowski, D., Arasimowicz-Jelonek, M., Izbiańska, K. et al. Nitric oxide modulates redox-mediated defense in potato challenged with Phytophthora infestans . Eur J Plant Pathol 143, 237–260 (2015). https://doi.org/10.1007/s10658-015-0677-9

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-015-0677-9

Keywords

Search

Navigation