Skip to main content
SpringerLink
Log in

Simultaneous inoculation with beneficial and pathogenic microorganisms modifies peanut plant responses triggered by each microorganism

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Plant signaling pathways activated by single microbial species may be modified by the presence of other microbial groups. Here, link between phenotypic changes of peanut plants co- inoculated with Bradyrhizobium sp. SEMIA6144, Bacillus sp. CHEP5 and Sclerotium rolfsii, and molecules involved in peanut responses to each microorganism was evaluated.

Methods

Phenolic compounds content, peroxidase activity and AhSymRK gene expression were evaluated in plants co-inoculated and inoculated with each microorganism.

Results

Peroxidase activity, associated with peanut response to the pathogen, was induced earlier in plants co-inoculated than in those inoculated only with S. rolfsii, in coincidence with their more tolerant phenotype to this pathogen. The increase in phenolic compounds content induced by the biocontrol agent Bacillus sp. CHEP5 was affected by the co-inoculation with Bradyrhizobium sp. SEMIA6144. However, the bacterial protection against S. rolfsii remains unaltered. In co-inoculated plants, AhSymRK gene expression level was similar to plants inoculated only with the microsymbiont, in concordance with their symbiotic phenotypes.

Conclusions

We demonstrated that responses triggered in peanut plants by single microbial species populations are modified in presence of others, highlighting the relevance to improve our understanding about plant responses to soil microbial communities.

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
Fig. 6

Similar content being viewed by others

References

  • Ainsworth EA, Gillespie KM (2007) Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin-Ciocalteu reagent. Nat Protoc 2:875–877

    Article  CAS  Google Scholar 

  • Almagro L, Gómez Ros LV, Belchi-Navarro S, Bru R, Ros Barceló A, Pedreno MA (2008) Class III peroxidases in plant defence reactions. J Exp Bot 60:377–390

    Article  Google Scholar 

  • Balasundram N, Sundram K, Samman S (2006) Phenolic compounds in plants and Agri-industrial by-products: antioxidant activity, occurrence, and potential uses. Food Chem 99:191–203

    Article  CAS  Google Scholar 

  • Bellincampi D, Cervone F, Lionetti V (2014) Plant cell wall dynamics and wall-related susceptibility in plant-pathogen interactions. Front Plant Sci 5:1–8

    Article  Google Scholar 

  • Berg G (2009) Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84:11–18

    Article  CAS  Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Chen T, Duan L, Zhou B, Yu H, Zhu H, Cao Y, Zhang Z (2017) Interplay of pathogen-induced defense responses and symbiotic establishment in Medicago truncatula. Front Microbiol 8:1–13

    Google Scholar 

  • Doley K, Dudhane M, Borde M (2017) Biocontrol of Sclerotium rolfsii in groundnut by using microbial inoculants. Not Sci Biol 9:124–130

    Article  CAS  Google Scholar 

  • Espelie K, Franceschi V, Kolattukudy P (1986) Immunocytochemical localization and time course of appearance of an anionic peroxidase associated with suberization in wound healing potato tuber tissue. Plant Physiol 81:487–492

    Article  CAS  Google Scholar 

  • Fabra A, Castro S, Taurian T, Angelini J, Ibañez F, Dardanelli M, Valetti L (2010) Interaction among Arachis hypogaea L. (peanut) and beneficial soil microorganisms: how much is it known? Crit Rev Microbiol 36:179–194

    Article  CAS  Google Scholar 

  • Faulkner C, Robatzek S (2012) Plants and pathogens: putting infection strategies and defence mechanisms on the map. Curr Opin Plant Biol 15:699–707

    Article  CAS  Google Scholar 

  • Figueredo MS, Tonelli ML, Taurian T, Angelini J, Ibañez F, Valetti L, Fabra A (2014) Interrelationships between Bacillus sp. CHEP5 and Bradyrhizobium sp. SEMIA6144 in the induced systemic resistance against Sclerotium rolfsii and symbiosis on peanut plants. J Biosci 39:877–885

    Article  CAS  Google Scholar 

  • Figueredo MS, Tonelli ML, Ibáñez F, Morla F, Cerioni G, del Carmen Tordable M, Fabra A (2017) Induced systemic resistance and symbiotic performance of peanut plants challenged with fungal pathogens and co-inoculated with the biocontrol agent Bacillus sp. CHEP5 and Bradyrhizobium sp. SEMIA6144. Microbiol Res 197:65–73

    Article  CAS  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    Article  CAS  Google Scholar 

  • Grupta CP, Dubey RC, Maheshwari DK (2002) Plant growth enhancement and suppression of Macrophomina phaseolina causing charcoal rot of peanut by fluorescent Pseudomonas. Biol Fertil Soils 35:399–405

    Article  Google Scholar 

  • Hoagland DR, Arnon DI (1950) Water culture method for growing plants without soil. Calif Agric Exp Stn Circ 347

  • Ibáñez F, Angelini J, Figueredo MS, Muñoz V, Tonelli ML, Fabra A (2015) Sequence and expression analysis of putative Arachis hypogaea (peanut) nod factor perception proteins. J Plant Res 128:709–718

    Article  Google Scholar 

  • Jain A, Singh S, Kumar Sarma B, Bahadur Singh H (2012) Microbial consortium-mediated reprogramming of defence network in pea to enhance tolerance against Sclerotinia sclerotiorum. J Appl Microbiol 112:537–550

    Article  CAS  Google Scholar 

  • 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 139:31–35

    Article  CAS  Google Scholar 

  • Lareen A, Burton F, Schäfer P (2016) Plant root-microbe communication in shaping root microbiomes. Plant Mol Biol 90:575–587

    Article  CAS  Google Scholar 

  • Lehmmann S, Serrano M, L’Haridon F, Tjamos SE, Metraux JP (2015) Reactive oxygen species and plant resistance to fungal pathogens. Phytochemistry 112:54–62

    Article  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • Lopez-Gomez M, Sandal N, Stougaard J, Boller T (2012) Interplay of flg22-induced defence responses and nodulation in Lotus japonicus. J Exp Bot 63:393–401

    Article  CAS  Google Scholar 

  • Mauch-Mani B, Baccelli I, Luna E, Flors V (2017) Defense priming: an adaptive part of induced resistance. Annu Rev Plant Biol 68:485–512

    Article  CAS  Google Scholar 

  • McDougall CJ (1991) Cell-wall-associated peroxidases and lignifications during growth of flax fibers. J Plant Physiol 139:182–186

    Article  CAS  Google Scholar 

  • McDougall CJ (1993) Accumulation of wall-associated peroxidases during wound-induced suberization in flax. J Plant Physiol 142:651–656

    Article  CAS  Google Scholar 

  • Passardi F, Penel C, Dunand C (2004) Performing the paradoxical: how plant peroxidases modify the cell wall. Trends Plant Sci 9:534–540

    Article  CAS  Google Scholar 

  • Pieterse CM, Zamioudis C, Berendsen RL, Weller DM, Van Wees SC, Bakker PA (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375

    Article  CAS  Google Scholar 

  • Singh A, Sarma BK, Upadhyay RS, Singh HB (2013) Compatible rhizosphere microbes mediated alleviation of biotic stress in chickpea through enhanced antioxidant and phenylpropanoid activities. Microbiol Res 168:33–40

    Article  CAS  Google Scholar 

  • Sinharoy S, Saha S, Chaudhury SR, DasGupta M (2009) Transformed hairy roots of Arachis hypogea: a tool for studying root nodule symbiosis in a non-infection thread legume of the Aeschynomeneae tribe. MPMI 22:132–142

    Article  CAS  Google Scholar 

  • Somasegaran P, Hoben H (1994) Quantifying the growth of rhizobia. In: Garber R (ed) Handbook for rhizobia: methods in legume rhizobia technology. Springer, New York, pp 382–390 Section 3

    Chapter  Google Scholar 

  • Sosa Alderete LG, Talano MA, Ibañez SG, Purro S, Agostini E, Milrad SR, Medina MI (2009) Establishment of transgenic tobacco hairy roots expressing basic peroxidases and its application for phenol removal. J Biotechnol 139:273–279

    Article  CAS  Google Scholar 

  • Tonelli ML, Taurian T, Ibáñez F, Angelini J, Fabra A (2010) Selection and in vitro characterization of biocontrol agents with potential to protect peanut plants against fungal pathogens. J Plant Pathol 92:73–82

    Google Scholar 

  • Tonelli M, Furlán A, Taurian T, Castro S, Fabra A (2011) Peanut priming induced by biocontrol agents. Physiol Mol Plant Pathol 75:100–105

    Article  Google Scholar 

  • van Dam NM, Bouwmeester HJ (2016) Metabolomics in the rhizosphere: tapping into belowground chemical communication. Trends Plant Sci 21:256–265

    Article  Google Scholar 

  • van Wees S, Van der Ent S, Pieterse C (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443–448

    Article  Google Scholar 

  • Vincent JM (1970) A manual for the practical study of root nodule bacteria. In: International biological program handbook no 15. Blackwell Scientific Publications Ltd, Oxford, pp 73–97

    Google Scholar 

  • Xie XG, Fu WQ, Zhang FM, Shi XM, Zeng YT, Li H, Dai CC (2017) The endophytic fungus Phomopsis liquidambari increases nodulation and N2 fixation in Arachis hypogaea by enhancing hydrogen peroxide and nitric oxide signalling. Microb Ecol 7:427–440

    Article  Google Scholar 

  • Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23:283–333

    Article  CAS  Google Scholar 

  • Zipfel C, Oldroyd GE (2017) Plant signalling in symbiosis and immunity. Nature 543:328–336

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was financially supported by Secretaría de Ciencia y Tecnología-Universidad Nacional de Río Cuarto, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) (PIP 01105) and Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT). María Soledad Figueredo and Johan Rodriguez hold a scholarship granted by CONICET and ANPCyT, respectively. Fernando Ibáñez and Adriana Fabra are members of the Research Career from CONICET.

Author information

Authors and Affiliations

  1. Departamento de Ciencias Naturales, Facultad de Ciencias Exactas, Físico-Químicas y Naturales, Universidad Nacional de Río Cuarto, Agencia Postal 3, 5800 Río Cuarto, Córdoba, Argentina

    María Soledad Figueredo, Fernando Ibáñez, Johan Rodríguez & Adriana Fabra

Authors
  1. María Soledad Figueredo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fernando Ibáñez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Johan Rodríguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Adriana Fabra
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Adriana Fabra.

Additional information

Responsible Editor: Matthew G. Bakker.

Electronic supplementary material

ESM 1

(PDF 355 kb)

ESM 2

(PDF 101 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Figueredo, M.S., Ibáñez, F., Rodríguez, J. et al. Simultaneous inoculation with beneficial and pathogenic microorganisms modifies peanut plant responses triggered by each microorganism. Plant Soil 433, 353–361 (2018). https://doi.org/10.1007/s11104-018-3846-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-018-3846-8

Keywords

Search

Navigation