Skip to main content

Advertisement

SpringerLink
Log in

Identification of mVOCs from Andean Rhizobacteria and Field Evaluation of Bacterial and Mycorrhizal Inoculants on Growth of Potato in its Center of Origin

  • Plant Microbe Interactions
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Food security (a pressing issue for all nations) faces a threat due to population growth, land availability for growing crops, a changing climate (leading to increases in both abiotic and biotic stresses), heightened consumer awareness of the risks related to the use of agrichemicals, and also the reliance on depleting fossil fuel reserves for their production. Legislative changes in Europe mean that fewer agrichemicals will be available in the future for the control of crop pests and pathogens. The need for the implementation of a more sustainable agricultural system globally, incorporating an integrated approach to disease management, has never been more urgent. To that end, the Valorizing Andean Microbial Diversity (VALORAM) project (http://valoram.ucc.ie), funded under FP7, examined the role of microbial communities in crop production and protection to improve the sustainability, food security, environmental protection, and productivity for rural Andean farmers. During this work, microbial volatile organic compounds (mVOCs) of 27 rhizobacterial isolates were identified using gas chromatography/mass spectrometry (GC/MS), and their antifungal activity against Rhizoctonia solani was determined in vitro and compared to the activity of a selection of pure volatile compounds. Five of these isolates, Pseudomonas palleroniana R43631, Bacillus sp. R47065, R47131, Paenibacillus sp. B3a R49541, and Bacillus simplex M3-4 R49538 trialled in the field in their respective countries of origin, i.e., Bolivia, Peru, and Ecuador, showed significant increase in the yield of potato. The strategy followed in the VALORAM project may offer a template for the future isolation and determination of putative biocontrol and plant growth-promoting agents, useful as part of a low-input integrated pest management system.

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

Similar content being viewed by others

References

  1. Ampofo JA, Tetteh W, Bello M (2009) Impact of commonly used agrochemicals on bacterial diversity in cultivated soils. Indian J Microbiol 49:223–229. doi:10.1007/s12088-009-0042-9

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  2. Adesemoye AO, Kloepper JW (2009) Plant-microbes interactions in enhanced fertilizer-use efficiency. Appl Microbiol Biotechnol 85:1–12. doi:10.1007/s00253-009-2196-0

    Article  CAS  PubMed  Google Scholar 

  3. Kloeppe JW, Rodríguez-Kábana R, Zehnder AW, Murphy JF, Sikora E, Fernández C (1999) Plant root-bacterial interactions in biological control of soilborne diseases and potential extension to systemic and foliar diseases. Australas Plant Pathol 28:21–26. doi:10.1071/AP99003

    Article  Google Scholar 

  4. Ryu C-M, Hu C-H, Locy R, Kloepper J (2005) Study of mechanisms for plant growth-promotion elicited by rhizobacteria in Arabidopsis thaliana. Plant Soil 268:285–292. doi:10.1007/s11104-004-0301-9

    Article  CAS  Google Scholar 

  5. Schüβler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421. doi:10.1017/S0953756201005196

    Article  Google Scholar 

  6. Senés-Guerrero C, Torres-Cortés G, Pfeiffer S, Rojas M, Schüßler A (2014) Potato-associated arbuscular mycorrhizal fungal communities in the Peruvian Andes. Mycorrhiza 24:405–417. doi:10.1007/s00572-013-0549-0

    Article  PubMed  Google Scholar 

  7. Vespermann A, Kai M, Piechulla B (2007) Rhizobacterial volatiles affect the growth of fungi and Arabidopsis thaliana. Appl Environ Microbiol 73:5639–5641. doi:10.1128/aem. 01078-07

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  8. Effmert U, Kalderás J, Warnke R, Piechulla B (2012) Volatile mediated interactions between bacteria and fungi in the soil. J Chem Ecol 38:665–703. doi:10.1007/s10886-012-0135-5

    Article  CAS  PubMed  Google Scholar 

  9. Ryu C-M, Farag MA, Hu C-H, Reddy MS, Wei H-X, Paré PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci 100:4927–4932. doi:10.1073/pnas.0730845100

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  10. Ryu C-M, Farag MA, Hu C-H, Reddy MS, Kloepper JW, Paré PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026. doi:10.1104/pp. 103.026583

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  11. Velázquez-Becerra C, Macías-Rodríguez L, López-Bucio J, Altamirano-Hernández J, Flores-Cortez I, Valencia-Cantero E (2011) A volatile organic compound analysis from Arthrobacter agilis identifies dimethylhexadecylamine, an amino-containing lipid modulating bacterial growth and Medicago sativa morphogenesis in vitro. Plant Soil 339:329–340. doi:10.1007/s11104-010-0583-z

    Article  Google Scholar 

  12. Zou C, Li Z, Yu D (2010) Bacillus megaterium strain XTBG34 promotes plant growth by producing 2-pentylfuran. J Microbiol 48:460–466. doi:10.1007/s12275-010-0068-z

    Article  CAS  PubMed  Google Scholar 

  13. Blom D, Fabbri C, Connor EC, Schiestl FP, Klauser DR, Boller T, Eberl L, Weisskopf L (2011) Production of plant growth modulating volatiles is widespread among rhizosphere bacteria and strongly depends on culture conditions. Environ Microbiol 13:3047–3058. doi:10.1111/j.1462-2920.2011.02582.x

    Article  CAS  PubMed  Google Scholar 

  14. Yu S-M, Lee Y (2013) Plant growth promoting rhizobacterium Proteus vulgaris JBLS202 stimulates the seedling growth of Chinese cabbage through indole emission. Plant Soil 370:485–495. doi:10.1007/s11104-013-1652-x

    Article  CAS  Google Scholar 

  15. Groenhagen U, Baumgartner R, Bailly A, Gardiner A, Eberl L, Schulz S, Weisskopf L (2013) Production of bioactive volatiles by different Burkholderia ambifaria strains. J Chem Ecol 39:892–906. doi:10.1007/s10886-013-0315-y

    Article  CAS  PubMed  Google Scholar 

  16. Blom D, Fabbri C, Eberl L, Weisskopf L (2010) Volatile-mediated killing of Arabidopsis thaliana by bacteria is mainly due to hydrogen cyanide. Appl Environ Microbiol 77:1000–1008. doi:10.1128/aem. 01968-10

    Article  PubMed Central  PubMed  Google Scholar 

  17. Kai M, Crespo E, Cristescu SM, Harren FJ, Francke W, Piechulla B (2010) Serratia odorifera: analysis of volatile emission and biological impact of volatile compounds on Arabidopsis thaliana. Appl Microbiol Biotechnol 88:965–976. doi:10.1007/s00253-010-2810-1

    Article  CAS  PubMed  Google Scholar 

  18. Weise T, Kai M, Piechulla B (2013) Bacterial ammonia causes significant plant growth inhibition. PLoS ONE 8:e63538. doi:10.1371/journal.pone.0063538

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Fernando WGD, Ramarathnam R, Krishnamoorthy AS, Savchuk SC (2005) Identification and use of potential bacterial organic antifungal volatiles in biocontrol. Soil Biol Biochem 37:955–964. doi:10.1016/j.soilbio.2004.10.021

    Article  CAS  Google Scholar 

  20. Yuan J, Raza W, Shen Q, Huang Q (2012) Antifungal activity of Bacillus amyloliquefaciens NJN-6 volatile compounds against Fusarium oxysporum f. sp. cubense. Appl Environ Microbiol 78:5942–5944. doi:10.1128/aem. 01357-12

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  21. Ghyselinck J, Velivelli SL, Heylen K, O’Herlihy E, Franco J, Rojas M, De Vos P, Prestwich BD (2013) Bioprospecting in potato fields in the Central Andean Highlands: screening of rhizobacteria for plant growth-promoting properties. Syst Appl Microbiol 36:116–127. doi:10.1016/j.syapm.2012.11.007

    Article  CAS  PubMed  Google Scholar 

  22. Velivelli S, O’Herlihy E, Janczura B, Doyle Prestwich B, Ghyselinck J, De Vos P (2012) Efficacy of rhizobacteria on plant growth-promotion and disease suppression in vitro. Acta Horticult 961:525–532

    Google Scholar 

  23. Athukorala SNP, Fernando WGD, Rashid KY, de Kievit T (2010) The role of volatile and non-volatile antibiotics produced by Pseudomonas chlororaphis strain PA23 in its root colonization and control of Sclerotinia sclerotiorum. Biocontrol Sci Tech 20:875–890. doi:10.1080/09583157.2010.484484

    Article  Google Scholar 

  24. Farag MA, Ryu C-M, Sumner LW, Paré PW (2006) GC–MS SPME profiling of rhizobacterial volatiles reveals prospective inducers of growth promotion and induced systemic resistance in plants. Phytochemistry 67:2262–2268. doi:10.1016/j.phytochem.2006.07.021

    Article  CAS  PubMed  Google Scholar 

  25. Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil–root interface. Plant Soil 321:5–33. doi:10.1007/s11104-009-9925-0

    Article  CAS  Google Scholar 

  26. Kai M, Effmert U, Berg G, Piechulla B (2007) Volatiles of bacterial antagonists inhibit mycelial growth of the plant pathogen Rhizoctonia solani. Arch Microbiol 187:351–360. doi:10.1007/s00203-006-0199-0

    Article  CAS  PubMed  Google Scholar 

  27. Sang MK, Kim JD, Kim BS, Kim KD (2011) Root treatment with rhizobacteria antagonistic to Phytophthora blight affects anthracnose occurrence, ripening, and yield of pepper fruit in the plastic house and field. Phytopathology 101:666–678. doi:10.1094/phyto-08-10-0224

    Article  CAS  PubMed  Google Scholar 

  28. Kai M, Haustein M, Molina F, Petri A, Scholz B, Piechulla B (2009) Bacterial volatiles and their action potential. Appl Microbiol Biotechnol 81:1001–1012. doi:10.1007/s00253-008-1760-3

    Article  CAS  PubMed  Google Scholar 

  29. Dandurishvili N, Toklikishvili N, Ovadis M, Eliashvili P, Giorgobiani N, Keshelava R, Tediashvili M, Vainstein A, Khmel I, Szegedi E, Chernin L (2011) Broad-range antagonistic rhizobacteria Pseudomonas fluorescens and Serratia plymuthica suppress Agrobacterium crown gall tumours on tomato plants. J Appl Microbiol 110:341–352. doi:10.1111/j.1365-2672.2010.04891.x

    Article  CAS  PubMed  Google Scholar 

  30. Zou C-S, Mo M-H, Gu Y-Q, Zhou J-P, Zhang K-Q (2007) Possible contributions of volatile-producing bacteria to soil fungistasis. Soil Biol Biochem 39:2371–2379. doi:10.1016/j.soilbio.2007.04.009

    Article  CAS  Google Scholar 

  31. Fiddaman PJ, Rossall S (1993) The production of antifungal volatiles by Bacillus subtilis. J Appl Bacteriol 74:119–126. doi:10.1111/j.1365-2672.1993.tb03004.x

    Article  CAS  PubMed  Google Scholar 

  32. Fiddaman PJ, Rossall S (1994) Effect of substrate on the production of antifungal volatiles from Bacillus subtilis. J Appl Bacteriol 76:395–405

    Article  CAS  PubMed  Google Scholar 

  33. Weise T, Kai M, Gummesson A, Troeger A, von Reuss S, Piepenborn S, Kosterka F, Sklorz M, Zimmermann R, Francke W, Piechulla B (2012) Volatile organic compounds produced by the phytopathogenic bacterium Xanthomonas campestris pv. vesicatoria 85–10. Beilstein J Org Chem 8:579–596. doi:10.3762/bjoc.8.65

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Nicholson WL (2008) The Bacillus subtilis ydjL (bdhA) gene encodes acetoin reductase/2,3-butanediol dehydrogenase. Appl Environ Microbiol 74:6832–6838. doi:10.1128/aem. 00881-08

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  35. Marquez-Villavicencio MP, Weber B, Witherell RA, Willis DK, Charkowski AO (2011) The 3-hydroxy-2-butanone pathway is required for Pectobacterium carotovorum pathogenesis. PLoS ONE 6:e22974. doi:10.1371/journal.pone.0022974

    Article  PubMed Central  CAS  Google Scholar 

  36. Huang C-J, Tsay J-F, Chang S-Y, Yang H-P, Wu W-S, Chen C-Y (2012) Dimethyl disulfide is an induced systemic resistance elicitor produced by Bacillus cereus C1L. Pest Manag Sci 68:1306–1310. doi:10.1002/ps.3301

    Article  CAS  PubMed  Google Scholar 

  37. Song G, Ryu C-M (2013) Two volatile organic compounds trigger plant self-defense against a bacterial pathogen and a sucking insect in cucumber under open field conditions. Int J Mol Sci 14:9803–9819

    Article  PubMed Central  PubMed  Google Scholar 

  38. Spinelli F, Cellini A, Vanneste J, Rodriguez-Estrada M, Costa G, Savioli S, Harren FM, Cristescu S (2012) Emission of volatile compounds by Erwinia amylovora: biological activity in vitro and possible exploitation for bacterial identification. Trees 26:141–152. doi:10.1007/s00468-011-0667-2

    Article  CAS  Google Scholar 

  39. de Faria, S.M., Resende A.S., Júnior O.J.S., Boddey, R.M.: Exploiting mycorrhizae and Rhizobium symbioses to recover seriously gegraded soils. In: Polacco, JC, Todd, CD (eds.) Ecological Aspects of Nitrogen Metabolism in Plants. John Wiley & Sons, Inc., pp. 195–215. (2011)

  40. Compant S, Duffy B, Nowak J, Clément C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959. doi:10.1128/aem. 71.9.4951-4959.2005

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  41. Lugtenberg B, Kamilova F (2009) Plant growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556. doi:10.1146/annurev.micro.62.081307.162918

    Article  CAS  PubMed  Google Scholar 

  42. Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Sci 2012:15. doi:10.6064/2012/963401

    Google Scholar 

Download references

Acknowledgments

The research project “VALORAM-Valorizing Andean microbial diversity through sustainable intensification of potato-based farming systems” was supported by European Commission’s Seventh Framework Program FP7/2007-2013 under grant agreement No 227522, 01/02/2009-31/01/2014.

Author information

Authors and Affiliations

  1. School of Biological Earth and Environmental Sciences, University College Cork, Butler Building, Distillery Fields, North Mall, Cork, Ireland

    Siva L. S. Velivelli & Barbara Doyle Prestwich

  2. International Potato Center (CIP), Panamericana Sur Km 1, Apartado, 17-21-1977, Quito, Ecuador

    Peter Kromann

  3. Departamento de Ciencias Naturales, Universidad Técnica Particular de Loja (UTPL), San Cayetano Alto y Paris s/n, C.P. 11 01 608, Loja, Ecuador

    Paul Lojan & Juan Pablo Suarez

  4. International Potato Center (CIP), Av. La Molina 1895, Apartado, 1558, Lima, Peru

    Mercy Rojas

  5. Fundación PROINPA Foundation, Casilla Postal 4285, Av. Meneces, Km 4, El Paso, Cochabamba, Bolivia

    Javier Franco

Authors
  1. Siva L. S. Velivelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter Kromann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paul Lojan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mercy Rojas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Javier Franco
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Juan Pablo Suarez
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Barbara Doyle Prestwich
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Barbara Doyle Prestwich.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Velivelli, S.L.S., Kromann, P., Lojan, P. et al. Identification of mVOCs from Andean Rhizobacteria and Field Evaluation of Bacterial and Mycorrhizal Inoculants on Growth of Potato in its Center of Origin. Microb Ecol 69, 652–667 (2015). https://doi.org/10.1007/s00248-014-0514-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-014-0514-2

Keywords

Search

Navigation