The Role of Rhizobacterial Volatile Organic Compounds in a Second Green Revolution—The Story so Far

  • Darren Heenan-Daly
  • Siva L. S. Velivelli
  • Barbara Doyle PrestwichEmail author
Part of the Sustainable Development and Biodiversity book series (SDEB, volume 23)


The role of microbial-emitted volatiles (mVOCs) also termed ‘infochemicals’ in agriculture is an emerging area of research with many perceived attributes including but not limited to the alleviation of abiotic and biotic stress factors. Several reports in the literature to date have demonstrated the potential of these mVOCs in plant growth-promotion and disease-suppression, albeit mainly under artificial conditions. The mVOCs are low molecular mass compounds with a high vapour pressure and low boiling point and through diffusion can affect a response over a long distance both above and below ground. They belong to many different classes of chemicals that include terpenes, alcohols, alkenes and ketones amongst others. This review examines recent literature in this area and cites examples of mVOCs, or more particularly; bacterial-derived volatile compounds hereby referred to as ‘BVCs’, that have plant growth promoting and biocontrol effects. The multifaceted role of BVCs can be viewed as an integral part of a second green revolution in agriculture where alternative environmentally-friendly solutions are being sought for crop protection and bio-stimulation. Their ability to modulate plant photosynthetic and ISR pathways may provide the agricultural sector with more sustainable solutions for increased crop protection and production in the face of increasing climate and population changes.


PGPR Volatile organic compounds BVCs Biocontrol 


Conflict of Interest

Author(s) have no conflict of interest


  1. Ahmed E, Holmström SJM (2014) Siderophores in environmental research: roles and applications. Microb. Biotech 7:196–208CrossRefGoogle Scholar
  2. Almenar E, Del Valle V, Catala R, Gavara R (2007) Active package for wild strawberry fruit (Fragaria vesca L.). J Agric Food Chem 55:2240–2245CrossRefGoogle Scholar
  3. Arrebola E, Sivakumar D, Korsten L (2010) Effect of volatile compounds produced by Bacillus strains on postharvest decay in citrus. Biol Cont 53:122–128CrossRefGoogle Scholar
  4. Athukorala SNP, Fernando WGD, Rashid KY, De Kievit T (2010) The role of volatile and non-volatile antibiotics produced by Pseudomonas chlororaphis strain PA23 in its root colonization and control of Sclerotinia sclerotiorum. Biocont Sci Technol 20:875–890CrossRefGoogle Scholar
  5. Bailly A, Weisskopf L (2012) The modulating effect of bacterial volatiles on plant growth: current knowledge and future challenges. Plant Signal Behav 7:79–85CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bailly A, Weisskopf L (2017) Mining the volatilomes of plant-associated microbiota for new biocontrol solutions. Front Microbiol 8:1638CrossRefPubMedPubMedCentralGoogle Scholar
  7. Besset-Manzoni Y, Rieusset L, Joly P, Comte G, Prigent-Combaret C (2018) Exploiting rhizosphere microbial cooperation for developing sustainable agriculture strategies. Environ Sci Pollut Res 25:29953CrossRefGoogle Scholar
  8. Biondi E, Blasioli S, Galeone A, Spinelli F, Cellini A, Luchese C, Braschi I (2014) Detection of potato brown rot and ring rot by electronic nose: From laboratory to real scale. Talanta 129:422–430CrossRefGoogle Scholar
  9. Blom D, Fabbri C, Connor EC, Schiestl FP, Klauser DR, Boller T, Eberl L, Weisskopf L (2011a) Production of plant growth modulating volatiles is widespread among rhizosphere bacteria and strongly depends on culture conditions. Environ Microbiol 13:3047–3058CrossRefGoogle Scholar
  10. Blom D, Fabbri C, Eberl L, Weisskopf L (2011b) Volatile-mediated killing of Arabidopsis thaliana by bacteria is mainly due to hydrogen cyanide. Appl Environ Microbiol 77:1000–1008CrossRefGoogle Scholar
  11. Blumer C, Haas D (2000) Iron regulation of the hcnABC genes encoding hydrogen cyanide synthase depends on the anaerobic regulator ANR rather than on the global activator GacA in Pseudomonas fluorescens CHA0. Microbiol 146:2417–2424CrossRefGoogle Scholar
  12. Brilli F, Loreto F, Baccelli I (2019) Exploiting Plant Volatile Organic Compounds (VOCs) in Agriculture to Improve Sustainable Defense Strategies and Productivity of Crops. Front Plant Sci 10:264CrossRefPubMedPubMedCentralGoogle Scholar
  13. Carmen Orozco-Mosqueda M, Macías-Rodríguez L, Santoyo G, Farías-Rodríguez R, Valencia-Cantero E (2013) Medicago truncatula increases its iron-uptake mechanisms in response to volatile organic compounds produced by Sinorhizobium meliloti. Folia Microbiol 58:579–585CrossRefGoogle Scholar
  14. Cernava T, Müller H, Aschenbrenner IA, Grube M, Berg G (2015) Analysing the antagonistic potential of the lichen microbiome against pathogens by bridging metagenomic with culture studies. Front Microbiol 6:620PubMedPubMedCentralGoogle Scholar
  15. Chen H, Xiao X, Wang J, Wu L, Zheng Z, Yu Z (2008) Antagonistic effects of volatiles generated by Bacillus subtilis on spore germination and hyphal growth of the plant pathogen, Botrytis cinerea. Biotechnol Lett 30:919–923CrossRefGoogle Scholar
  16. Cho G, Kim J, Park CG, Nislow C, Weller DM, Kwak Y-S (2017) Caryolan-1-ol, an antifungal volatile produced by Streptomyces spp., inhibits the endomembrane system of fungi. Open Biol 7:170075Google Scholar
  17. Cho SM, Kang BR, Han SH, Anderson AJ, Park J-Y, Lee Y-H, Cho BH, Yang K-Y, Ryu C-M, 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 21:1067–1075CrossRefGoogle Scholar
  18. Choi HK, Song GC, Yi HS, Ryu C-M (2014) Field evaluation of the bacterial volatile derivative 3-pentanol in priming for induced resistance in pepper. J Chem Ecol 40:882–892CrossRefGoogle Scholar
  19. Chuankun X, Minghe M, Leming Z, Keqin Z (2004) Soil volatile fungistasis and volatile fungistatic compounds. Soil Biol Biochem 36:1997–2004CrossRefGoogle Scholar
  20. Compant S, Duffy B, Nowak J, Clément C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959CrossRefPubMedPubMedCentralGoogle Scholar
  21. Coosemans J (2005) Dimethyl disulphide (DMDS): a potential novel nematicide and soil disinfectant. Acta Hortic (ISHS) 698:57–64CrossRefGoogle Scholar
  22. Dandurishvili N, Toklikishvili N, Ovadis M, Eliashvili P, Giorgobiani N, Keshelava R, Tediashvili M, Vainstein A, Khmel I, Szegedi E, Chernin L (2011) Broad-range antagonistic rhizobacteria Pseudomonas fluorescens and Serratia plymuthica suppress Agrobacterium crown gall tumours on tomato plants. J Appl Microbiol 110:341–352CrossRefGoogle Scholar
  23. Dimkić I, Stanković S, Nišavić M, Petković M, Ristivojević P, Fira D, Berić T (2017) The profile and antimicrobial activity of Bacillus lipopeptide extracts of five potential biocontrol strains. Front Microbiol 8:925CrossRefPubMedPubMedCentralGoogle Scholar
  24. Effmert U, Kalderás J, Warnke R, Piechulla B (2012) Volatile mediated interactions between bacteria and fungi in the soil. J Chem Ecol 38:665–703CrossRefGoogle Scholar
  25. Farag MA, Ryu C-M, 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 67:2262–2268CrossRefGoogle Scholar
  26. Farag MA, Song GC, Park Y-S, Audrain B, Lee S, Ghigo JM, Kloepper JW, Ryu C-M (2017) Biological and chemical strategies for exploring inter- and intra-kingdom communication mediated via bacterial volatile signals. Nat Protoc 12:1359–1377CrossRefGoogle Scholar
  27. Fernando WGD, Ramarathnam R, Krishnamoorthy AS, Savchuk SC (2005) Identification and use of potential bacterial organic antifungal volatiles in biocontrol. Soil Biol Biochem 37:955–964CrossRefGoogle Scholar
  28. Fiddaman PJ, Rossall S (1993) The production of antifungal volatiles by Bacillus subtilis. J Appl Bacteriol 74:119–126CrossRefGoogle Scholar
  29. Fiddaman PJ, Rossall S (1994) Effect of substrate on the production of antifungal volatiles from Bacillus subtilis. J Appl Bacteriol 76:395–405CrossRefGoogle Scholar
  30. Fincheira P, Quiroz A (2018) Microbial volatiles as plant growth inducers. Microbiol Res 208:63–75CrossRefGoogle Scholar
  31. Fritsch J (2005) Dimethyl disulfide as a new chemical potential alternative to methyl bromide in soil disinfestation in France. Acta Hortic (ISHS) 698:71–76CrossRefGoogle Scholar
  32. Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 69:30–39CrossRefGoogle Scholar
  33. Groenhagen U, Baumgartner R, Bailly A, Gardiner A, Eberl L, Schulz S, Weisskopf L (2013) Production of bioactive volatiles by different Burkholderia ambifaria Strains. J Chem Ecol 39:892–906CrossRefGoogle Scholar
  34. Grosch R, Faltin F, Lottmann J, Kofoet A, Berg G (2005) Effectiveness of 3 antagonistic bacterial isolates to control Rhizoctonia solani Kühn on lettuce and potato. Can J Microbiol 51:345–353CrossRefGoogle Scholar
  35. Gu Y-Q, Mo M-H, Zhou J-P, Zou C-S, Zhang K-Q (2007) Evaluation and identification of potential organic nematicidal volatiles from soil bacteria. Soil Biol Biochem 39:2567–2575CrossRefGoogle Scholar
  36. Gutiérrez-Luna F, López-Bucio J, Altamirano-Hernández J, Valencia-Cantero E, Cruz H, Macías-Rodríguez L (2010) Plant growth-promoting rhizobacteria modulate root-system architecture in Arabidopsis thaliana through volatile organic compound emission. Symbiosis 51:75–83CrossRefGoogle Scholar
  37. Hérnandez-Calderón E, Aviles-Garcia ME, Castulo-Rubio DY, Macías-Rodríguez L, Ramírez VM, Santoyo G, López-Bucio J, Valencia-Cantero E (2018) Volatile compounds from beneficial or pathogenic bacteria differentially regulate root exudation, transcription of iron transporters, and defense signaling pathways in Sorghum bicolor. Plant Mol Biol 96:291–304CrossRefGoogle Scholar
  38. Howell CR, Beier RC, Stipanovic RD (1988) Production of ammonia by Enterobacter cloacae and its possible role in the biological control of Pythium preemergence damping-off by the bacterium. Phytopathology 78:1075–1078CrossRefGoogle Scholar
  39. Huang C-J, Tsay J-F, Chang S-Y, Yang H-P, Wu W-S, Chen C-Y (2012) Dimethyl disulfide is an induced systemic resistance elicitor produced by Bacillus cereus C1L. Pest Manag Sci 68:1306–1310CrossRefGoogle Scholar
  40. Huang Y, Xu C, Ma L, Zhang K, Duan C, Mo M (2010) Characterisation of volatiles produced from Bacillus megaterium YFM3.25 and their nematicidal activity against Meloidogyne incognita. Euro J Plant Pathol 126:417–422CrossRefGoogle Scholar
  41. Jeong H, Choi S-K, Ryu C-M, Park S-H (2019) Chronicle of a soil bacterium: Paenibacillus polymyxa E681 as a tiny guardian of plant and human health. Front Microbiol 10:467CrossRefPubMedPubMedCentralGoogle Scholar
  42. Kai M, Crespo E, Cristescu SM, Harren FJ, Francke W, Piechulla B (2010) Serratia odorifera: analysis of volatile emission and biological impact of volatile compounds on Arabidopsis thaliana. Appl Microbiol Biotechnol 88:965–976CrossRefGoogle Scholar
  43. Kai M, Effmert U, Berg G, Piechulla B (2007) Volatiles of bacterial antagonists inhibit mycelial growth of the plant pathogen Rhizoctonia solani. Arch Microbiol 187:351–360CrossRefGoogle Scholar
  44. Kai M, Haustein M, Molina F, Petri A, Scholz B, Piechulla B (2009) Bacterial volatiles and their action potential. Appl Microbiol Biotechnol 81:1001–1012CrossRefGoogle Scholar
  45. Kai M, Piechulla B (2009) Plant growth promotion due to rhizobacterial volatiles – An effect of CO2? FEBS Lett 583:3473–3477CrossRefGoogle Scholar
  46. Kai M, Piechulla B (2010) Impact of volatiles of the rhizobacteria Serratia odorifera on the moss Physcomitrella patens. Plant Signal Behav 5:444–446CrossRefGoogle Scholar
  47. Kai M, Effmert U, Piechulla B (2016) Bacterial-plant-interactions: approaches to unravel the biological function of bacterial volatiles in the rhizosphere. Front. Microbiol. 7Google Scholar
  48. Kanchiswamy CN, Malnoy M, Maffei M (2015) Chemical diversity of microbial volatiles and their potential for plant growth and productivity. Front Plant Sci 6:151CrossRefPubMedPubMedCentralGoogle Scholar
  49. Kim J-S, Lee J, Seo S-J, Lee C, Woo SY, Kim S-H (2015) Gene expression profile affected by volatiles of new plant growth promoting rhizobacteria, Bacillus subtilis strain JS, in tobacco. Genes Genom 37:387–397CrossRefGoogle Scholar
  50. Kloepper JW, Rodríguez-Kábana R, Zehnder AW, Murphy JF, Sikora E, Fernández C (1999) Plant root-bacterial interactions in biological control of soilborne diseases and potential extension to systemic and foliar diseases. Australas Plant Pathol 28:21–26CrossRefGoogle Scholar
  51. Kloepper JW and Schroth MN (1978) Plant growth promoting rhizobacteria on radishes. In: Proceedings of the 4th international conference on plant pathogenic bacteria, angers, France, vol 2, pp 879–882Google Scholar
  52. Kurze S, Bahl H, Dahl R, Berg G (2001) Biological control of fungal strawberry diseases by Serratia plymuthica HRO-C48. Plant Dis 85:529–534CrossRefGoogle Scholar
  53. Kwon Y, Ryu C-M, Lee S, Park H, Han K, Lee J, Lee K, Chung W, Jeong M-J, Kim H, Bae D-W (2010) Proteome analysis of Arabidopsis seedlings exposed to bacterial volatiles. Planta 232:1355–1370CrossRefGoogle Scholar
  54. Leach J, Triplett LR, Argueso CT, Trivedi P (2017) Communication in the phytobiome. Cell 169(4):587–596CrossRefGoogle Scholar
  55. Lee B, Farag MA, Park HB, Kloepper JW, Lee SH, Ryu C-M (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:e48744CrossRefPubMedPubMedCentralGoogle Scholar
  56. Liu H, Brettell LE (2019) Plant defense by VOC-induced microbial priming. Trends Plant Sci 24:187–189CrossRefGoogle Scholar
  57. Liu W, Zhao L, Wang C, Mu W, Liu F (2009) Bioactive evaluation and application of antifungal volatiles generated by five soil bacteria. Acta Phytophyl Sin 36:97–105Google Scholar
  58. 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 20:207–217CrossRefGoogle Scholar
  59. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Ann Rev Microbiol 63:541–556CrossRefGoogle Scholar
  60. 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:e22974CrossRefPubMedPubMedCentralGoogle Scholar
  61. Müller H, Westendorf C, Leitner E, Chernin L, Riedel K, Schmidt S, Eberl L, Berg G (2009) Quorum-sensing effects in the antagonistic rhizosphere bacterium Serratia plymuthica HRO-C48. FEMS Microbiol Ecol 67:468–478CrossRefGoogle Scholar
  62. Nawrath T, Mgode GF, Weetjens B, Kaufmann SH, Schulz S (2012) The volatiles of pathogenic and nonpathogenic mycobacteria and related bacteria. Beilstein J Org Chem 8:290–299CrossRefPubMedPubMedCentralGoogle Scholar
  63. Nicholson WL (2008) The Bacillus subtilis ydjL (bdhA) gene encodes acetoin reductase/2,3-Butanediol dehydrogenase. Appl Environ Microbiol 74:6832–6838CrossRefPubMedPubMedCentralGoogle Scholar
  64. Oteino N, Lally RD, Kiwanuka S, Lloyd A, Ryan D, Germaine KJ, Dowling DN (2015) Plant growth promotion induced by phosphate solubilizing endophytic Pseudomonas isolates. Front Microbiol 6:745CrossRefPubMedPubMedCentralGoogle Scholar
  65. Park Y-S, Dutta S, Ann M, Raajmakers JM, Park K (2015) Promotion of plant growth by Pseudomonas fluorescens strain SS101 via novel volatile organic compounds. Biochem Biophys Res Commun 461:361–365CrossRefGoogle Scholar
  66. Park HB, Lee B, Kloepper JW, Ryu CM (2013) One shot-two pathogens blocked: exposure of Arabidopsis to hexadecane, a long chain volatile organic compound, confers induced resistance against both Pectobacterium carotovorum and Pseudomonas syringae. Plant Signal Behav 8:e24619CrossRefGoogle Scholar
  67. Rath M, Mitchell TR, Gold SE (2018) Volatiles produced by Bacillus mojavensis RRC101 act as plant growth modulators and are strongly culture-dependent. Microbiol Res 208:76–84CrossRefGoogle Scholar
  68. Rijavec T, Lapanje A (2016) Hydrogen cyanide in the rhizosphere: not suppressing plant pathogens, but rather regulating availability of phosphate. Front Microbiol 7:1785CrossRefPubMedPubMedCentralGoogle Scholar
  69. Romera FJ, García MJ, Lucena C, Martínez-Medina A, Aparicio MA, Ramos J, Alcántara E, Angulo M, Pérez-Vicente R (2019) Induced systemic resistance (ISR) and fe deficiency responses in dicot plants. Front Plant Sci 10:287CrossRefPubMedPubMedCentralGoogle Scholar
  70. Rosier A, Medeiros FHV, Bais HP (2018) Defining plant growth promoting rhizobacteria molecular and biochemical networks in beneficial plant-microbe interactions. Plant Soil 428:35CrossRefGoogle Scholar
  71. Rudrappa T, Biedrzycki ML, Kunjeti SG, Donofrio NM, Czymmek KJ, Paul WP, Bais HP (2010) The rhizobacterial elicitor acetoin induces systemic resistance in Arabidopsis thaliana. Commun Integr Biol 3:130–138CrossRefPubMedPubMedCentralGoogle Scholar
  72. Ryu C-M, Farag MA, Hu C-H, Reddy MS, Kloepper JW, Paré PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026Google Scholar
  73. Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Paré PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134(3):1017–1026 (Published correction appears in Plant Physiol. 2005 Apr;137(4):1486)Google Scholar
  74. Ryu C-M, Farag MA, Hu C-H, Reddy MS, Wei H-X, Paré PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci 100:4927–4932CrossRefGoogle Scholar
  75. Ryu C-M, Hu C-H, Locy R, Kloepper J (2005a) Study of mechanisms for plant growth promotion elicited by rhizobacteria in Arabidopsis thaliana. Plant Soil 268:285–292CrossRefGoogle Scholar
  76. Ryu C-M, 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
  77. Sang MK, Kim JD, Kim BS, Kim KD (2011) Root treatment with rhizobacteria antagonistic to Phytophthora blight affects anthracnose occurrence, ripening, and yield of pepper fruit in the plastic house and field. Phytopathology 101(6):666–678Google Scholar
  78. 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 49:1177–1182CrossRefGoogle Scholar
  79. Schulz-Bohm K (2017) Microbial volatiles: small molecules with an important role in intra- and inter-kingdom interactions. Front Microbiol 8:2484CrossRefPubMedPubMedCentralGoogle Scholar
  80. Shao J, Xu Z, Zhang N, Shen Q, Zhang R (2015) Contribution of indole-3-acetic acid in the plant growth promotion by the rhizospheric strain Bacillus amyloliquefaciens SQR9. Biol Fertil Soils 51:321CrossRefGoogle Scholar
  81. Sharifi R, Ryu CM (2016) Making healthier or killing enemies? Bacterial volatile-elicited plant immunity plays major role upon protection of Arabidopsis than the direct pathogen inhibition. Commun Integr Biol 9:e1197445Google Scholar
  82. Sharifi R, Ryu C-M (2018a) Revisiting bacterial volatile-mediated plant growth promotion: lessons from the past and objectives for the future. Ann Bot 122:349–358CrossRefPubMedPubMedCentralGoogle Scholar
  83. Sharifi R, Ryu C-M (2018b) Biogenic volatile compounds for plant disease diagnosis and health improvement. Plant Pathol J 34:459–469PubMedPubMedCentralGoogle Scholar
  84. Singh S (2014) A review on possible elicitor molecules of cyanobacteria: their role in improving plant growth and providing tolerance against biotic or abiotic stress. J Appl Microbiol 117:1221–1244CrossRefGoogle Scholar
  85. Song G, Ryu C-M (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 14:9803–9819CrossRefPubMedPubMedCentralGoogle Scholar
  86. Song GC, Ryu CM (2018) Evidence for Volatile Memory in Plants: Boosting Defence Priming through the Recurrent Application of Plant Volatiles. Mol. cells 41(8):724Google Scholar
  87. Song GC, Riu M, Ryu C-M (2019) Beyond the two compartments Petri-dish: optimising growth promotion and induced resistance in cucumber exposed to gaseous bacterial volatiles in a miniature greenhouse system. Plant Methods 15:9CrossRefPubMedPubMedCentralGoogle Scholar
  88. Spinelli F, Cellini A, Vanneste J, Rodriguez-Estrada M, Costa G, Savioli S, Harren FM, Cristescu S (2012) Emission of volatile compounds by Erwinia amylovora: biological activity in vitro and possible exploitation for bacterial identification. Trees 26:141–152CrossRefGoogle Scholar
  89. Spinelli F, Costa G, Rondelli E, Busi S, Vanneste JL, Rodriguez EMT, Savioli S, Harren FJM, Crespo E, Cristescu SM (2011) Emission of volatiles during the pathogenic interaction between Erwinia amylovora and Malus domestica. Acta Hortic (ISHS) 896:55–63CrossRefGoogle Scholar
  90. Spinelli F, Noferini M, Vanneste JL, Costa G (2010) Potential of the electronic-nose for the diagnosis of bacterial and fungal diseases in fruit trees. EPPO Bull 40:59–67CrossRefGoogle Scholar
  91. Tahir JAS, Gu Q, Wu J, Niu Y, Huo R, Gao X (2017a) Bacillus volatiles adversely affect the physiology and ultra-structure of Ralstonia solanacearum and induce systemic resistance in tobacco against bacterial wilt. Sci Rep 7:40481CrossRefPubMedPubMedCentralGoogle Scholar
  92. Tahir JAS, Gu Q, Wu J, Raza W, Hanif A, Wu L, Colman MV, Gao X (2017b) Plant growth promotion by volatile organic compounds produced by Bacillus subtilis SYST2. Front Microbiol 8:171CrossRefPubMedPubMedCentralGoogle Scholar
  93. Tahir JAS, Gu Q, Wu H, Raza W, Safdar A, Huang Z, Rajer FU, Gao X (2017c) Effect of volatile compounds produced by Ralstonia solanacearum on plant growth promoting and systemic resistance inducing potential of Bacillus volatiles. BMC Plant Biol 17:133CrossRefPubMedPubMedCentralGoogle Scholar
  94. Tenorio-Salgado S, Tinoco R, Vazquez-Duhalt R, Caballero-Mellado J, Perez-Rueda E (2013) Identification of volatile compounds produced by the bacterium Burkholderia tropica that inhibit the growth of fungal pathogens. Bioengineered 4:236–243CrossRefPubMedPubMedCentralGoogle Scholar
  95. Ting A, Mah S, Tee C (2011) Detection of potential volatile inhibitory compounds produced by endobacteria with biocontrol properties towards Fusarium oxysporum f. sp. cubense race 4. World J Microbiol Biotechnol 27:229–235CrossRefGoogle Scholar
  96. Van Der Kooij LAW, Kok LJD, Stulen I (1999) Biomass production and carbohydrate content of Arabidopsis thaliana at atmospheric CO2 concentrations from 390 to 1680 μl l-1. Plant Biol 1:482–486CrossRefGoogle Scholar
  97. Velázquez-Becerra C, Macías-Rodríguez L, López-Buci J, Altamirano-Hernández J, Flores-Cortez I, Valencia-Cantero E (2011) 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 339:329–340CrossRefGoogle Scholar
  98. Velázquez-Becerra C, Macías-Rodríguez L, López-Bucio J, Flores-Cortez I, Santoyo G, Hernández-Soberano C, Valencia-Cantero E (2013) The rhizobacterium Arthrobacter agilis produces dimethylhexadecylamine, a compound that inhibits growth of phytopathogenic fungi in vitro. Protoplasma 250:1251–1262CrossRefGoogle Scholar
  99. Velivelli SL, Sessitch A, Doyle Prestwich B (2014) The role of microbial inoculants in integrated crop management systems. Potato Res 57:291–309CrossRefGoogle Scholar
  100. Velivelli SL, Kromann P, Lojan P, Rojas M, Franco J, Suarez JP, Doyle Prestwich B (2015) Identification of mVOCs from Andean rhizobacteria and field evaluation of bacterial and mycorrhizal inoculants on growth of potato in its center of origin. Microb Ecol 69:652–667CrossRefGoogle Scholar
  101. Vespermann A, Kai M, Piechulla B (2007) Rhizobacterial volatiles affect the growth of fungi and Arabidopsis thaliana. Appl Environ Microbiol 73:5639–5641CrossRefPubMedPubMedCentralGoogle Scholar
  102. Voisard C, Keel C, Haas D, Defago G (1989) Cyanide production by Pseudomonas fluorescens helps suppress black root rot of tobacco under gnotobiotic conditions. EMBO J 8:351–358CrossRefPubMedPubMedCentralGoogle Scholar
  103. Wan M, Li G, Zhang J, Jiang D, Huang H-C (2008) Effect of volatile substances of Streptomyces platensis F-1 on control of plant fungal diseases. Biol Control 46:552–559CrossRefGoogle Scholar
  104. Ward JK, Strain BR (1999) Elevated CO2 studies: past, present and future. Tree Physiol 19:211–220CrossRefGoogle Scholar
  105. Weise T, Kai M, Gummesson A, Troeger A, Von Reuss S, Piepenborn S, Kosterka F, Sklorz M, Zimmermann R, Francke W, Piechulla B (2012) Volatile organic compounds produced by the phytopathogenic bacterium Xanthomonas campestris pv. vesicatoria 85-10. Beilstein J Org Chem 8:579–596CrossRefPubMedPubMedCentralGoogle Scholar
  106. Weise T, Kai M, Piechulla B (2013) Bacterial ammonia causes significant plant growth inhibition. PLoS One 8:e63538CrossRefPubMedPubMedCentralGoogle Scholar
  107. Weisskopf L, Ryu CM, Raaijmakers JM, Garbeva P (2016) Smelly fumes-volatile-mediated communication between bacteria and other organisms. Front. Microbiol. 7Google Scholar
  108. Xie X, Zhang H, Pare PW (2009) Sustained growth promotion in Arabidopsis with long-term exposure to the beneficial soil bacterium Bacillus subtilis (GB03). Plant Signal Behav 4:948–953CrossRefPubMedPubMedCentralGoogle Scholar
  109. Yang L-L, Huang Y, Liu J, Ma L, Mo M-H, Li W-J, Yang F-X (2012) Lysinibacillus mangiferahumi sp. nov., a new bacterium producing nematicidal volatiles. Antonie Van Leeuwenhoek 102:53–59CrossRefGoogle Scholar
  110. Yaoyao E, Yuan J, Yang F, Wang L, Ma J, Li J, Pu X, Raza W, Hwang Q, Shen Q (2017) PGPR strain Paenibacillus polymyxa SQR-21 potentially benefts watermelon growth by re-shaping root protein expression. AMB Expr 7:104CrossRefGoogle Scholar
  111. Yu SM, Lee Y (2013) Plant growth promoting rhizobacterium Proteus vulgaris JBLS202 stimulates the seedling growth of Chinese cabbage through indole emission. Plant Soil 370:485–495CrossRefGoogle Scholar
  112. Yuan J, Raza W, Shen Q, Huang Q (2012) Antifungal activity of Bacillus amyloliquefaciens NJN-6 volatile compounds against Fusarium oxysporum f. sp. cubense. Appl Environ Microbiol 78:5942–5944CrossRefPubMedPubMedCentralGoogle Scholar
  113. Yuan J, Zhao M, Li R, Huang Q, Raza W, Rensing C, Shen Q (2017) Microbial volatile compounds alter the soil microbial community. Environ Sci Pollut Res 24:22485–22493CrossRefGoogle Scholar
  114. Zhang H, Kim MS, Sun Y, Dowd SE, Shi H, Paré PW (2008a) Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter HKT1. Mol Plant Microbe Interact 21:737–744CrossRefGoogle Scholar
  115. Zhang H, Kim MS, Krishnamachari V, Payton P, Sun Y, Grimson M, Farag MA, Ryu CM, Allen R, Melo IS, Pare PW (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226:839–851CrossRefGoogle Scholar
  116. 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 58:568–577CrossRefPubMedPubMedCentralGoogle Scholar
  117. Zhang H, Xie X, Kim MS, Kornyeyev DA, Holaday S, Pare PW (2008b) Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant J 56:264–273CrossRefGoogle Scholar
  118. Zhang X, Li B, Wang Y, Guo Q, Lu X, Li S, Ma P (2013) Lipopeptides, a novel protein, and volatile compounds contribute to the antifungal activity of the biocontrol agent Bacillus atrophaeus CAB-1. Appl Microbiol Biotechnol 97:9525–9534CrossRefGoogle Scholar
  119. Zhao L-J, Yang X-N, Li X-Y, Mu W, Liu F (2011) Antifungal, insecticidal and herbicidal properties of volatile components from Paenibacillus polymyxa strain BMP-11. Agric Sci China 10:728–736CrossRefGoogle Scholar
  120. Zou C, Li Z, Yu D (2010) Bacillus megaterium strain XTBG34 promotes plant growth by producing 2-pentylfuran. J Microbiol 48:460–466CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Darren Heenan-Daly
    • 1
  • Siva L. S. Velivelli
    • 2
  • Barbara Doyle Prestwich
    • 1
    Email author
  1. 1.School of Biological Earth and Environmental ScienceUniversity College CorkCorkIreland
  2. 2.Donald Danforth Plant Science CenterSt LouisUSA

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