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Plant Molecular Biology

, Volume 90, Issue 6, pp 677–687 | Cite as

Sweet scents from good bacteria: Case studies on bacterial volatile compounds for plant growth and immunity

  • Joon-hui Chung
  • Geun Cheol Song
  • Choong-Min RyuEmail author
Article

Abstract

Beneficial bacteria produce diverse chemical compounds that affect the behavior of other organisms including plants. Bacterial volatile compounds (BVCs) contribute to triggering plant immunity and promoting plant growth. Previous studies investigated changes in plant physiology caused by in vitro application of the identified volatile compounds or the BVC-emitting bacteria. This review collates new information on BVC-mediated plant-bacteria airborne interactions, addresses unresolved questions about the biological relevance of BVCs, and summarizes data on recently identified BVCs that improve plant growth or protection. Recent explorations of bacterial metabolic engineering to alter BVC production using heterologous or endogenous genes are introduced. Molecular genetic approaches can expand the BVC repertoire of beneficial bacteria to target additional beneficial effects, or simply boost the production level of naturally occurring BVCs. The effects of direct BVC application in soil are reviewed and evaluated for potential large-scale field and agricultural applications. Our review of recent BVC data indicates that BVCs have great potential to serve as effective biostimulants and bioprotectants even under open-field conditions.

Keywords

Bacterial volatile compound 2,3-butanediol Induced systemic resistance Plant growth-promoting rhizobacteria Metabolic engineering 

Notes

Acknowledgments

This research was supported by grants from BioNano Health-Guard Research Center funded by the Ministry of Science, ICT, and Future Planning of Korea as a Global Frontier Project (Grant H-GUARD_2013M3A6B2078953), Cooperative Research Program for Agriculture Science & Technology Development (Project No. PJ01093904) Rural Development Administration (RDA), and from the KRIBB initiative program, South Korea.

References

  1. Atsumi S et al (2008) Metabolic engineering of Escherichia coli for 1-butanol production. Metab Eng 10:305–311. doi: 10.1016/j.ymben.2007.08.003 CrossRefPubMedGoogle Scholar
  2. Audrain B, Farag MA, Ryu CM, Ghigo JM (2015) Role of bacterial volatile compounds in bacterial biology. FEMS Microbiol Rev 39:222–233. doi: 10.1093/femsre/fuu013 CrossRefPubMedGoogle Scholar
  3. Bai F, Dai L, Fan J, Truong N, Rao B, Zhang L, Shen Y (2015) Engineered Serratia marcescens for efficient (3R)-acetoin and (2R,3R)-2,3-butanediol production. J Ind Microbiol Biotechnol 42:779–786. doi: 10.1007/s10295-015-1598-5 CrossRefPubMedGoogle Scholar
  4. Bailly A, Weisskopf L (2012) The modulating effect of bacterial volatiles on plant growth: current knowledge and future challenges. Plant Signal Behav 7:79–85. doi: 10.4161/psb.7.1.18418 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bailly A, Groenhagen U, Schulz S, Geisler M, Eberl L, Weisskopf L (2014) The inter-kingdom volatile signal indole promotes root development by interfering with auxin signalling. Plant J 80:758–771. doi: 10.1111/tpj.12666 CrossRefPubMedGoogle Scholar
  6. Bengtsson JM et al (2009) Field attractants for Pachnoda interrupta selected by means of GC-EAD and single sensillum screening. J Chem Ecol 35:1063–1076. doi: 10.1007/s10886-009-9684-7 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Berendsen R, Kalkhove SC, Lugones L, Baars JP, Wösten HB, Bakker PHM (2013) Effects of the mushroom-volatile 1-octen-3-ol on dry bubble disease. Appl Microbiol Biotechnol 97:5535–5543. doi: 10.1007/s00253-013-4793-1 CrossRefPubMedGoogle Scholar
  8. Bernier SP, Letoffe S, Delepierre M, Ghigo JM (2011) Biogenic ammonia modifies antibiotic resistance at a distance in physically separated bacteria. Mol Microbiol 81:705–716. doi: 10.1111/j.1365-2958.2011.07724.x CrossRefPubMedGoogle Scholar
  9. Bitas V, Kim HS, Bennett JW, Kang S (2013) Sniffing on microbes: diverse roles of microbial volatile organic compounds in plant health. Mol Plant Microbe Interact 26:835–843. doi: 10.1094/MPMI-10-12-0249-CR CrossRefPubMedGoogle Scholar
  10. Blom D, Fabbri C, Eberl L, Weisskopf L (2011) 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 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Börjesson T, Stöllman U, Schnürer J (1992) Volatile metabolites produced by six fungal species compared with other indicators of fungal growth on cereal grains. Appl Environ Microbiol 58:2599–2605PubMedPubMedCentralGoogle Scholar
  12. Broberg M, Lee GW, Nykyri J, Lee YH, Pirhonen M, Palva ET (2014) The global response regulator ExpA controls virulence gene expression through RsmA-mediated and RsmA-independent pathways in Pectobacterium wasabiae SCC3193. Appl Environ Microbiol 80:1972–1984. doi: 10.1128/AEM.03829-13 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Buttery RGKJ, Ling LC (1984) Volatile components of red clover leaves, flowers, and seed pods: possible insect attractants. J Agric Food Chem 32:254–256CrossRefGoogle Scholar
  14. Celinska E, Grajek W (2009) Biotechnological production of 2,3-butanediol–current state and prospects. Biotechnol Adv 27:715–725. doi: 10.1016/j.biotechadv.2009.05.002 CrossRefPubMedGoogle Scholar
  15. Cho SM, Kang BR, Han SH, Anderson AJ, Park JY, Lee YH, Cho BH, Yang KY, Ryu CM, Kim YC (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(8):1067–1075. doi:  10.1094/MPMI-21-8-1067 CrossRefPubMedGoogle Scholar
  16. Choi HK, Song GC, Yi HS, Ryu CM (2014) Field evaluation of the bacterial volatile derivative 3-pentanol in priming for induced resistance in pepper. J Chem Ecol 40:882–892. doi: 10.1007/s10886-014-0488-z CrossRefPubMedGoogle Scholar
  17. Cortes-Barco AM, Hsiang T, Goodwin PH (2010a) Induced systemic resistance against three foliar diseases of Agrostis stolonifera by (2R,3R)-butanediol or an isoparaffin mixture. Ann Appl Biol 157:179–189CrossRefGoogle Scholar
  18. Cortes-Barco AM, Goodwin PH, Hsiang T (2010b) Comparison of induced resistance activated by benzothiadiazole, (2R,3R)-butanediol and an isoparaffin mixture against anthracnose of Nicotiana benthamiana. Plant Pathol 59:643–653CrossRefGoogle Scholar
  19. D’Alessandro M, Erb M, Ton J, Brandenburg A, Karlen D, Zopfi J, Turlings TC (2014) Volatiles produced by soil-borne endophytic bacteria increase plant pathogen resistance and affect tritrophic interactions. Plant, Cell Environ 37:813–826. doi: 10.1111/pce.12220 CrossRefGoogle Scholar
  20. Effantin G, Rivasseau C, Gromova M, Bligny R, Hugouvieux-Cotte-Pattat N (2011) Massive production of butanediol during plant infection by phytopathogenic bacteria of the genera Dickeya and Pectobacterium. Mol Microbiol 82:988–997. doi: 10.1111/j.1365-2958.2011.07881.x CrossRefPubMedGoogle Scholar
  21. 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. doi: 10.1007/s10886-012-0135-5 CrossRefPubMedGoogle Scholar
  22. Erb M, Veyrat N, Robert CAM, Xu H, Frey M, Ton J, Turlings TCJ (2015) Indole is an essential herbivore-induced volatile priming signal in maize. Nat Commun 6:6273. doi: 10.1038/ncomms7273 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 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. doi: 10.1016/j.phytochem.2006.07.021 CrossRefPubMedGoogle Scholar
  24. Farag MA, Zhang H, Ryu CM (2013) Dynamic chemical communication between plants and bacteria through airborne signals: induced resistance by bacterial volatiles. J Chem Ecol 39:1007–1018. doi: 10.1007/s10886-013-0317-9 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Garg SK, Jain A (1995) Fermentative production of 2,3-butanediol: a review. Bioresour Technol 51:103–109. doi: 10.1016/0960-8524(94)00136-O CrossRefGoogle Scholar
  26. Gutiérrez-Luna F, López-Bucio J, Altamirano-Hernández J, Valencia-Cantero E, 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 51:75–83. doi: 10.1007/s13199-010-0066-2 CrossRefGoogle Scholar
  27. Hahm MS et al (2012) Biological control and plant growth promoting capacity of rhizobacteria on pepper under greenhouse and field conditions. J Microbiol 50:380–385. doi: 10.1007/s12275-012-1477-y CrossRefPubMedGoogle Scholar
  28. Han SH, Lee SJ, Moon JH, Park KH, Yang KY, Cho BH, Kim KY, Kim YW, Lee MC, Anderson AJ, Kim YC (2006) GacS-dependent production of 2R, 3R-butanediol by Pseudomonas chlororaphis O6 is a major determinant for eliciting systemic resistance against Erwinia carotovora but not against Pseudomonas syringae pv. tabaci in tobacco. Mol Plant Microbe Interact 19:924–930. doi: 10.1094/mpmi-19-0924 CrossRefPubMedGoogle Scholar
  29. Hsieh SC, Lu CC, Horng YT, Soo PC, Chang YL, Tsai YH, Lin CS, Lai HC (2007) The bacterial metabolite 2,3-butanediol ameliorates endotoxin-induced acute lung injury in rats. Microbes Infect 9:1402–1409. doi: 10.1016/j.micinf.2007.07.004 CrossRefPubMedGoogle Scholar
  30. Huang CJ, Tsay JF, Chang SY, Yang HP, Wu WS, Chen CY (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 CrossRefPubMedGoogle Scholar
  31. Ji XJ, Huang H, Zhu JG, Ren LJ, Nie ZK, Du J, Li S (2010) Engineering Klebsiella oxytoca for efficient 2,3-butanediol production through insertional inactivation of acetaldehyde dehydrogenase gene. Appl Microbiol Biotechnol 85:1751–1758. doi: 10.1007/s00253-009-2222-2 CrossRefPubMedGoogle Scholar
  32. Ji XJ, Nie ZK, Huang H, Ren LJ, Peng C, Ouyang PK (2011) Elimination of carbon catabolite repression in Klebsiella oxytoca for efficient 2,3-butanediol production from glucose-xylose mixtures. Appl Microbiol Biotechnol 89:1119–1125. doi: 10.1007/s00253-010-2940-5 CrossRefPubMedGoogle Scholar
  33. Ji XJ, Liu LG, Shen MQ, Nie ZK, Tong YJ, Huang H (2014) Constructing a synthetic metabolic pathway in Escherichia coli to produce the enantiomerically pure (R,R)-2,3-butanediol. Biotechnol Bioeng 112:1056–1059. doi: 10.1002/bit.25512 CrossRefGoogle Scholar
  34. Kai M, Piechulla B (2009) Plant growth promotion due to rhizobacterial volatiles—An effect of CO2? FEBS Lett 583:3473–3477. doi: 10.1016/j.febslet.2009.09.053 CrossRefPubMedGoogle Scholar
  35. Kanchiswamy CN, Malnoy M, Maffei ME (2015) Bioprospecting bacterial and fungal volatiles for sustainable agriculture. Trends Plant Sci 20:206–211. doi: 10.1016/j.tplants.2015.01.004 CrossRefPubMedGoogle Scholar
  36. Kappers IF, Verstappen FW, Luckerhoff LL, Bouwmeester HJ, Dicke M (2010) Genetic variation in jasmonic acid- and spider mite-induced plant volatile emission of cucumber accessions and attraction of the predator Phytoseiulus persimilis. J Chem Ecol 36:500–512. doi: 10.1007/s10886-010-9782-6 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2007) Volatile 1-octen-3-ol induces a defensive response in Arabidopsis thaliana. J Gen Plant Pathol 73:35–37. doi: 10.1007/s10327-006-0314-8 CrossRefGoogle Scholar
  38. Kõiv V et al (2013) Lack of RsmA-mediated control results in constant hypervirulence, cell elongation, and hyperflagellation in Pectobacterium wasabiae. PLoS ONE 8:e54248. doi: 10.1371/journal.pone.0054248 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Kwan G, Charkowski AO, Barak JD (2013) Salmonella enterica suppresses Pectobacterium carotovorum subsp. carotovorum population and soft rot progression by acidifying the microaerophilic environment. MBio 4:e00512–e00557. doi: 10.1128/mBio.00557-12 CrossRefGoogle Scholar
  40. Lee JH, Lee J (2010) Indole as an intercellular signal in microbial communities. FEMS Microbiol Rev 34:426–444. doi: 10.1111/j.1574-6976.2009.00204.x CrossRefPubMedGoogle Scholar
  41. Lee B, Farag MA, Park HB, Kloepper JW, Lee SH, Ryu CM (2012) Induced resistance by a long-chain bacterial volatile: elicitation of plant systemic defense by a C13 volatile produced by Paenibacillus polymyxa. PLoS ONE 7:e48744. doi: 10.1371/journal.pone.0048744 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Li J, Wang W, Ma Y, Zeng AP (2013) Medium optimization and proteome analysis of (R,R)-2,3-butanediol production by Paenibacillus polymyxa ATCC 12321. Appl Microbiol Biotechnol 97:585–597. doi: 10.1007/s00253-012-4331-6 CrossRefPubMedGoogle Scholar
  43. Li L, Wang Y, Li K, Su F, Ma C, Xu P (2014) Genome sequence of meso-2,3-butanediol-producing strain Serratia marcescens ATCC 14041. Genome Announc. 2(3):e00590. doi: 10.1128/genomeA.00590-14 PubMedPubMedCentralGoogle Scholar
  44. Li L, Li K, Wang Y, Chen C, Xu Y, Zhang L, Han B, Gao C, Tao F, Ma C, Xu P (2015) Metabolic engineering of Enterobacter cloacae for high-yield production of enantiopure (2R,3R)-2,3-butanediol from lignocellulose-derived sugars. Metab Eng 28:19–27. doi: 10.1016/j.ymben.2014.11.010 CrossRefPubMedGoogle Scholar
  45. Marquez-Villavicencio MdP, Weber B, Witherell RA, Willis DK, Charkowski AO (2011) The 3-Hydroxy-2-Butanone Pathway Is Required for Pectobacterium carotovorum Pathogenesis. PLoS ONE 6(8):e22974. doi: 10.1371/journal.pone.0022974 CrossRefPubMedCentralGoogle Scholar
  46. Meldau DG, Meldau S, Hoang LH, Underberg S, Wunsche H, Baldwin IT (2013) Dimethyl disulfide produced by the naturally associated bacterium bacillus sp. B55 promotes Nicotiana attenuata growth by enhancing sulfur nutrition. Plant Cell 25:2731–2747. doi: 10.1105/tpc.113.114744 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Mercke P, Kappers IF, Verstappen FW, Vorst O, Dicke M, Bouwmeester HJ (2004) Combined transcript and metabolite analysis reveals genes involved in spider mite induced volatile formation in cucumber plants. Plant Physiol 135:2012–2024. doi: 10.1104/pp.104.048116 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Moons P, van Houdt R, Vivijs B, Michiels CW, Aertsen A (2011) Integrated regulation of acetoin fermentation by quorum sensing and pH in Serratia plymuthica RVH1. Appl Environ Microbiol 77:3422–3427. doi: 10.1128/AEM.02763-10 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Moore AJ, Moore PJ (1999) Balancing sexual selection through opposing mate choice and male competition. Proc R Soc Lond B Biol Sci 266:711–716CrossRefGoogle Scholar
  50. Moore AJ, Haynes KF, Preziosi RF, Moore PJ (2002) The evolution of interacting phenotypes: genetics and evolution of social dominance. Am Nat 160(Suppl 6):S186–S197. doi: 10.1086/342899 CrossRefPubMedGoogle Scholar
  51. Nielsen DR, Yoon SH, Yuan CJ, Prather KL (2010) Metabolic engineering of acetoin and meso-2,3-butanediol biosynthesis in E. coli. Biotechnol J 5:274–284. doi: 10.1002/biot.200900279 CrossRefPubMedGoogle Scholar
  52. Nout MJR, Bartelt RJ (1998) Attraction of a flying nitidulid (Carpophilus humeralis) to volatiles produced by yeasts grown on sweet corn and a corn-based medium. J Chem Ecol 24:1217–1239CrossRefGoogle Scholar
  53. Okubara P, Paulitz T (2005) Root defense responses to fungal pathogens: a molecular perspective. In: Lambers H, Colmer T (eds) Root physiology: from gene to function, vol 4., Plant EcophysiologySpringer, Netherlands, pp 215–226. doi: 10.1007/1-4020-4099-7_11 CrossRefGoogle Scholar
  54. Oliver JW, Machado IM, Yoneda H, Atsumi S (2013) Cyanobacterial conversion of carbon dioxide to 2,3-butanediol. Proc Natl Acad Sci USA 110:1249–1254. doi: 10.1073/pnas.1213024110 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Peralta-Yahya PP, Keasling JD (2010) Advanced biofuel production in microbes. Biotechnol J 5:147–162. doi: 10.1002/biot.200900220 CrossRefPubMedGoogle Scholar
  56. Rao B, Zhang LY, Sun J, Su G, Wei D, Chu J, Zhu J, Shen Y (2012) Characterization and regulation of the 2,3-butanediol pathway in Serratia marcescens. Appl Microbiol Biotechnol 93:2147–2159. doi: 10.1007/s00253-011-3608-5 CrossRefPubMedGoogle Scholar
  57. Renna MC, Najimudin N, Winik LR, Zahler SA (1993) Regulation of the Bacillus subtilis alsS, alsD, and alsR genes involved in post-exponential-phase production of acetoin. J Bacteriol 175:3863–3875PubMedPubMedCentralGoogle Scholar
  58. Robacker DC, Lauzon CR (2002) Purine metabolizing capability of Enterobacter agglomerans affects volatiles production and attractiveness to Mexican fruit fly. J Chem Ecol 28:1549–1563CrossRefPubMedGoogle Scholar
  59. Rochat D, Morin JP, Kakul T, Beaudoin-Ollivier L, Prior R, Renou M, Malosse I, Stathers T, Embupa S, Laup S (2002) Activity of male pheromone of Melanesian rhinoceros beetle Scapanes australis. J Chem Ecol 28:479–500CrossRefPubMedGoogle Scholar
  60. Rudrappa T, Biedrzycki ML, Kunjeti SG, Donofrio NM, Czymmek KJ, Pare PW, Bais HP (2010) The rhizobacterial elicitor acetoin induces systemic resistance in Arabidopsis thaliana. Commun Integr Biol 3:130–138CrossRefPubMedPubMedCentralGoogle Scholar
  61. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Pare PW (2004a) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026. doi: 10.1104/pp.103.026583 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Ryu CM, Murphy JF, Mysore KS, Kloepper JW (2004b) Plant growth-promoting rhizobacteria systemically protect Arabidopsis thaliana against Cucumber mosaic virus by a salicylic acid and NPR1-independent and jasmonic acid-dependent signaling pathway. Plant J 39:381–392. doi: 10.1111/j.1365-313X.2004.02142.x CrossRefPubMedGoogle Scholar
  64. Ryu CM, Hu C-H, Locy R, Kloepper J (2005a) 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 CrossRefGoogle Scholar
  65. Ryu CM, Farag MA, Paré PW, Kloepper JW (2005b) Invisible signals from the underground: bacterial volatiles elicit plant growth promotion and induce systemic resistance. Plant Pathol J 21:7–12CrossRefGoogle Scholar
  66. Ryu CM, Choi HK, Lee CH, Murphy JF, Lee JK, Kloepper JW (2013) Modulation of quorum sensing in acylhomoserine lactone-producing or -degrading tobacco plants leads to alteration of induced systemic resistance elicited by the rhizobacterium Serratia marcescens 90-166. Plant Pathol J 29:182–192. doi: 10.5423/PPJ.SI.11.2012.0173.R2 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Song GC, Ryu CM (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. doi: 10.3390/ijms14059803 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Ton J, D’Alessandro M, Jourdie V, Jakab G, Karlen D, Held M, Mauch-Mani B, Turlings TC (2007) Priming by airborne signals boosts direct and indirect resistance in maize. Plant J 49:16–26. doi: 10.1111/j.1365-313X.2006.02935.x CrossRefPubMedGoogle Scholar
  69. Ui S, Okajima Y, Mimura A, Kanai H, Kudo T (1997) Molecular generation of an Escherichia coli strain producing only the meso-isomer of 2,3-butanediol. J Ferment Bioeng 84:185–189. doi: 10.1016/S0922-338X(97)82052-1 CrossRefGoogle Scholar
  70. Velázquez-Becerra C, Macías-Rodríguez LI, López-Bucio J, Altamirano-Hernández J, Flores-Cortez I, Valencia-Cantero E (2010) 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 CrossRefGoogle Scholar
  71. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Weisskopf L (2013) The potential of bacterial volatiles for crop protection against phytophathogenic fungi. In: Méndez-Vilas A (ed) Microbial pathogens and strategies for combating them: science, technology and education, vol 2. Formatex Research Center, Spain, pp 1352–1363. ISBN: 978-84-942134-0-3Google Scholar
  73. Wevers E, Moons P, van Houdt R, Lurquin I, Aertsen A, Michiels CW (2009) Quorum sensing and butanediol fermentation affect colonization and spoilage of carrot slices by Serratia plymuthica. Int J Food Microbiol 134:63–69. doi: 10.1016/j.ijfoodmicro.2008.12.017 CrossRefPubMedGoogle Scholar
  74. Wheatley RE (2002) The consequences of volatile organic compound mediated bacterial and fungal interactions. Antonie Van Leeuwenhoek 81:357–364CrossRefPubMedGoogle Scholar
  75. Xiao Z, Xu P (2007) Acetoin metabolism in bacteria. Crit Rev Microbiol 33:127–140. doi: 10.1080/10408410701364604 CrossRefPubMedGoogle Scholar
  76. Xu Y, Chang P, Liu D, Narasimhan ML, Raghothama KG, Hasegawa PM, Bressan RA (1994) Plant defense genes are synergistically induced by ethylene and methyl jasmonate. Plant Cell 6:1077–1085. doi: 10.1105/tpc.6.8.1077 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Xu Y, Chu H, Gao C, Tao F, Zhou Z, Li K, Li L, Ma C, Xu P (2014) Systematic metabolic engineering of Escherichia coli for high-yield production of fuel bio-chemical 2,3-butanediol. Metab Eng 23:22–33. doi: 10.1016/j.ymben.2014.02.004 CrossRefPubMedGoogle Scholar
  78. Yang T, Rao Z, Zhang X, Xu M, Xu Z, Yang S-T (2013) Improved production of 2,3-butanediol in Bacillus amyloliquefaciens by over-expression of glyceraldehyde-3-phosphate dehydrogenase and 2,3-butanediol dehydrogenase. PLoS ONE 8:e76149. doi: 10.1371/journal.pone.0076149 CrossRefPubMedPubMedCentralGoogle Scholar
  79. Yu Q, Tang C, Kuo J (2000) A critical review on methods to measure apoplastic pH in plants. Plant Soil 219:29–40CrossRefGoogle Scholar
  80. Zeng AP, Sabra W (2011) Microbial production of diols as platform chemicals: recent progresses. Curr Opin Biotechnol 22:749–757. doi: 10.1016/j.copbio.2011.05.005 CrossRefPubMedGoogle Scholar
  81. Zhang X et al (2013) Mutation breeding of acetoin high producing Bacillus subtilis blocked in 2,3-butanediol dehydrogenase. World J Microbiol Biotechnol 29:1783–1789. doi: 10.1007/s11274-013-1339-8 CrossRefPubMedGoogle Scholar
  82. 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 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Joon-hui Chung
    • 1
    • 2
  • Geun Cheol Song
    • 1
  • Choong-Min Ryu
    • 1
    • 2
  1. 1.Molecular Phytobactriology LaboratoryKRIBBDaejeonSouth Korea
  2. 2.Biosystems and Bioengineering ProgramUniversity of Science and Technology (UST)Yuseong-gu, DaejeonSouth Korea

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