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

Journal of Plant Growth Regulation

Volumn 34, Issue 1, 2015, Pages 158-168

  Bhattacharyya, Dipto ^a   Garladinne, Mallikarjuna ^a   Lee, Yong Hoon ^a  

^a Chonbuk National University   (South Korea)

Author keywords

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

Indexed keywords

EID: 84925486968     PISSN: 07217595     EISSN: 14358107     Source Type: Journal    
DOI: 10.1007/s00344-014-9453-x     Document Type: Article

References (52)

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 13:3047–3058
2. Boller T, Herner RC, Kende H (1979) Assay for and enzymatic formation of an ethylene precursor, 1-aminocyclopropane-1-carboxylic acid. Planta 145:293–303
3. Chang C, Kwok SF, Bleecker AB, Meyerowitz EM (1993) Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262:539–544
4. Chant EL, Summers DK (2007) Indole signalling contributes to the stable maintenance of Escherichia coli multicopy plasmids. Mol Microbiol 63:35–43
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 64:1565–1573
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 21:1067–1075
7. Effmert U, Kalderas J, Warnke R, Piechulla B (2012) Volatile mediated interactions between bacteria and fungi in the soil. J Chem Ecol 38:665–703
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 69:6083–6091
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 67:2262–2268
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 139:865–871
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 51:75–83
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:e36625
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 55:1113–1126
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 155:541–550
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 409:1060–1063
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 30:185–190
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 74:2345–2347
18. Kai M, Haustein M, Molina F, Petri A, Scholz B, Piechulla B (2009) Bacterial volatiles and their action potential. Appl Microbiol Biotechnol 81:1001–1012
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 9:701–713
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 13:4491–4498
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 54:609–621
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 65:33–39
23. Lee HH, Molla MN, Cantor CR, Collins JJ (2010) Bacterial charity work leads to population-wide resistance. Nature 467:82–86
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 20:207–217
25. Lugtenberg BJ, Chin AWTF, Bloemberg GV (2002) Microbe-plant interactions: principles and mechanisms. Antonie Van Leeuwenhoek 81:373–383
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 12:2175–2187
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 49:443–449
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 45:804–818
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 189:5348–5360
30. Negi S, Ivanchenko MG, Muday GK (2008) Ethylene regulates lateral root formation and auxin transport in Arabidopsis thaliana. Plant J 55:175–187
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 16:1365–1377
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 4:701–712
33. Rademacher W (2000) Growth Retardants: Effects on gibberellin biosynthesis and other metabolic pathways. Annu Rev Plant Physiol Plant Mol Biol 51:501–531
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 197–216
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 100:4927–4932
36. Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Pare PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026
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 268:285–292
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 49:1177–1182
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 285:194–204
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 131:287–297
41. Smith T (1897) A modification of the method for determining the production of indole by bacteria. J Exp Med 2:543–547
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 51:524–536
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 104:20623–20628
44. Van Loon LC (2007) Plant responses to plant growth-promoting rhizobacteria. Eur J Plant Pathol 119:243–254
45. Wang D, Ding X, Rather PN (2001) Indole can act as an extracellular signal in Escherichia coli. J Bacteriol 183:4210–4216
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 51:1754–1765
47. Wheatley RE (2002) The consequences of volatile organic compound mediated bacterial and fungal interactions. Antonie Van Leeuwenhoek 81:357–364
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 278:49102–49112
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 370:485–495
50. Zamioudis C, Mastranesti P, Dhonukshe P, Blilou I, Pieterse CM (2013) Unraveling root developmental programs initiated by beneficial Pseudomonas spp. bacteria. Plant Physiol 162:304–318
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 226:839–851
52. Zou CS, Mo MH, Gu YQ, Zhou JP, Zhang KQ (2007) Possible contributions of volatile-producing bacteria to soil fungistasis. Soil Biol Biochem 39:2371–2379