Plant and Soil

, Volume 339, Issue 1–2, pp 329–340 | Cite as

A volatile organic compound analysis from Arthrobacter agilis identifies dimethylhexadecylamine, an amino-containing lipid modulating bacterial growth and Medicago sativa morphogenesis in vitro

  • Crisanto Velázquez-Becerra
  • Lourdes Iveth Macías-Rodríguez
  • José López-Bucio
  • Josué Altamirano-Hernández
  • Idolina Flores-Cortez
  • Eduardo Valencia-Cantero
Regular Article


Plant growth promoting rhizobacteria (PGPR) stimulate plant growth and development by different mechanisms, including the production of different classes of signaling molecules, which may directly affect plant morphogenesis. Here, we report the effects of inoculation of Arthrobacter agilis UMCV2, a PGPR isolated from the rhizosphere of maize plants on growth and development of Medicago sativa seedlings. A. agilis UMCV2 inoculation promoted growth in M. sativa plants as revealed by increased stem length, root length and plant biomass. Inoculation of A. agilis using divided Petri plates decreased taproot growth and increased lateral root formation in plants grown in separate compartments suggesting a role of volatile organic compounds (VOCs) produced by this bacterium in root development. The analysis of VOCs produced by A. agilis UMCV2 identified N,N-dimethyl-hexadecanamine (dimethylhexadecylamine), an amino lipid structurally related to bacterial quorum-sensing signals, which modulated A. agilis UMCV2 growth and plant development in a dose-dependent way. Taken together, our results indicate that bacterial VOCs can be perceived by legume plants to modulate growth and morphogenetic processes and identify a novel signaling molecule potentially involved in plant-rhizobacterial interactions.


Legume plants Arthrobacter agilis Dimethylhexadecylamine Root development 



We thank the Consejo Nacional de Ciencia y Tecnología, México (grant 60999) and Coordinación de la Investigación Científica-Universidad Michoacana de San Nicolás de Hidalgo (Grant 2.22) for financial support.

Supplementary material

11104_2010_583_Fig7_ESM.jpg (26 kb)
Supplemental fig. S1

Comparative structure of dimethylhexadecylamine and related compounds that modulate plant development and root architecture in plants. (a) N-dodecanoyl-homoserine lactone from bacteria, (b) N-isobutyl decanamide from plants, and (c) dimethylhexadecylamine from bacteria (JPEG 26 kb)


  1. Arkhipova TN, Veselov SU, Melentiev AI, Martynenko EV, Kudoyarova GR (2005) Ability of bacterium Bacillus subtilis to produce cytokinins and to influence the growth and endogenous hormone content of lettuce plants. Plant Soil 272:201–209. doi: 10.1007/s11104-004-5047-x CrossRefGoogle Scholar
  2. Babana AH, Antoun H (2005) Biological system for improving the availability of tilemsi phosphate rock for wheat (Triticum aestivum L.) cultivated in Mali. Nutr Cycl Agroecosyst 72:147–157. doi: 10.1007/s10705-005-0241-7 CrossRefGoogle Scholar
  3. Badri D, Vivanco J (2009) Regulation and function of root exudates. Plan Cell Environ 32:666–68. doi: 10.1111/j.1365-3040.2009.01926.x CrossRefGoogle Scholar
  4. Batchelor SE, Cooper M, Chhabra SR, Glover LA, Stewart GSAB, Williams P, Prosser JI (1997) Cell density-regulated recovery of starved biofilm populations of ammonia-oxidizing bacteria. Appl Environ Microbiol 63:2281–2286PubMedGoogle Scholar
  5. Bowen GD, Rovira AD (1999) The rhizosphere and its management to improve plant growth. Adv Agron 66:1–102. doi: 10.1016/S0065-2113(08)60425-3 CrossRefGoogle Scholar
  6. Brenic A, Winans S (2005) Detection of and response to signals involved in host-microbe interactions by plant associated bacteria. Microbiol Mol Biol Rev 69:155–195. doi: 10.1128/MMBR.69.1.155-194.2005 CrossRefGoogle Scholar
  7. Camilli A, Bassler BL (2006) Bacterial small-molecule signaling pathways. Science 311:1113–1116. doi: 10.1126/science.1121357 CrossRefPubMedGoogle Scholar
  8. Campbell R, Greaves MP (1990) Anatomy and community structure of the rhizosphere. In: Lynch JM (ed) The Rhizosphere. Wiley, Chichester, pp 11–34Google Scholar
  9. Farag MA, Ryu CM, 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 CrossRefPubMedGoogle Scholar
  10. Gao MM, Teplitski JB, Robinson JB, Bauer WD (2003) Production of substances by Medicago truncatula that affect bacterial quorum sensing. Mol Plant Microbe Interact 16:827–834. doi: 10.1094/MPMI.2003.16.9.827 CrossRefPubMedGoogle Scholar
  11. Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251:1–7. doi: 10.1016/j.femsle.2005.07.030 CrossRefPubMedGoogle Scholar
  12. Graham PH, Vance CP (2003) Legumes: Importance and constraints to greater use. Plant Physiol 131:872–877. doi: 10.1104/pp.017004 CrossRefPubMedGoogle Scholar
  13. Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant-bacterium signaling processes. Soil Biol Biochem 37:395–412. doi: 10.1016/j.soilbio.2004.08.030 CrossRefGoogle Scholar
  14. Gray MK, Pearson JP, Downie JA, Boboye BE A, Greenberg EP (1996) Cell-to-cell signaling in the symbiotic nitrogen-fixing bacterium Rhizobium leguminosarum: autoinduction of a stationary phase and rhizosphere-expressed genes. J Bacteriol 178:372–376PubMedGoogle Scholar
  15. Gutiérrez-Luna FM, López-Bucio J, Altamirano-Hernández J, Valencia-Cantero E, Reyes de la Cruz H, Macías-Rodríguez L (2010) Plant growth-promoting rhizobacteria modulate root-system architecture in Arabidopsis thaliana through volatile organic compound emission. Symbiosis. doi: 10.1007/s13199-010-0066-2 Google Scholar
  16. 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 CrossRefPubMedGoogle Scholar
  17. Liu W, Wei M, Bingyu Z, Feng L (2008) Antifungal activities and components of VOCs produced by Bacillus subtilis G8. Curr Res Bacteriol 1:28–34CrossRefGoogle Scholar
  18. López-Bucio J, Acevedo-Hernández G, Ramírez-Chávez E, Molina-Torres J, Herrera-Estrella L (2006) Novel signals for plant development. Curr Opin Plant Biol 9:523–9. doi: 10.1016/j.pbi.2006.07.002 CrossRefPubMedGoogle Scholar
  19. López-Bucio J, Campos-Cuevas JC, Hernández-Calderón E, Velásquez-Becerra C, Farías-Rodríguez R, Macías-Rodríguez 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. doi: 10.1094/MPMI-20-2-0207 CrossRefPubMedGoogle Scholar
  20. Mathesius U, Mulders S, Gao M, Teplitski M, Caetano-Anollés G, Rolfe BG, Bauer WD (2003) Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Nat Acad Sci USA 100:1444–1449. doi: 10.1073_pnas.262672599 CrossRefPubMedGoogle Scholar
  21. Nilsson P, Olofsson A, Fagerlind M, Fagerström TE, Rice S, Kjelleberg S, Steinberg P (2001) Kinetics of the AHL regulatory system in a model biofilm system: How many bacteria constitute a “quorum”? J Mol Biol 309:631–640. doi: 10.1006/jmbi.2001.4697 CrossRefPubMedGoogle Scholar
  22. Ortíz-Castro R, Martínez-Trujillo M, López-Bucio J (2008) N-acyl-L-homoserine lactones: a class of bacterial quorum-sensing signals alter post-embryonic root development in Arabidopsis thaliana. Pant Cell Environ 31:1497–1509. doi: 10.1111/j.1365-3040.2008.01863.x CrossRefGoogle Scholar
  23. Ortíz-Castro R, Contreras-Cornejo HA, Macías-Rodríguez L, López-Bucio J (2009) The role of microbial signals in plant growth and development. Plant Signal Behav 4:701–712CrossRefPubMedGoogle Scholar
  24. Patten CL, Glick BR (2002) Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Appl Environ Microbiol 68:3795–3801. doi: 10.1128/AEM.68.8.3795-3801.2002 CrossRefPubMedGoogle Scholar
  25. Persello-Cartieaux F, David P, Sarrobert C, Thibaud MC, Robaglia C, Nussaume L (2001) Utilization of mutants to analyze the interaction between Arabidopsis thaliana and its naturally root-associated Pseudomonas. Planta 212:190–198. doi: 10.1007/s004250000384 CrossRefPubMedGoogle Scholar
  26. Persello-Cartieaux F, Nussaume L, Robaglia C (2003) Tales from the underground: Molecular plant-rhizobacteria interactions. Plant Cell Environ 26:189–199. doi: 10.1046/j.1365-3040.2003.00956.x CrossRefGoogle Scholar
  27. Russelle M (2001) Alfalfa Am Sci 89:252–259. doi: 10.1511/2001.3.252 Google Scholar
  28. 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. doi: 10.1073/pnas.0730845100 CrossRefPubMedGoogle Scholar
  29. Sanchez-Contreras M, Bauer WD, Gao M, Robinson JB, Downie A (2007) Quorum-sensing regulation in rhizobia and its role in symbiotic interactions with legumes. Philos Trans R Soc Lond Biol Sci 362:1149–1163. doi: 10.1098/rstb.2007.2041 CrossRefGoogle Scholar
  30. Teplitski M, Robinson JB, Bauer WD (2000) Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol Plant Microbe Interact 13:637–648. doi: 10.1094/MPMI.2000.13.6.637 CrossRefPubMedGoogle Scholar
  31. Valencia-Cantero E, Hernández-Calderón E, Velázquez-Becerra C, López-Meza LE, Alfaro-Cuevas R, López-Bucio J (2007) Role of dissimilatory fermentative iron-reducing bacteria in Fe uptake by common bean (Phaseolus vulgaris L.) plants grown in alkaline soil. Plant Soil 291:263–273, doi: 10.1007/s11104-007-9191-y CrossRefGoogle Scholar
  32. Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346. doi: 10.1146/annurev.cellbio.21.012704.131001 CrossRefPubMedGoogle Scholar
  33. Williams P, Winzer K, Chan WC, Cámara M (2007) Look who’s talking: communication and quorum sensing in the bacterial world. Philos Trans R Soc Lond Biol Sci 362:1119–1134. doi: 10.1098/rstb.2007.2039 CrossRefGoogle Scholar
  34. Yang S, Gao M, Xu C, Gao J, Deshpande S, Lin S, Roe BA, Zhu H (2008) Alfalfa benefits from Medicago truncatula: The RCT1 gene from M. truncatula confers broad-spectrum resistance to anthracnose in alfalfa. Proc Nat Acad Sci USA 105:12164–12169, doi: 10.1073/pnas.0802518105 CrossRefPubMedGoogle Scholar
  35. Zhang H, Kim MS, Krishnamachari V, Payton P, Sun Y, Grimson M, Farag MA, Ryu CM, Allen R, Melo S, Paré PW (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226:839–851. doi: 10.1007/s00425-007-0530-2 CrossRefPubMedGoogle Scholar
  36. Zhang H, Sun Y, Xie X, Kim MS, Dowd SE, Paré PW (2009) A soil bacterium regulates plant acquisition of iron via deficiency-inducible mechanisms. Plant J 58:568–577. doi: 10.1111/j.1365-313X.2009.03803.x CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Crisanto Velázquez-Becerra
    • 1
  • Lourdes Iveth Macías-Rodríguez
    • 1
  • José López-Bucio
    • 1
  • Josué Altamirano-Hernández
    • 1
  • Idolina Flores-Cortez
    • 1
  • Eduardo Valencia-Cantero
    • 1
  1. 1.Instituto de Investigaciones Químico-BiológicasUniversidad Michoacana de San Nicolás de HidalgoMoreliaMexico

Personalised recommendations