Journal of Plant Growth Regulation

, Volume 34, Issue 1, pp 158–168 | Cite as

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

  • Dipto Bhattacharyya
  • Mallikarjuna Garladinne
  • Yong Hoon Lee
Article

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 Arabidopsisthaliana 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 (gai1) 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.

Keywords

Growth-promoting rhizobacterium Hormone inhibitor Indole Phytohormone Signaling pathway Volatile organic compound 

Supplementary material

344_2014_9453_MOESM1_ESM.doc (2.9 mb)
Supplementary material 1 (DOC 2924 kb)

References

  1. 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 13:3047–3058CrossRefPubMedGoogle Scholar
  2. Boller T, Herner RC, Kende H (1979) Assay for and enzymatic formation of an ethylene precursor, 1-aminocyclopropane-1-carboxylic acid. Planta 145:293–303CrossRefPubMedGoogle Scholar
  3. Chang C, Kwok SF, Bleecker AB, Meyerowitz EM (1993) Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262:539–544CrossRefPubMedGoogle Scholar
  4. Chant EL, Summers DK (2007) Indole signalling contributes to the stable maintenance of Escherichia coli multicopy plasmids. Mol Microbiol 63:35–43CrossRefPubMedGoogle Scholar
  5. 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 64:1565–1573CrossRefPubMedCentralPubMedGoogle Scholar
  6. 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 21:1067–1075CrossRefPubMedGoogle Scholar
  7. Effmert U, Kalderas J, Warnke R, Piechulla B (2012) Volatile mediated interactions between bacteria and fungi in the soil. J Chem Ecol 38:665–703CrossRefPubMedGoogle Scholar
  8. 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 69:6083–6091CrossRefPubMedCentralPubMedGoogle Scholar
  9. 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 67:2262–2268CrossRefPubMedGoogle Scholar
  10. 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 139:865–871CrossRefGoogle Scholar
  11. 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 51:75–83CrossRefGoogle Scholar
  12. 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:e36625Google Scholar
  13. Hirakawa H, Inazumi Y, Masaki T, Hirata T, Yamaguchi A (2005) Indole induces the expression of multidrug exporter genes in Escherichia coli. Mol Microbiol 55:1113–1126CrossRefPubMedGoogle Scholar
  14. 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 155:541–550CrossRefPubMedGoogle Scholar
  15. 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 409:1060–1063CrossRefPubMedGoogle Scholar
  16. 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 30:185–190CrossRefGoogle Scholar
  17. 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 74:2345–2347CrossRefGoogle Scholar
  18. Kai M, Haustein M, Molina F, Petri A, Scholz B, Piechulla B (2009) Bacterial volatiles and their action potential. Appl Microbiol Biotechnol 81:1001–1012CrossRefPubMedGoogle Scholar
  19. 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 9:701–713CrossRefGoogle Scholar
  20. 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 13:4491–4498CrossRefPubMedGoogle Scholar
  21. 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 54:609–621Google Scholar
  22. 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 65:33–39CrossRefGoogle Scholar
  23. Lee HH, Molla MN, Cantor CR, Collins JJ (2010) Bacterial charity work leads to population-wide resistance. Nature 467:82–86CrossRefPubMedCentralPubMedGoogle Scholar
  24. 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 20:207–217CrossRefPubMedGoogle Scholar
  25. Lugtenberg BJ, Chin AWTF, Bloemberg GV (2002) Microbe-plant interactions: principles and mechanisms. Antonie Van Leeuwenhoek 81:373–383CrossRefPubMedGoogle Scholar
  26. 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 12:2175–2187CrossRefPubMedCentralPubMedGoogle Scholar
  27. 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 49:443–449CrossRefPubMedGoogle Scholar
  28. 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 45:804–818Google Scholar
  29. 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 189:5348–5360CrossRefPubMedCentralPubMedGoogle Scholar
  30. Negi S, Ivanchenko MG, Muday GK (2008) Ethylene regulates lateral root formation and auxin transport in Arabidopsis thaliana. Plant J 55:175–187CrossRefPubMedCentralPubMedGoogle Scholar
  31. 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 16:1365–1377CrossRefPubMedCentralPubMedGoogle Scholar
  32. 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 4:701–712CrossRefPubMedCentralPubMedGoogle Scholar
  33. Rademacher W (2000) Growth Retardants: Effects on gibberellin biosynthesis and other metabolic pathways. Annu Rev Plant Physiol Plant Mol Biol 51:501–531Google Scholar
  34. 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 197–216Google Scholar
  35. 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 100:4927–4932CrossRefPubMedCentralPubMedGoogle Scholar
  36. Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Pare PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026CrossRefPubMedCentralPubMedGoogle Scholar
  37. Ryu CM, Hu CH, Locy RD, Kloepper JW (2005) Study of mechanisms for plant growth promotion elicited by rhizobacteria in Arabidopsis thaliana. Plant Soil 268:285–292CrossRefGoogle Scholar
  38. 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 49:1177–1182CrossRefPubMedGoogle Scholar
  39. 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 285:194–204CrossRefPubMedGoogle Scholar
  40. 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 131:287–297Google Scholar
  41. Smith T (1897) A modification of the method for determining the production of indole by bacteria. J Exp Med 2:543–547CrossRefPubMedCentralPubMedGoogle Scholar
  42. 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 51:524–536CrossRefPubMedGoogle Scholar
  43. 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 104:20623–20628CrossRefPubMedCentralPubMedGoogle Scholar
  44. Van Loon LC (2007) Plant responses to plant growth-promoting rhizobacteria. Eur J Plant Pathol 119:243–254CrossRefGoogle Scholar
  45. Wang D, Ding X, Rather PN (2001) Indole can act as an extracellular signal in Escherichia coli. J Bacteriol 183:4210–4216CrossRefPubMedCentralPubMedGoogle Scholar
  46. 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 51:1754–1765CrossRefPubMedGoogle Scholar
  47. Wheatley RE (2002) The consequences of volatile organic compound mediated bacterial and fungal interactions. Antonie Van Leeuwenhoek 81:357–364CrossRefPubMedGoogle Scholar
  48. 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 278:49102–49112CrossRefPubMedGoogle Scholar
  49. Yu SM, Lee YH (2013) Plant growth promoting rhizobacterium Proteus vulgaris JBLS202 stimulates the seedling growth of Chinese cabbage through indole emission. Plant Soil 370:485–495CrossRefGoogle Scholar
  50. Zamioudis C, Mastranesti P, Dhonukshe P, Blilou I, Pieterse CM (2013) Unraveling root developmental programs initiated by beneficial Pseudomonas spp. bacteria. Plant Physiol 162:304–318CrossRefPubMedCentralPubMedGoogle Scholar
  51. 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 226:839–851CrossRefPubMedGoogle Scholar
  52. Zou CS, Mo MH, Gu YQ, Zhou JP, Zhang KQ (2007) Possible contributions of volatile-producing bacteria to soil fungistasis. Soil Biol Biochem 39:2371–2379CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Dipto Bhattacharyya
    • 1
  • Mallikarjuna Garladinne
    • 1
  • Yong Hoon Lee
    • 1
    • 2
  1. 1.Division of BiotechnologyChonbuk National UniversityIksan-siRepublic of Korea
  2. 2.Advanced Institute of Environment and Bioscience, and Plant Medical Research CenterChonbuk National UniversityIksanRepublic of Korea

Personalised recommendations