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Archives of Microbiology

, Volume 199, Issue 9, pp 1283–1291 | Cite as

Symbiotic performance and induction of systemic resistance against Cercospora sojina in soybean plants co-inoculated with Bacillus sp. CHEP5 and Bradyrhizobium japonicum E109

  • María Laura Tonelli
  • C. Magallanes-Noguera
  • A. Fabra
Original Paper

Abstract

Soybean is an economically very important crop throughout the word and particularly in Argentina. Soybean yield may be affected by many factors such as the lack of some essential nutrients or pathogens attack. In this work we demonstrated that the co-inoculation of the native biocontrol bacterium Bacillus sp. CHEP5 which induces resistance against Cercospora sojina in soybean and the nitrogen fixing strain Bradyrhizobium japonicum E109, was more effective in reducing frog leaf spot severity than the inoculation of the biocontrol agent alone. Probably, this is related with the increase in the ability to form biofilm when both bacteria are growing together. Furthermore, Bacillus sp. CHEP5 inoculation did not affect Bradyrhizobium japonicum E109 symbiotic behavior and flavonoids composition of root exudates in pathogen challenged plants. These results suggest that co-inoculation of plants with rhizobia and biocontrol agents could be a strategy to improve soybean production in a sustainable system.

Keywords

Soybean Bacillus sp. Cercospora sojina Induced systemic resistance Bradyrhizobium japonicum E109 Nodulation 

Notes

Acknowledgements

This study was financially supported by the SECyT-UNRC, CONICET, Ministerio de Ciencia y Tecnología de Cordoba, ANPCyT. M. L. Tonelli, C. Magallanes-Noguera and A. Fabra are members of the Research Career from CONICET.

References

  1. Baetz U, Martinoia E (2014) Root exudates: the hidden part of plant defense. Trends Plant Sci 19:90–98CrossRefPubMedGoogle Scholar
  2. Bais HP, Fall R, Vivanco JM (2004) Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin Production. Plant Physiol 134:307–319CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266CrossRefPubMedGoogle Scholar
  4. Barea JM, Pozo MJ, Azcón R, Azcón-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778CrossRefPubMedGoogle Scholar
  5. Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350CrossRefPubMedGoogle Scholar
  6. Buensateai N, Yuen G, Prathuangwong S (2009) Priming, signaling, and protein production associated with induced resistance by Bacillus amyloliquefaciens KPS46. World J Microbiol Biotechnol 25:1275–1286CrossRefGoogle Scholar
  7. BurmØlle M, Webb JS, Rao D, Hansen LH, SØrensen SJ, Kielleberg S (2006) Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms. Appl Environ Microbiol 72:3916–3923CrossRefPubMedPubMedCentralGoogle Scholar
  8. Carmona MA, Scandiani M, Luque A (2009) Severe outbreaks of soybean frogeye leaf spot caused by Cercospora sojinain the pampean region, Argentina. Plant Dis 93:966CrossRefGoogle Scholar
  9. Cassán F, Perrig D, Sgroy V, Masciarelli O, Penna C, Luna V (2009) Azospirillum brasilense Az39 and Bradyrhizobium japonicum E109, inoculated singly or in combination, promote seed germination and early seedling growth in corn (Zea mays L.) and soybean (Glycine max L.). Eur J Soil Biol 45:28–35CrossRefGoogle Scholar
  10. Cooper JE (2004) Multiple responses of rhizobia to flavonoids during legume root infection. Inc Adv Plant Pathol 41:1–62CrossRefGoogle Scholar
  11. Deshwal VK, Pandey P, Kang SC, Maheshwari DK (2003) Rhizobia as a biological control agent against soil borne plant pathogenic fungi. Indian J Exp Biol 41:1160–1164PubMedGoogle Scholar
  12. Evangelisti E, Rey T, Schornack S (2014) Cross-interference of plant development and plant–microbe interactions. Curr Opin Plant Biol 20:118–126CrossRefPubMedGoogle Scholar
  13. Fabra A, Castro S, Taurian T, Angelini J, Ibañez F, Dardanelli M, Tonelli ML, Bianucci E, Valetti L (2010) Interaction among Arachis hypogaea L. (peanut) and beneficial soil microorganisms: how much is it known? Crit Rev Microbiol 36:179–194CrossRefPubMedGoogle Scholar
  14. Fehr WR, Caviness CE (1977) Stages of soybean development. Iowa St Univ Spec Rep 80:11pGoogle Scholar
  15. Foster-Hartnett D, Danesh D, Peñuela S, Sharopova N, Endre G, VandenBosch KA, Young ND, Samac DA (2007) Molecular and cytological responses of Medicago truncatula to Erysiphepisi. Mol Plant Pathol 8:307–319CrossRefPubMedGoogle Scholar
  16. Hassan S, Mathesius U (2012) The role of flavonoids in root–rhizosphere signalling: opportunities and challenges for improving plant–microbe interactions. J Exp Bot 63:3429–3444CrossRefPubMedGoogle Scholar
  17. Hershman DE (2013) Soybean foliar spots and blights. Plant pathology fact sheet. Cooperative extension service. University of Kentucky, College of Agriculture, USAGoogle Scholar
  18. Hoagland DR, Arnon DI (1950) The water culture method for growing plants without soil. Calif Agric Exp Stn Circ 347:1–39Google Scholar
  19. Iqbal MJ, Yaegashi S, Ahsan R, Shopinski K, Lightfoot DA (2005) Root response to F. solani f. sp. glycines, temporal accumulation of transcripts in partially resistant and susceptible soybean. Theor App Genet 110:1429–1438CrossRefGoogle Scholar
  20. Kataran E, Watnick P (2009) Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Mol Biol R73:310–347CrossRefGoogle Scholar
  21. Kloepper J, Tuzun S, Kúc J (1992) Proposed definitions related to induced disease resistance. Biocontrol Sci Technol 2:349–351CrossRefGoogle Scholar
  22. Kong Q, Shan S, Liu Q, Wang X, Yu F (2010) Biocontrol of Aspergillus flavus on peanut kernels by use of a strain of marine Bacillus megaterium. Int J Food Microbiol 139:31–35CrossRefPubMedGoogle Scholar
  23. Lagunas B, Schäfer P, Gifford ML (2015) Housing helpful invaders: the evolutionary and molecular architecture underlying plant root-mutualist microbe interactions. J Exp Bot 66:2177–2186CrossRefPubMedPubMedCentralGoogle Scholar
  24. Liang Y, Cao Y, Tanaka K, Thibivilliers S, Wan J, Choi J, Ho Kang C, Qiu J, Stacey G (2013) Nonlegumes respond to rhizobial Nod factors by suppressing the innate immune response. Science 341:1384–1387CrossRefPubMedGoogle Scholar
  25. Lodeiro AR, López-García SL, Vázquez TEE, Favelukes G (2000) Stimulation of adhesiveness, infectivity, and competitiveness for nodulation of Bradyrhizobium japonicum by its pretreatment with soybean seed lectin. FEMS Microbiol Lett 188:177–184CrossRefPubMedGoogle Scholar
  26. López-García S, Vázquez TEE, Favelukes G, Lodeiro A (2001) Improved soybean root association of N-starved Bradyrhizobium japonicum. J Bacteriol 183:7241–7252CrossRefPubMedPubMedCentralGoogle Scholar
  27. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting Rhizobacteria. Annu Rev Microbiol 63:541–556CrossRefPubMedGoogle Scholar
  28. Mian MAR, Missaoui AM, Walker DR, Phillips DV, Boerma HR (2008) Frogeye leaf spot of soybean: a review and proposed race designations for Isolates of Cercospora sojina Hara. Crop Sci 48:14–24CrossRefGoogle Scholar
  29. Miyata K, Kozaki T, Kouzai Y, Ozawa K, Ishii K, Asamizu E, Yoshihiro O, Yosuke U, Ayano M, Yoshihiro K, Kohki A, Hanae K, Yoko N, Naoto S, Tomomi N (2014) The bifunctional plant receptor, OsCERK1, regulates both chitin-triggered immunity and arbuscular mycorrhizal symbiosis in rice. Plant Cell Physiol 55:1864–1872CrossRefPubMedGoogle Scholar
  30. O’Toole GA, Kolter R (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30:295–304CrossRefPubMedGoogle Scholar
  31. Pel MJC, Pieterse CMJ (2013) Microbial recognition and evasion of host immunity. J Exp Bot. doi: 10.1093/jxb/err313 PubMedGoogle Scholar
  32. Pineda A, Soler R, Pozo MJ, Rasmann S, Turlings TCJ (2015) Editorial: above-belowground interactions involving plants, microbes and insects. Front Plant Sci 6:1–3CrossRefGoogle Scholar
  33. Podile AR, Kishore K (2006) Plant growth-promoting rhizabacteria. In: Gnanamanickam SS (ed) Plant-associated bacteria. Springer, New York, pp 195–230CrossRefGoogle Scholar
  34. Rafique M, Hayat K, Mukhtar T, Khan AA, Afridi MS, Hussain T, Sultan T, Munis MFH, Imran M, Chaudhary HJ (2015) Bacterial biofilm formation and its role against agricultural pathogens. In: Méndez-Vilas A (ed.) The battle against microbial pathogens: basic science, Technological Advances and Educational Programs, pp 373–382Google Scholar
  35. Ressia JL, Lázaro L, Lett G, Mendivil G, Portela R, Balbuena RH (2003) Sistemas de labranza e inoculación en soja. Ef Sobre Crecim Rend Cultivo Agrocienc 37:167–176Google Scholar
  36. Samac DA, Graham MA (2007) Recent advances in legume-microbe interactions: recognition, defense response, and symbiosis from a genomic perspective. Microb Interact Plant Defin 144:582–587Google Scholar
  37. Somasegaran P, Hoben H (1994) Quantifying the growth of rhizobia. Hand book for rhizobia: methods in legume rhizobiatechnology. Springer-Verlag Inc, New York, pp 382–390 (Section 3) CrossRefGoogle Scholar
  38. Stevens RB (1974) Mycology guidebook. University of Washington, Seattle, p 703Google Scholar
  39. Tonelli ML, Fabra A (2014) The biocontrol agent Bacillus sp. CHEP5 primes the defense response against Cercospora sojina. World J Microbiol Biot 30:2503–2509CrossRefGoogle Scholar
  40. Tonelli ML, Taurian T, Ibáñez F, Angelini J, Fabra A (2010) Selection and in vitro characterization of biocontrol agents to protect peanut plants against fungal pathogens. J, Plant Pathol 92:73–82Google Scholar
  41. Vincent JM (1970) A manual for the practical study of root nodule bacteria. International biological programme handbook no. 15. Blackwell Scientific Publications Ltd, Oxford, pp 73–97Google Scholar
  42. Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51CrossRefPubMedPubMedCentralGoogle Scholar
  43. Wang W, Xie Z-P, Staehelin C (2014) Functional analysis of chimeric lysin motif domain receptors mediating Nod factor-induced defense signaling in Arabidopsis thaliana and chitin-induced nodulation signaling in Lotus japonicus. Plant J78:56–69Google Scholar
  44. Webster G, Jain V, Davey MR, GsugC VasseJ, Dénarié J, Cocking EC (1998) The flavonoid naringenin stimulates he intercellular colonization of wheat roots by Azorhizobium caulinodans. Plant Cell Environ 21:373–383CrossRefGoogle Scholar
  45. Wheeler JB (1969) An introduction to plant diseases. Wiley, London, p 347Google Scholar
  46. Williams RJ, Spencer JP, Rice-Evans C (2004) Flavonoids: antioxidants or signalling molecules? Free Radic Bio Med 36:838–849CrossRefGoogle Scholar
  47. Yamazaki A, Hayashi M (2015) Building the interaction interfaces: host responses upon infection with microorganisms. Curr Opin Plant Biol 23:132–139CrossRefPubMedGoogle Scholar
  48. Yaryura PM, León M, Correa OS, Kerber NL, Pucheu NL, García AF (2008) Assessment of the role of chemotaxis and biofilm formation as requirements for colonization of roots and seeds of soybean plants by Bacillus amyloliquefaciens BNM339. Curr Microbiol 56:625–632CrossRefPubMedGoogle Scholar
  49. Zhang X, Dong W, Sun J, Feng F, Deng Y, He Z et al (2015) The receptor kinase CERK1 has dual functions in symbiosis and immunity signalling. Plant J81:258–267Google Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • María Laura Tonelli
    • 1
  • C. Magallanes-Noguera
    • 1
  • A. Fabra
    • 1
  1. 1.Departamento de Ciencias Naturales, Facultad de Ciencias Exactas, Físico-Químicas y NaturalesUniversidad Nacional de Río CuartoRío CuartoArgentina

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