Skip to main content
Log in

Volatile Indole Produced by Rhizobacterium Proteus vulgaris JBLS202 Stimulates Growth of Arabidopsis thaliana Through Auxin, Cytokinin, and Brassinosteroid Pathways

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Volatile compounds produced by bacteria play an important role in plant and bacteria interactions. Volatiles from the rhizobacterium Proteus vulgaris JBLS202 or synthetic indole increased the fresh weight of Arabidopsis thaliana Col-0 by 74.9–80.3 %, and 48.0–56.3 %, respectively. However, exposure to volatiles from JBLS202 or indole was unable to promote growth in the mutant lines of A. thaliana defective in auxin transport (eir1), cytokinin (cre1), and brassinosteroid metabolism (cbb1), whereas growth was significantly stimulated in the ethylene- (etr1) and gibberellin-insensitive (gai 1) mutants. In addition, Arabidopsis Col-0 treated with auxin, and brassinosteroid biosynthesis inhibitors was considerably arrested in growth-promoting performance by the volatiles. Moreover, exposure of Col-0 seedlings to JBLS202 or indole for 14 days resulted in overexpression of small auxin up RNA, histidine kinase1, and brassinosteroid biosynthetic cytochrome P450 genes. Overall, the results indicate that the indole emitted by JBLS202 stimulates the growth of A. thaliana through an interplay between the auxin, cytokinin, and brassinosteroid pathways. This is the first report on how bacterial indole influences the plant hormone signaling pathways.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

  • Blom D, Fabbri C, Connor EC, Schiestl FP, Klauser DR, Boller T et al (2011) Production of plant growth modulating volatiles is widespread among rhizosphere bacteria and strongly depends on culture conditions. Environ Microbiol 13:3047–3058

    Article  CAS  PubMed  Google Scholar 

  • Boller T, Herner RC, Kende H (1979) Assay for and enzymatic formation of an ethylene precursor, 1-aminocyclopropane-1-carboxylic acid. Planta 145:293–303

    Article  CAS  PubMed  Google Scholar 

  • Chang C, Kwok SF, Bleecker AB, Meyerowitz EM (1993) Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262:539–544

    Article  CAS  PubMed  Google Scholar 

  • Chant EL, Summers DK (2007) Indole signalling contributes to the stable maintenance of Escherichia coli multicopy plasmids. Mol Microbiol 63:35–43

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Dodd IC, Theobald JC, Belimov AA, Davies WJ (2013) The rhizobacterium Variovorax paradoxus 5C-2, containing ACC deaminase, promotes growth and development of Arabidopsis thaliana via an ethylene-dependent pathway. J Exp Bot 64:1565–1573

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cho SM, Kang BR, Han SH, Anderson AJ, Park JY, Lee YH et al (2008) 2R,3R-butanediol, a bacterial volatile produced by Pseudomonas chlororaphis O6, is involved in induction of systemic tolerance to drought in Arabidopsis thaliana. Mol Plant Microbe Interact 21:1067–1075

    Article  CAS  PubMed  Google Scholar 

  • Effmert U, Kalderas J, Warnke R, Piechulla B (2012) Volatile mediated interactions between bacteria and fungi in the soil. J Chem Ecol 38:665–703

    Article  CAS  PubMed  Google Scholar 

  • Fan S, Meng Q, Saha T, Sarkar FH, Rosen EM (2009) Low concentrations of diindolylmethane, a metabolite of indole-3-carbinol, protect against oxidative stress in a BRCA1-dependent manner. Cancer Res 69:6083–6091

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Farag MA, Ryu CM, Sumner LW, Pare 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

    Article  CAS  PubMed  Google Scholar 

  • Gerth K, Metzger R, Reichenbach H (1993) Induction of myxospores in Stigmatella aurantiaca (myxobacteria): inducers and inhibitors of myxospore formation, and mutants with a changed sporulation behaviour. J Gen Microbiol 139:865–871

    Article  CAS  Google Scholar 

  • Gutierrez-Luna FM, Lopez.-Bucio J, Altamirano-Hernandez J, Valencia-Cantero E, Reyes de la Cruz H, Macias-Rodriquez L (2010) Plant growth-promoting rhizobacteria modulate root-system architecture in Arabidopsis thaliana through volatile organic compound emission. Symbiosis 51:75–83

    Article  CAS  Google Scholar 

  • Hartwig T, Corvalan C, Best NB, Budka JS, Zhu JY, Choe S, Schulz B (2012) Propiconazole is a specific and accessible brassinosteroid (BR) biosynthesis inhibitor for Arabidopsis and maize. PLoS One 7:e36625

  • Hirakawa H, Inazumi Y, Masaki T, Hirata T, Yamaguchi A (2005) Indole induces the expression of multidrug exporter genes in Escherichia coli. Mol Microbiol 55:1113–1126

    Article  CAS  PubMed  Google Scholar 

  • Hirakawa H, Kodama T, Takumi-Kobayashi A, Honda T, Yamaguchi A (2009) Secreted indole serves as a signal for expression of type III secretion system translocators in enterohaemorrhagic Escherichia coli O157:H7. Microbiology 155:541–550

    Article  CAS  PubMed  Google Scholar 

  • Inoue T, Higuchi M, Hashimoto Y, Seki M, Kobayashi M, Kato T et al (2001) Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409:1060–1063

    Article  CAS  PubMed  Google Scholar 

  • Ishida Y, Nakamura A, Mitani Y, Suzuki M, Soeno K, Asami T, Shimada Y (2013) Comparison of indole derivatives as potential intermediates of auxin biosynthesis in Arabidopsis. Plant Biotechnol 30:185–190

    Article  CAS  Google Scholar 

  • Ishii T, Soeno K, Asami T, Fujioka S, Shimada Y (2010) Arabidopsis seedlings overaccumulated indole-3-acetic acid in response to aminooxyacetic acid. Biosci Bitotechnol Biochem 74:2345–2347

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kauschmann A, Jessop A, Koncz C, Szekeres M, Willmitzer L, Altmann T (1996) Genetic evidence for an essential role of brassinosteroids in plant development. Plant J 9:701–713

    Article  CAS  Google Scholar 

  • Kitahata N, Saito S, Miyazawa Y, Umezawa T, Shimada Y, Min YK et al (2005) Chemical regulation of abscisic acid catabolism in plants by cytochrome P450 inhibitors. Bioorg Med Chem 13:4491–4498

    Article  CAS  PubMed  Google Scholar 

  • Kong Y, Zhu Y, Gao C, She W, Lin W, Chen Y, Han N, Bian H, Zhu M, Wang J (2013) Tissue-specific expression of SMALL AUXIN UP RNA41 differentially regulates cell expansion and root meristem patterning in Arabidopsis. Plant Cell Physiol 54:609–621

  • Koorneef M, Elgersma A, Hanhart CJ, van Loenen-Martinet EP, van Rijn L, Zeevaart JAD (1985) A gibberellin insensitive mutant of Arabidopsis thaliana. Physiol Plant 65:33–39

    Article  Google Scholar 

  • Lee HH, Molla MN, Cantor CR, Collins JJ (2010) Bacterial charity work leads to population-wide resistance. Nature 467:82–86

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lopez-Bucio J, Campos-Cuevas JC, Hernandez-Calderon E, Velasquez-Becerra C, Farias-Rodriguez R, Macias-Rodriguez LI, Valencia-Cantero E (2007) Bacillus megaterium rhizobacteria promote growth and alter root-system architecture through an auxin- and ethylene-independent signaling mechanism in Arabidopsis thaliana. Mol Plant Microbe Interact 20:207–217

    Article  CAS  PubMed  Google Scholar 

  • Lugtenberg BJ, Chin AWTF, Bloemberg GV (2002) Microbe-plant interactions: principles and mechanisms. Antonie Van Leeuwenhoek 81:373–383

    Article  CAS  PubMed  Google Scholar 

  • Luschnig C, Gaxiola RA, Grisafi P, Fink GR (1998) EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev 12:2175–2187

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Martino PD, Fursy R, Bret L, Sundararaju B, Phillips RS (2003) Indole can act as an extracellular signal to regulate biofilm formation of Escherichia coli and other indole-producing bacteria. Can J Microbiol 49:443–449

    Article  PubMed  Google Scholar 

  • Mitchum MG, Yamaguchi S, Hanada A, Kuwahara A, Yoshioka Y, Kato T, Tabata S, Kamiya Y, Sun TP (2006) Distinct and overlapping roles of two gibberellin 3-oxidases in Arabidopsis development. Plant J 45:804–818

  • Mueller RS, McDougald D, Cusumano D, Sodhi N, Kjelleberg S, Azam F, Bartlett DH (2007) Vibrio cholerae strains possess multiple strategies for abiotic and biotic surface colonization. J Bacteriol 189:5348–5360

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Negi S, Ivanchenko MG, Muday GK (2008) Ethylene regulates lateral root formation and auxin transport in Arabidopsis thaliana. Plant J 55:175–187

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nishimura C, Ohashi Y, Sato S, Kato T, Tabata S, Ueguchi C (2004) Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell 16:1365–1377

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ortiz-Castro R, Contreras-Cornejo HA, Macias-Rodriguez L, Lopez-Bucio J (2009) The role of microbial signals in plant growth and development. Plant Signal Behav 4:701–712

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rademacher W (2000) Growth Retardants: Effects on gibberellin biosynthesis and other metabolic pathways. Annu Rev Plant Physiol Plant Mol Biol 51:501–531

  • Raj SN, Shetty HS, Reddy MS (2006) Plant growth promoting rhizobacteria: potential green alternative for plant productivity. In: Siddiqui ZA (ed) PGPR: biocontrol and biofertilization. Springer, Netherlands, pp 197–216

    Google Scholar 

  • Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Pare PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci USA 100:4927–4932

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Pare PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ryu CM, Hu CH, Locy RD, Kloepper JW (2005) Study of mechanisms for plant growth promotion elicited by rhizobacteria in Arabidopsis thaliana. Plant Soil 268:285–292

    Article  CAS  Google Scholar 

  • Santoro MV, Zygadlo J, Giordano W, Banchio E (2011) Volatile organic compounds from rhizobacteria increase biosynthesis of essential oils and growth parameters in peppermint (Mentha piperita). Plant Physiol Biochem 49:1177–1182

    Article  CAS  PubMed  Google Scholar 

  • Schmittgen TD, Zakrajsek BA, Mills AG, Gorn V, Singer MJ, Reed MW (2000) Quantitative reverse transcription–polymerase chain reaction to study mRNA decay: comparison of endpoint and real-time methods. Anal Biochem 285:194–204

    Article  CAS  PubMed  Google Scholar 

  • Shimada Y, Goda H, Nakamura A, Takatsuto S, Fujioka S, Yoshida S (2003) Organ-specific expression of brassinosteroid-biosynthetic genes and distribution of endogenous brassinosteroids in Arabidopsis. Plant Physiol 131:287–297

  • Smith T (1897) A modification of the method for determining the production of indole by bacteria. J Exp Med 2:543–547

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Soeno K, Goda H, Ishii T, Ogura T, Tachikawa T, Sasaki E, Yoshida S, Fujioka S, Asami T, Yukihisa S (2010) Auxin biosynthesis inhibitors, identified by a genomics-based approach, provide insights into auxin biosynthesis. Plant Cell Physiol 51:524–536

    Article  CAS  PubMed  Google Scholar 

  • Tran LS, Urao T, Qin F, Maruyama K, Kakimoto T, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl Acad Sci USA 104:20623–20628

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Van Loon LC (2007) Plant responses to plant growth-promoting rhizobacteria. Eur J Plant Pathol 119:243–254

    Article  Google Scholar 

  • Wang D, Ding X, Rather PN (2001) Indole can act as an extracellular signal in Escherichia coli. J Bacteriol 183:4210–4216

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang H, Liang X, Huang J, Zhang D, Lu H, Liu Z, Bi Y (2010) Involvement of ethylene and hydrogen peroxide in induction of alternative respiratory pathway in salt-treated Arabidopsis calluses. Plant Cell Physiol 51:1754–1765

    Article  CAS  PubMed  Google Scholar 

  • Wheatley RE (2002) The consequences of volatile organic compound mediated bacterial and fungal interactions. Antonie Van Leeuwenhoek 81:357–364

    Article  CAS  PubMed  Google Scholar 

  • Yamagami T, Tsuchisaka A, Yamada K, Haddon WF, Harden LA, Theologis A (2003) Biochemical diversity among the 1-amino-cyclopropane-1-carboxylate synthase isozymes encoded by the Arabidopsis gene family. J Biol Chem 278:49102–49112

    Article  CAS  PubMed  Google Scholar 

  • Yu SM, Lee YH (2013) Plant growth promoting rhizobacterium Proteus vulgaris JBLS202 stimulates the seedling growth of Chinese cabbage through indole emission. Plant Soil 370:485–495

    Article  CAS  Google Scholar 

  • Zamioudis C, Mastranesti P, Dhonukshe P, Blilou I, Pieterse CM (2013) Unraveling root developmental programs initiated by beneficial Pseudomonas spp. bacteria. Plant Physiol 162:304–318

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang H, Kim MS, Krishnamachari V, Payton P, Sun Y, Grimson M et al (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226:839–851

    Article  CAS  PubMed  Google Scholar 

  • Zou CS, Mo MH, Gu YQ, Zhou JP, Zhang KQ (2007) Possible contributions of volatile-producing bacteria to soil fungistasis. Soil Biol Biochem 39:2371–2379

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank the two anonymous referees for their constructive comments and corrections. We gratefully acknowledge a Grant from the Basic Research Laboratory Program (2011-0020202) and Basic Science Research program (2014R1A1A4A01003957) through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yong Hoon Lee.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 2924 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bhattacharyya, D., Garladinne, M. & Lee, Y.H. Volatile Indole Produced by Rhizobacterium Proteus vulgaris JBLS202 Stimulates Growth of Arabidopsis thaliana Through Auxin, Cytokinin, and Brassinosteroid Pathways. J Plant Growth Regul 34, 158–168 (2015). https://doi.org/10.1007/s00344-014-9453-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-014-9453-x

Keywords

Navigation