Skip to main content
Log in

Expressed Proteins of Herbaspirillum seropedicae in Maize (DKB240) Roots-Bacteria Interaction Revealed Using Proteomics

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Several molecular tools have been used to clarify the basis of plant-bacteria interaction; however, the mechanism behind the association is still unclear. In this study, we used a proteomic approach to investigate the root proteome of Zea mays (cv. DKB240) inoculated with Herbaspirillum seropedicae strain SmR1 grown in vitro and harvested 7 days after inoculation. Eighteen differentially accumulated proteins were observed in root samples, ten of which were identified by MALDI-TOF mass spectrometry peptide mass fingerprint. Among the identified proteins, we observed three proteins present exclusively in inoculated root samples and six upregulated proteins and one downregulated protein relative to control. Differentially expressed maize proteins were identified as hypothetical protein ZEAMMB73_483204, hypothetical protein ZEAMMB73_269466, and tubulin beta-7 chain. The following were identified as H. seropedicae proteins: peroxiredoxin protein, EF-Tu elongation factor protein, cation transport ATPase, NADPH:quinone oxidoreductase, dinitrogenase reductase, and type III secretion ATP synthase. Our results presented the first evidence of type III secretion ATP synthase expression during H. seropedicae-maize root interaction.

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.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Alberton, D., Mueller-Santos, M., Campos Brusamarello-Santos, L. C., Valdameri, G., Cordeiro, F. A., Yates, M. G., del Pedrosa, O. F., & de Souza, E. M. (2013). Comparative proteomics analysis of the rice roots colonized by Herbaspirillum seropedicae strain SmR1 reveals induction of the methionine recycling in the plant host. Journal of Proteome Research, 12, 4757–4768.

    Article  CAS  Google Scholar 

  2. Amaral, F., Bueno, J., Hermes, V., & Arisi, A. (2014). Gene expression analysis of maize seedlings (DKB240 variety) inoculated with plant growth promoting bacterium Herbaspirillum seropedicae. Symbiosis, 62, 41–50.

    Article  CAS  Google Scholar 

  3. Amiour, N., Imbaud, S., Clement, G., Agier, N., Zivy, M., Valot, B., Balliau, T., Armengaud, P., Quillere, I., Canas, R., Tercet-Laforgue, T., & Hirel, B. (2012). The use of metabolomics integrated with transcriptomic and proteomic studies for identifying key steps involved in the control of nitrogen metabolism in crops such as maize. Journal of Experimental Botany, 63, 5017–5033.

    Article  CAS  Google Scholar 

  4. Baldani, V. L. D., Baldani, J. I., Olivares, F., & Dobereiner, J. (1992). Identification and ecology of Herbaspirillum seropedicae and the closely related Pseudomonas rubrisubalbicans. Symbiosis, 13, 65–73.

    Google Scholar 

  5. Baldani, V. L. D., Baldani, J. I., & Dobereiner, J. (2000). Inoculation of rice plants with the endophytic diazotrophs Herbaspirillum seropedicae and Burkholderia spp. Biology and Fertility of Soils, 30, 485–491.

    Article  Google Scholar 

  6. Balsanelli, E., Serrato, R. V., de Baura, V. A., Sassaki, G., Yates, M. G., Rigo, L. U., Pedrosa, F. O., de Souza, E. M., & Monteiro, R. A. (2010). Herbaspirillum seropedicae rfbB and rfbC genes are required for maize colonization. Environmental Microbiology, 12, 2233–2244.

    CAS  Google Scholar 

  7. Botta, A. L., Santacecilia, A., Ercole, C., Cacchio, P., & Gallo, M. D. (2013). In vitro and in vivo inoculation of four endophytic bacteria on Lycopersicon esculentum. New Biotechnology, 30, 666–674.

    Article  CAS  Google Scholar 

  8. Canellas, L. P., Balmori, D. M., Medici, L. O., Aguiar, N. O., Campostrini, E., Rosa, R. C. C., Facanha, A. R., & Olivares, F. L. (2013). A combination of humic substances and Herbaspirillum seropedicae inoculation enhances the growth of maize (Zea mays L.). Plant and Soil, 366, 119–132.

    Article  CAS  Google Scholar 

  9. Chaves, D. F. S., Ferrer, P. P., de Souza, E. M., Gruz, L. M., Monteiro, R. A., & de Pedrosa, O. F. (2007). Two-dimensional proteome reference map of Herbaspirillum seropedicae proteins. Proteomics, 7, 3759–3763.

    Article  CAS  Google Scholar 

  10. Cheng, Z., McConkey, B. J., & Glick, B. R. (2010). Proteomic studies of plant-bacterial interactions. Soil Biology & Biochemistry, 42, 1673–1684.

    Article  CAS  Google Scholar 

  11. Chubatsu, L. S., Monteiro, R. A., de Souza, E. M., Schuler de Oliveira, M. A., Yates, M. G., Wassem, R., Bonatto, A. C., Huergo, L. F., Reynaud Steffens, M. B., Rigo, L. U., & del Pedrosa, O. F. (2012). Nitrogen fixation control in Herbaspirillum seropedicae. Plant and Soil, 356.

  12. Cordeiro, F. A., Tadra-Sfeir, M. Z., Huergo, L. F., de Pedrosa, O. F., Monteiro, R. A., & de Souza, E. M. (2013). Proteomic analysis of Herbaspirillum seropedicae cultivated in the presence of sugar cane extract. Journal of Proteome Research, 12, 1142–1150.

    Article  CAS  Google Scholar 

  13. Dinkova-Kostova, A. T., & Talalay, P. (2010). NAD(P)H:quinone acceptor oxidoreductase 1 (NQO1), a multifunctional antioxidant enzyme and exceptionally versatile cytoprotector. Archives of Biochemistry and Biophysics, 501, 116–123.

    Article  CAS  Google Scholar 

  14. dos Santos, M. F., Muniz de Padua, V. L., de Nogueira, M. E., Hemerly, A. S., & Domont, G. B. (2010). Proteome of Gluconacetobacter diazotrophicus co-cultivated with sugarcane plantlets. Journal of Proteomics, 73, 917–931.

    Article  Google Scholar 

  15. Egener, T., Hurek, T., & Reinhold-Hurek, B. (1999). Endophytic expression of nif genes of Azoarcus sp strain BH72 in rice roots. Molecular Plant-Microbe Interactions, 12, 813–819.

    Article  CAS  Google Scholar 

  16. Frendo, P., Matamoros, M. A., Alloing, G., & Becana, M. (2013). Thiol-based redox signaling in the nitrogen-fixing symbiosis. Frontiers in Plant Science, 4, 376.

    Article  Google Scholar 

  17. Furukawa, T., Inagaki, H., Takai, R., Hirai, H., & Che, F.-S. (2014). Two distinct EF-Tu epitopes induce immune responses in rice and Arabidopsis. Molecular Plant-Microbe Interactions, 27, 113–124.

    Article  CAS  Google Scholar 

  18. Hakeem, K. R., Chandna, R., Ahmad, A., Qureshi, M. I., & Iqbal, M. (2012). Proteomic analysis for low and high nitrogen-responsive proteins in the leaves of rice genotypes grown at three nitrogen levels. Applied Biochemistry and Biotechnology, 168, 834–850.

    Article  CAS  Google Scholar 

  19. He, S. Y., Nomura, K., & Whittam, T. S. (2004). Type III protein secretion mechanism in mammalian and plant pathogens. Biochimica Et Biophysica Acta-Molecular Cell Research, 1694, 181–206.

    Article  CAS  Google Scholar 

  20. Huergo, L. F., Noindorf, L., Gimenes, C., Lemgruber, R. S. P., Cordellini, D. F., Falarz, L. J., Cruz, L. M., Monteiro, R. A., Pedrosa, F. O., Chubatsu, L. S., Souza, E. M., & Steffens, M. B. R. (2010). Proteomic analysis of Herbaspirillum seropedicae reveals ammonium-induced AmtB-dependent membrane sequestration of P-II proteins. FEMS Microbiology Letters, 308, 40–47.

    Article  CAS  Google Scholar 

  21. Hungria, M., Campo, R. J., Souza, E. M., & Pedrosa, F. O. (2010). Inoculation with selected strains of Azospirillum brasilense and A. lipoferum improves yields of maize and wheat in Brazil. Plant and Soil, 331, 413–425.

    Article  CAS  Google Scholar 

  22. Jonak, J. (2007). Bacterial elongation factors EF-Tu, their mutants, chimeric forms, and domains: isolation and purification. Journal of Chromatography B-Analytical Technologies in the Biomedical and Life Sciences, 849, 141–153.

    Article  CAS  Google Scholar 

  23. Klassen, G., Pedrosa, F. O., Souza, E. M., Funayama, S., & Rigo, L. U. (1997). Effect of nitrogen compounds on nitrogenase activity in Herbaspirillum seropedicae SMR1. Canadian Journal of Microbiology, 43, 887–891.

    Article  CAS  Google Scholar 

  24. Kunze, G., Zipfel, C., Robatzek, S., Niehaus, K., Boller, T., & Felix, G. (2004). The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell, 16, 3496–3507.

    Article  CAS  Google Scholar 

  25. Lery, L. M. S., Hemerly, A. S., Nogueira, E. M., von Krueger, W. M. A., & Bisch, P. M. (2011). Quantitative proteomic analysis of the interaction between the endophytic plant-growth-promoting bacterium Gluconacetobacter diazotrophicus and sugarcane. Molecular Plant-Microbe Interactions, 24, 562–576.

    Article  CAS  Google Scholar 

  26. Mochida, K., & Shinozaki, K. (2011). Advances in omics and bioinformatics tools for systems analyses of plant functions. Plant and Cell Physiology, 52, 2017–2038.

    Article  CAS  Google Scholar 

  27. Monteiro, R. A., Balsanelli, E., Wassem, R., Marin, A. M., Brusamarello-Santos, L. C. C., Schmidt, M. A., Tadra-Sfeir, M. Z., Pankievicz, V. C. S., Cruz, L. M., Chubatsu, L. S., Pedrosa, F. O., & Souza, E. M. (2012). Herbaspirillum-plant interactions: microscopical, histological and molecular aspects. Plant and Soil, 356, 175–196.

    Article  CAS  Google Scholar 

  28. Olivares, F. L., Baldani, V. L. D., Reis, V. M., Baldani, J. I., & Dobereiner, J. (1996). Occurrence of the endophytic diazotrophs Herbaspirillum spp in roots, stems, and leaves, predominantly of Gramineae. Biology and Fertility of Soils, 21, 197–200.

    Article  Google Scholar 

  29. Park, H. Y., Seok, H. Y., Park, B. K., Kim, S. H., Goh, C. H., Lee, B., Lee, C. H., & Moon, Y. H. (2008). Overexpression of Arabidopsis ZEP enhances tolerance to osmotic stress. Biochemical and Biophysical Research Communications, 375, 80–85.

    Article  CAS  Google Scholar 

  30. Pedrosa, F. O., Monteiro, R. A., Wassem, R., Cruz, L. M., Ayub, R. A., Colauto, N. B., Fernandez, M. A., Fungaro, M. H. P., Grisard, E. C., Hungria, M., Madeira, H. M. F., Nodari, R. O., Osaku, C. A., Petzl-Erler, M. L., Terenzi, H., Vieira, L. G. E., Steffens, M. B. R., Weiss, V. A., Pereira, L. F. P., Almeida, M. I. M., Alves, L. R., Marin, A., Araujo, L. M., Balsanelli, E., Baura, V. A., Chubatsu, L. S., Faoro, H., Favetti, A., Friedermann, G., Glienke, C., Karp, S., Kava-Cordeiro, V., Raittz, R. T., Ramos, H. J. O., Ribeiro, E., Rigo, L. U., Rocha, S. N., Schwab, S., Silva, A. G., Souza, E. M., Tadra-Sfeir, M. Z., Torres, R. A., Dabul, A. N. G., Soares, M. A. M., Gasques, L. S., Gimenes, C. C. T., Valle, J. S., Ciferri, R. R., Correa, L. C., Murace, N. K., Pamphile, J. A., Patussi, E. V., Prioli, A. J., Prioli, S. M. A., Rocha, C., Arantes, O. M. N., Furlaneto, M. C., Godoy, L. P., Oliveira, C. E. C., Satori, D., Vilas-Boas, L. A., Watanabe, M. A. E., Dambros, B. P., Guerra, M. P., Mathioni, S. M., Santos, K. L., Steindel, M., Vernal, J., Barcellos, F. G., Campo, R. J., Chueire, L. M. O., Nicolas, M. F., Pereira-Ferrari, L., Silva, J. L. D., Gioppo, N. M. R., Margarido, V. P., Menck-Soares, M. A., Pinto, F. G. S., Simao, R. D. G., Takahashi, E. K., & Yates, M. G. (2011). Genome of Herbaspirillum seropedicae strain SmR1, a specialized diazotrophic endophyte of tropical grasses. Plos Genetics, 7, e1002064.

    Article  CAS  Google Scholar 

  31. Pereira, T.S., Amaral, F., Dall’Asta, P., Brod, F.B., Arisi, A, Real-Time P.C.R. Quantification of the Plant Growth Promoting Bacteria Herbaspirillum seropedicae Strain SmR1 in Maize Roots. Molecular Biotechnology, 1–11.

  32. Prinsi, B., Negri, A.S., Pesaresi, P., Cocucci, M., Espen, L. (2009) Evaluation of protein pattern changes in roots and leaves of Zea mays plants in response to nitrate availability by two-dimensional gel electrophoresis analysis. Bmc Plant Biology, 9.

  33. Raaijmakers, J. M., Paulitz, T. C., Steinberg, C., Alabouvette, C., & Moenne-Loccoz, Y. (2009). The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant and Soil, 321, 341–361.

    Article  CAS  Google Scholar 

  34. Rhee, S. G., & Woo, H. A. (2011). Multiple functions of peroxiredoxins: peroxidases, sensors and regulators of the intracellular messenger H2O2, and protein chaperones. Antioxidants & Redox Signaling, 15, 781–794.

    Article  CAS  Google Scholar 

  35. Richardson, A. E., Barea, J.-M., McNeill, A. M., & Prigent-Combaret, C. (2009). Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant and Soil, 321, 305–339.

    Article  CAS  Google Scholar 

  36. Roncato-Maccari, L. D. B., Ramos, H. J. O., Pedrosa, F. O., Alquini, Y., Chubatsu, L. S., Yates, M. G., Rigo, L. U., Steffens, M. B. R., & Souza, E. M. (2003). Endophytic Herbaspirillum seropedicae expresses nif genes in gramineous plants. FEMS Microbiology Ecology, 45, 39–47.

    Article  CAS  Google Scholar 

  37. Schmidt, M. A., Balsanelli, E., Faoro, H., Cruz, L. M., Wassem, R., de Baura, V. A., Weiss, V., Yates, M. G., Madeira, H. M. F., Pereira-Ferrari, L., Fungaro, M. H. P., de Paula, F. M., Pereira, L. F. P., Vieira, L. G. E., Olivares, F. L., Pedrosa, F. O., de Souza, E. M., & Monteiro, R. A. (2012). The type III secretion system is necessary for the development of a pathogenic and endophytic interaction between Herbaspirillum rubrisubalbicans and Poaceae. BMC Microbiology, 12, 98.

    Article  CAS  Google Scholar 

  38. Souza, E. M., Pedrosa, F. O., Rigo, L. U., Machado, H. B., & Yates, M. G. (2000). Expression of the nifA gene of Herbaspirillum seropedicae: role of the NtrC and NifA binding sites and of the-24/-12 promoter element. Microbiology-Uk, 146, 1407–1418.

    CAS  Google Scholar 

  39. Vargas, L., Gurjao de Carvalho, T. L., Gomes Ferreira, P. C., Divan Baldani, V. L., Baldani, J. I., & Hemerly, A. S. (2012). Early responses of rice (Oryza sativa L.) seedlings to inoculation with beneficial diazotrophic bacteria are dependent on plant and bacterial genotypes. Plant and Soil, 356, 127–137.

    Article  CAS  Google Scholar 

  40. Verhagen, B. W. M., Glazebrook, J., Zhu, T., Chang, H. S., van Loon, L. C., & Pieterse, C. M. J. (2004). The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis. Molecular Plant-Microbe Interactions, 17, 895–908.

    Article  CAS  Google Scholar 

  41. Walker, V., Couillerot, O., Von Felten, A., Bellvert, F., Jansa, J., Maurhofer, M., Bally, R., Moenne-Loccoz, Y., & Comte, G. (2012). Variation of secondary metabolite levels in maize seedling roots induced by inoculation with Azospirillum, Pseudomonas and Glomus consortium under field conditions. Plant and Soil, 356, 151–163.

    Article  CAS  Google Scholar 

  42. Wang, H.-C., Wang, H.-C., Leu, J.-H., Kou, G.-H., Wang, A. H. J., & Lo, C.-F. (2007). Protein expression profiling of the shrimp cellular response to white spot syndrome virus infection. Developmental and Comparative Immunology, 31, 672–686.

    Article  CAS  Google Scholar 

  43. Wood, Z. A., Schroder, E., Harris, J. R., & Poole, L. B. (2003). Structure, mechanism and regulation of peroxiredoxins. Trends in Biochemical Sciences, 28, 32–40.

    Article  CAS  Google Scholar 

  44. Xiong, L. M., & Zhu, J. K. (2003). Regulation of abscisic acid biosynthesis. Plant Physiology, 133, 29–36.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The present study was financially supported by the National Institute of Science and Technology—Biological Nitrogen Fixation, INCT FBN, National Council for Scientific and Technological Development, CNPq, and Ministry of Science and Technology, Brazil. CSF is a recipient of PDJ fellowship from CNPq. FPA is a recipient of PhD fellowship from INCT FBN, CAPES, Ministry of Education, Brazil. PAVN is a recipient of PNPD fellowship from CAPES. ACMA is a recipient of research fellowship (PQ-2) from CNPq. We would like to express our gratitude to Dr. Fábio de Oliveira Pedrosa, Universidade Federal do Paraná, for providing H. seropedicae strain.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ana Carolina Maisonnave Arisi.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Figure S1

(DOCX 56 kb)

Table S1

(DOCX 11 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ferrari, C.S., Amaral, F.P., Bueno, J.C.F. et al. Expressed Proteins of Herbaspirillum seropedicae in Maize (DKB240) Roots-Bacteria Interaction Revealed Using Proteomics. Appl Biochem Biotechnol 174, 2267–2277 (2014). https://doi.org/10.1007/s12010-014-1197-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-014-1197-3

Keywords

Navigation