Journal of Chemical Ecology

, Volume 39, Issue 7, pp 810–825 | Cite as

Volatile Organic Compound Mediated Interactions at the Plant-Microbe Interface

  • Robert R. Junker
  • Dorothea Tholl
Review Article


Microorganisms colonize the surfaces of plant roots, leaves, and flowers known as the rhizosphere, phyllosphere, and anthosphere. These spheres differ largely in a number of factors that may determine the ability of microbes to establish themselves and to grow in these habitats. In this article, we focus on volatile organic compounds (VOCs) emitted by plants, and we discuss their effects on microbial colonizers, with an emphasis on bacteria. We present examples of how growth-inhibiting properties and mechanisms of VOCs such as terpenoids, benzenoid compounds, aliphatics, and sulfur containing compounds prevent bacterial colonization at different spheres, in antagonism with their role as carbon-sources that support the growth of different bacterial taxa. The notion that VOCs represent important factors that define bacterial niches is further supported by results for representatives of two bacterial genera that occupy strongly diverging niches based on scent emissions of different plant species and organs. Bacteria are known to either positively or negatively affect plant fitness and to interfere with plant-animal interactions. Thus, bacteria and other microbes may select for VOCs, enabling plants to control microbial colonizers on their surfaces, thereby promoting the growth of mutualists and preventing the establishment of detrimental microbes.


Anthosphere Epiphytic bacteria Microbiota Niches Plant volatiles Phyllosphere Rhizosphere Terpenes 



We thank Maren Höfers for help with Fig. 1 and Afroditi Kantsa for valuable comments on the manuscript. Research by R.R.J. on bacterial communities on petals and leaves was funded by the Deutsche Forschungsgemeinschaft (BL960/1-1). Work by D.T. was supported by a National Science Foundation Advance Virginia Tech research and development grant, National Science Foundation Grant MCB-0950865, Thomas and Kate Jeffress Memorial Trust Grant J-850, and a US Department of Agriculture Cooperative State Research, Education, and Extension Service National Research Initiative Grant 2007-35318-18384 (to D.T.).


  1. Abanda-Nkpwatt D, Musch M, Tschiersch J, Boettner M, Schwab W (2006) Molecular interaction between Methylobacterium extorquens and seedlings: growth promotion, methanol consumption, and localization of the methanol emission site. J Exp Bot 57:4025–4032PubMedCrossRefGoogle Scholar
  2. Adler LS (2000) The ecological significance of toxic nectar. Oikos 91:409–420CrossRefGoogle Scholar
  3. Ahmad A, Khan A, Akhtar F, Yousuf S, Xess I, Khan LA, Manzoor N (2011) Fungicidal activity of thymol and carvacrol by disrupting ergosterol biosynthesis and membrane integrity against Candida. Eur J Clin Microbiol Infect Dis 30:41–50PubMedCrossRefGoogle Scholar
  4. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827PubMedCrossRefGoogle Scholar
  5. Aligiannis N, Kalpoutzakis E, Kyriakopoulou I, Mitaku S, Chinou IB (2004) Essential oil of Phlomis species growing in Greece: chemical composition and antimicrobial activity. Flavour Fragr J 19:320–324CrossRefGoogle Scholar
  6. Ashour HM (2008) Antibacterial, antifungal, and anticancer activities of volatile oils and extracts from stems, leaves, and flowers of Eucalyptus sideroxylon and Eucalyptus torquata. Cancer Biol Ther 7:399–403PubMedCrossRefGoogle Scholar
  7. Atkinson R, Arey J (2003) Atmospheric degradation of volatile organic compounds. Chem Rev 103:4605–4638PubMedCrossRefGoogle Scholar
  8. Attaran E, Rostás M, Zeier J (2008) Pseudomonas syringae elicits emission of the terpenoid (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene in Arabidopsis leaves via jasmonate signaling and expression of the terpene synthase TPS4. Mol Plant-Microbe Interact 21:1482–1497PubMedCrossRefGoogle Scholar
  9. Baas Becking LGM (1934) Geobiologie of inleiding tot de milieukunde. W.P. Van Stockum & Zoon, The HagueGoogle Scholar
  10. Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681PubMedCrossRefGoogle Scholar
  11. Banchio E, Xie XT, Zhang HM, Pare PW (2009) Soil bacteria elevate essential oil accumulation and emissions in sweet basil. J Agric Food Chem 57:653–657PubMedCrossRefGoogle Scholar
  12. Basim E, Basim H, Ozcan M (2006) Antibacterial activities of Turkish pollen and propolis extracts against plant bacterial pathogens. J Food Eng 77:992–996CrossRefGoogle Scholar
  13. Beisner BE, Peres PR, Lindstrom ES, Barnett A, Longhi ML (2006) The role of environmental and spatial processes in structuring lake communities from bacteria to fish. Ecology 87:2985–2991PubMedCrossRefGoogle Scholar
  14. Belisle M, Peay KG, Fukami T (2012) Flowers as islands: spatial distribution of nectar-inhabiting microfungi among plants of Mimulus aurantiacus, a hummingbird-pollinated shrub. Microb Ecol 63:711–718PubMedCrossRefGoogle Scholar
  15. Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486PubMedCrossRefGoogle Scholar
  16. Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13PubMedCrossRefGoogle Scholar
  17. Bodenhausen N, Horton MW, Bergelson J (2013) Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLoS One 8:e56329PubMedCrossRefGoogle Scholar
  18. Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat Commun 1:48PubMedCrossRefGoogle Scholar
  19. Bressan M, Roncato MA, Bellvert F, Comte G, Haichar FE, Achouak W, Berge O (2009) Exogenous glucosinolate produced by Arabidopsis thaliana has an impact on microbes in the rhizosphere and plant roots. ISME J 3:1243–1257PubMedCrossRefGoogle Scholar
  20. Bruce TJA, Pickett JA (2011) Perception of plant volatile blends by herbivorous insects - Finding the right mix. Phytochemistry 72:1605–1611PubMedCrossRefGoogle Scholar
  21. Bulgarelli D, Rott M, Schlaeppi K, van Themaat EVL, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E et al (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95PubMedCrossRefGoogle Scholar
  22. Bulgarelli D, Schlaeppi K, Spaepen S, Loren V, van Themaat E, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838PubMedCrossRefGoogle Scholar
  23. Carter C, Thornburg RW (2004) Is the nectar redox cycle a floral defense against microbial attack? Trends Plant Sci 9:320–324PubMedCrossRefGoogle Scholar
  24. Cecchini C, Coman MM, Cresci A, Tirillini B, Cristalli G, Papa F, Sagratini G, Vittori S, Maggi F (2010) Essential oil from fruits and roots of Ferulago campestris (Besser) Grecescu (Apiaceae): composition and antioxidant and anti-Candida activity. Flavour Fragr J 25:493–502CrossRefGoogle Scholar
  25. Chen F, Tholl D, D’Auria JC, Farooq A, Pichersky E, Gershenzon J (2003) Biosynthesis and emission of terpenoid volatiles from Arabidopsis flowers. Plant Cell 15:481–494PubMedCrossRefGoogle Scholar
  26. Chen F, Ro D-K, Petri J, Gershenzon J, Bohlmann J, Pichersky E, Tholl D (2004) Characterization of a root-specific Arabidopsis terpene synthase responsible for the formation of the volatile monoterpene 1,8-cineole. Plant Physiol 135:1956–1966PubMedCrossRefGoogle Scholar
  27. Cho SM, Kang BR, Han SH, Anderson AJ, Park JY, Lee YH, Cho BH, Yang KY, Ryu CM, Kirn 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 21:1067–1075PubMedCrossRefGoogle Scholar
  28. Clark L, Mason JR (1985) Use of nest material as insecticidal and anti-pathogenic agents by the European Starling. Oecologia 67:169–176CrossRefGoogle Scholar
  29. Cowan MM (1999) Plant products as antimicrobial agents. Clin Microbiol Rev 12:564–582PubMedGoogle Scholar
  30. Cristani M, D’Arrigo M, Mandalari G, Castelli F, Sarpietro MG, Micieli D, Venuti V, Bisignano G, Saija A, Trombetta D (2007) Interaction of four monoterpenes contained in essential oils with model membranes: Implications for their antibacterial activity. J Agric Food Chem 55:6300–6308PubMedCrossRefGoogle Scholar
  31. Croft KPC, Juttner F, Slusarenko AJ (1993) Volatile products of the lipoxygenase pathway evolved from Phaseolus vulgaris (L) leaves inoculated with Pseudomonas syringae pv phaseolicola. Plant Physiol 101:13–24PubMedGoogle Scholar
  32. Davis TS, Crippen TL, Hofstetter RW, and Tomberlin JK (2013) Microbial volatile emissions as insect semiochemicals. J Chem Ecol, this volumeGoogle Scholar
  33. de Carvalho C, de Fonseca MMR (2007) Preventing biofilm formation: promoting cell separation with terpenes. FEMS Microbiol Ecol 61:406–413PubMedCrossRefGoogle Scholar
  34. Del Giudice L, Massardo DR, Pontieri P, Bertea CM, Mombello D, Carata E, Tredici SM, Tala A, Mucciarelli M, Groudeva VI et al (2008) The microbial community of Vetiver root and its involvement into essential oil biogenesis. Environ Microbiol 10:2824–2841PubMedCrossRefGoogle Scholar
  35. Desbrosses GJ, Stougaard J (2011) Root nodulation: A paradigm for how plant-microbe symbiosis influences host developmental pathways. Cell Host Microbe 10:348–358PubMedCrossRefGoogle Scholar
  36. Di Pasqua R, Hoskins N, Betts G, Mauriello G (2006) Changes in membrane fatty acids composition of microbial cells induced by addiction of thymol, carvacrol, limonene, cinnamaldehyde, and eugenol in the growing media. J Agric Food Chem 54:2745–2749PubMedCrossRefGoogle Scholar
  37. Di Pasqua R, Betts G, Hoskins N, Edwards M, Ercolini D, Mauriello G (2007) Membrane toxicity of antimicrobial compounds from essential oils. J Agric Food Chem 55:4863–4870PubMedCrossRefGoogle Scholar
  38. Di Pasqua R, Mamone G, Ferranti P, Ercolini D, Mauriello G (2010) Changes in the proteome of Salmonella enterica serovar Thompson as stress adaptation to sublethal concentrations of thymol. Proteomics 10:1040–1049PubMedGoogle Scholar
  39. Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15:167–175PubMedCrossRefGoogle Scholar
  40. Dobson HEM, Bergström G (2000) The ecology and evolution of pollen odors. Plant Syst Evol 222:63–87CrossRefGoogle Scholar
  41. Dudareva N, Negre F, Nagegowda DA, Orlova I (2006) Plant volatiles: Recent advances and future perspectives. Crit Rev Plant Sci 25:417–440CrossRefGoogle Scholar
  42. Effmert U, Kalderas J, Warnke R, Piechulla B (2012) Volatile mediated interactions between bacteria and fungi in the soil. J Chem Ecol 38:665–703PubMedCrossRefGoogle Scholar
  43. Erb M, Glauser G, Robert CAM (2012) Induced immunity against belowground insect herbivores - Activation of defenses in the absence of a jasmonate burst. J Chem Ecol 38:629–640PubMedCrossRefGoogle Scholar
  44. Fahlgren C, Hagstrom A, Nilsson D, Zweifel UL (2010) Annual variations in the diversity, viability, and origin of airborne bacteria. Appl Environ Microbiol 76:3015–3025PubMedCrossRefGoogle Scholar
  45. Fall R, Benson AA (1996) Leaf methanol - The simplest natural product from plants. Trends Plant Sci 1:296–301Google Scholar
  46. 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 67:2262–2268PubMedCrossRefGoogle Scholar
  47. Farag MA, Zhang H and Ryu C-M (2013) Dynamic chemical communication between plants and bacteria through airborne signals: Induced resistance by bacterial volatiles. J Chem Ecol, this volumeGoogle Scholar
  48. Field B, Osbourn AE (2008) Metabolic diversification-independent assembly of operon-like gene clusters in different plants. Science 320:543–547PubMedCrossRefGoogle Scholar
  49. Fontana A, Reichelt M, Hempel S, Gershenzon J, Unsicker SB (2009) The effects of arbuscular mycorrhizal fungi on direct and indirect defense metabolites of Plantago lanceolata L. J Chem Ecol 35:833–843PubMedCrossRefGoogle Scholar
  50. Fridman S, Izhaki I, Gerchman Y, Halpern M (2012) Bacterial communities in floral nectar. Environ Microbiol Rep 4:97–104PubMedCrossRefGoogle Scholar
  51. Fuernkranz M, Lukesch B, Müller H, Huss H, Grube M, Berg G (2012) Microbial diversity inside pumpkins: microhabitat-specific communities display a high antagonistic potential against phytopathogens. Microb Ecol 63:418–428CrossRefGoogle Scholar
  52. Galbally IE, Kirstine W (2002) The production of methanol by flowering plants and the global cycle of methanol. J Atmos Chem 43:195–229CrossRefGoogle Scholar
  53. Gao Y, Jin YJ, Li HD, Chen HJ (2005) Volatile organic compounds and their roles in bacteriostasis in five conifer species. J Integr Plant Biol 47:499–507CrossRefGoogle Scholar
  54. Guenther A, Hewitt CN, Erickson D, Fall R, Geron C, Graedel T, Harley P, Klinger L, Lerdau M, Mckay WA et al (1995) A global-model of natural volatile organic-compound emissions. J Geophys Res Atmos 100:8873–8892CrossRefGoogle Scholar
  55. Hardoim PR, van Overbeek LS, van Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471PubMedCrossRefGoogle Scholar
  56. Heil M, Karban R (2010) Explaining evolution of plant communication by airborne signals. Trends Ecol Evol 25:137–144PubMedCrossRefGoogle Scholar
  57. Heil M, Silva Bueno JC (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci USA 104:5467–5472PubMedCrossRefGoogle Scholar
  58. Herde M, Gärtner K, Köllner TG, Fode B, Boland W, Gershenzon J, Gatz C, Tholl D (2008) Identification and regulation of TPS04/GES, an Arabidopsis geranyllinalool synthase catalyzing the first step in the formation of the insect-induced volatile C16-homoterpene TMTT. Plant Cell 20:1152–1168PubMedCrossRefGoogle Scholar
  59. Himanen SJ, Blande JD, Klemola T, Pulkkinen J, Heijari J, Holopainen JK (2010) Birch (Betula spp.) leaves adsorb and re-release volatiles specific to neighbouring plants - a mechanism for associational herbivore resistance? New Phytol 186:722–732PubMedCrossRefGoogle Scholar
  60. Horvath G, Kovacs K, Kocsis B, Kustos I (2009) Effect of thyme (Thymus vulgaris L.) essential oil and its main constituents on the outer membrane protein composition of Erwinia strains studied with microfluid chip technology. Chromatographia 70:1645–1650CrossRefGoogle Scholar
  61. Hountondji FCC, Sabelis MW, Hanna R, Janssen A (2005) Herbivore-induced plant volatiles trigger sporulation in entomopathogenic fungi: The case of Neozygites tanajoae infecting the cassava green mite. J Chem Ecol 31:1003–1021PubMedCrossRefGoogle Scholar
  62. Huang J, Cardoza YJ, Schmelz EA, Raina R, Engelberth J, Tumlinson JH (2003) Differential volatile emissions and salicylic acid levels from tobacco plants in response to different strains of Pseudomonas syringae. Planta 217:767–775PubMedCrossRefGoogle Scholar
  63. Huang MS, Abel C, Sohrabi R, Petri J, Haupt I, Cosimano J, Gershenzon J, Tholl D (2010) Variation of herbivore-induced volatile terpenes among Arabidopsis ecotypes depends on allelic differences and subcellular targeting of two terpene synthases, TPS02 and TPS03. Plant Physiol 153:1293–1310PubMedCrossRefGoogle Scholar
  64. Huang M, Sanchez-Moreiras AM, Abel C, Sohrabi R, Lee S, Gershenzon J, Tholl D (2012) The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)-β-caryophyllene, is a defense against a bacterial pathogen. New Phytol 193:997–1008PubMedCrossRefGoogle Scholar
  65. Hutchinson GE (1957) Concluding remarks. Cold Spring Harb Symp Quant Biol 22:415–427CrossRefGoogle Scholar
  66. Huttenhower C, Gevers D, Knight R, Abubucker S, Badger JH, Chinwalla AT, Creasy HH, Earl AM, FitzGerald MG, Fulton RS et al (2012) Structure, function and diversity of the healthy human microbiome. Nature 486:207–214CrossRefGoogle Scholar
  67. Ibekwe AM, Grieve CM (2004) Changes in developing plant microbial community structure as affected by contaminated water. FEMS Microbiol Ecol 48:239–248PubMedCrossRefGoogle Scholar
  68. Inoue Y, Hada T, Shiraishi A, Hirose K, Hamashima H, Kobayashi S (2005) Biphasic effects of geranylgeraniol, teprenone, and phytol on the growth of Staphylococcus aureus. Antimicrob Agents Chemother 49:1770–1774PubMedCrossRefGoogle Scholar
  69. Jallow MFA, Dugassa-Gobena D, Vidal S (2008) Influence of an endophytic fungus on host plant selection by a polyphagous moth via volatile spectrum changes. Arthropod-Plant Interactions 2:53–62CrossRefGoogle Scholar
  70. Johnson SN, Nielsen UN (2012) Foraging in the dark - Chemically mediated host plant location by belowground insect herbivores. J Chem Ecol 38:604–614PubMedCrossRefGoogle Scholar
  71. Jung SC, Martinez-Medina A, Lopez-Raez, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38:651–664PubMedCrossRefGoogle Scholar
  72. Junker RR, Höcherl N, Blüthgen N (2010) Responses to olfactory signals reflect network structure of flower-visitor interactions. J Anim Ecol 79:818–823PubMedGoogle Scholar
  73. Junker RR, Loewel C, Gross R, Dötterl S, Keller A, Blüthgen N (2011) Composition of epiphytic bacterial communities differs on petals and leaves. Plant Biol 13:918–924PubMedCrossRefGoogle Scholar
  74. Junker RR, Blüthgen N, Brehm T, Binkenstein J, Paulus J, Schaefer HM, Stang M (2013) Specialization on traits as basis for the niche-breadth of flower visitors and as structuring mechanism of ecological networks. Funct Ecol 27:329–341CrossRefGoogle Scholar
  75. Kalemba D, Kunicka A (2003) Antibacterial and antifungal properties of essential oils. Curr Med Chem 10:813–829PubMedCrossRefGoogle Scholar
  76. Karamanoli K, Vokou D, Menkissoglu U, Constantinidou HI (2000) Bacterial colonization of phyllosphere of mediterranean aromatic plants. J Chem Ecol 26:2035–2048CrossRefGoogle Scholar
  77. Karamanoli K, Menkissoglu-Spiroudi U, Bosabalidis AM, Vokou D, Constantinidou HIA (2005) Bacterial colonization of the phyllosphere of nineteen plant species and antimicrobial activity of their leaf secondary metabolites against leaf associated bacteria. Chemoecology 15:59–67CrossRefGoogle Scholar
  78. Karamanoli K, Thalassinos G, Karpouzas D, Bosabalidis AM, Vokou D, Constantinidou HI (2012) Are leaf glandular trichomes of Oregano hospitable habitats for bacterial growth? J Chem Ecol 38:476–485PubMedCrossRefGoogle Scholar
  79. Karapinar M, Aktug SE (1987) Inhibition of foodborne pathogens by thymol, eugenol, menthol and anethole. Int J Food Microbiol 4:161–166CrossRefGoogle Scholar
  80. Kessler D, Baldwin IT (2007) Making sense of nectar scents: the effects of nectar secondary metabolites on floral visitors of Nicotiana attenuata. Plant J 49:840–854PubMedCrossRefGoogle Scholar
  81. Kim YS, Park SJ, Lee EJ, Cerbo RM, Lee SM, Ryu CH, Kim GS, Kim JO, Ha YL (2008) Antibacterial compounds from Rose Bengal-sensitized photooxidation of beta-caryophyllene. J Food Sci 73:C540–C545PubMedCrossRefGoogle Scholar
  82. Kleinheinz GT, Bagley ST, St John WP, Rughani JR, McGinnis GD (1999) Characterization of alpha-pinene-degrading microorganisms and application to a bench-scale biofiltration system for VOC degradation. Arch Environ Contam Toxicol 37:151–157PubMedCrossRefGoogle Scholar
  83. Knudsen JT, Eriksson R, Gershenzon J, Stahl B (2006) Diversity and distribution of floral scent. Bot Rev 72:1–120CrossRefGoogle Scholar
  84. Kpoviessi DSS, Gbenou JD, Gbaguidi FA, Ahoussi L, Accrombessi GC, Moudachirou M, Quetin-Leclercq J (2009) Justicia anselliana (Nees) T. Anders essential oils compounds and allelopathic effects on cowpea Vigna unguiculata (L.) Walp plant. J Essent Oil Res 21:83–88CrossRefGoogle Scholar
  85. Kubo I, Muroi H, Himejima M (1992) Antimicrobial activity of green tea flavor components and their combination effects. J Agric Food Chem 40:245–248CrossRefGoogle Scholar
  86. Lachance MA, Starmer WT, Rosa CA, Bowles JM, Barker JSF, Janzen DH (2001) Biogeography of the yeasts of ephemeral flowers and their insects. FEMS Yeast Res 1:1–8PubMedGoogle Scholar
  87. Lambais MR, Crowley DE, Cury JC, Bull RC, Rodrigues RR (2006) Bacterial diversity in tree canopies of the Atlantic forest. Science 312:1917PubMedCrossRefGoogle Scholar
  88. Leitner M, Kaiser R, Hause B, Boland W, Mithofer A (2010) Does mycorrhization influence herbivore-induced volatile emission in Medicago truncatula? Mycorrhiza 20:89–101PubMedCrossRefGoogle Scholar
  89. Leroy PD, Sabri A, Heuskin S, Thonart P, Lognay G, Verheggen FJ, Francis F, Brostaux Y, Felton GW, Haubruge E (2011) Microorganisms from aphid honeydew attract and enhance the efficacy of natural enemies. Nat Commun 2Google Scholar
  90. Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883PubMedCrossRefGoogle Scholar
  91. Lindow SE, Arny DC, Upper CD (1978) Distribution of ice nucleation-active bacteria on plants in nature. Appl Environ Microbiol 36:831–838PubMedGoogle Scholar
  92. Lindström ES, Langenheder S (2012) Local and regional factors influencing bacterial community assembly. Environ Microbiol Rep 4:1–9PubMedCrossRefGoogle Scholar
  93. Lokvam J, Braddock JF (1999) Anti-bacterial function in the sexually dimorphic pollinator rewards of Clusia grandiflora (Clusiaceae). Oecologia 119:534–540CrossRefGoogle Scholar
  94. Luciano FB, Holley RA (2009) Enzymatic inhibition by allyl isothiocyanate and factors affecting its antimicrobial action against Escherichia coli O157:H7. Int J Food Microbiol 131:240–245PubMedCrossRefGoogle Scholar
  95. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, del Rio TG et al (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86PubMedCrossRefGoogle Scholar
  96. Madhaiyan M, Poonguzhali S, Lee HS, Hari K, Sundaram SP, Sa TM (2005) Pink-pigmented facultative methylotrophic bacteria accelerate germination, growth and yield of sugarcane clone Co86032 (Saccharum officinarum L.). Biol Fertil Soils 41:350–358CrossRefGoogle Scholar
  97. Madhaiyan M, Poonguzhali S, Kwon SW, Sa TM (2009) Methylobacterium phyllosphaerae sp nov., a pink-pigmented, facultative methylotroph from the phyllosphere of rice. Int J Syst Evol Microbiol 59:22–27PubMedCrossRefGoogle Scholar
  98. Matsui K (2006) Green leaf volatiles: hydroperoxide lyase pathway of oxylipin metabolism. Curr Opin Plant Biol 9:274–280PubMedCrossRefGoogle Scholar
  99. Miron T, Rabinkov A, Mirelman D, Wilchek M, Weiner L (2000) The mode of action of allicin: its ready permeability through phospholipid membranes may contribute to its biological activity. Biochim Biophys Acta-Biomembranes 1463:20–30CrossRefGoogle Scholar
  100. Oldroyd GED (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11:252–263PubMedCrossRefGoogle Scholar
  101. Osbourn AE, Qi XQ, Townsend B, Qin B (2003) Dissecting plant secondary metabolism - constitutive chemical defences in cereals. New Phytol 159:101–108CrossRefGoogle Scholar
  102. Östman Ö, Drakare S, Kritzberg ES, Langenheder S, Logue JB, Lindström ES (2010) Regional invariance among microbial communities. Ecol Lett 13:118–127PubMedCrossRefGoogle Scholar
  103. Owen SM, Clark S, Pompe M, Semple KT (2007) Biogenic volatile organic compounds as potential carbon sources for microbial communities in soil from the rhizosphere of Populus tremula. FEMS Microbiol Lett 268:34–39PubMedCrossRefGoogle Scholar
  104. Papadopoulou K, Melton RE, Leggett M, Daniels MJ, Osbourn AE (1999) Compromised disease resistance in saponin-deficient plants. Proc Natl Acad Sci USA 96:12923–12928PubMedCrossRefGoogle Scholar
  105. Parveen M, Hasan MK, Takahashi J, Murata Y, Kitagawa E, Kodama O, Iwahashi H (2004) Response of Saccharomyces cerevisiae to a monoterpene: evaluation of antifungal potential by DNA microarray analysis. J Antimicrob Chemother 54:46–55PubMedCrossRefGoogle Scholar
  106. Piesik D, Lemnczyk G, Skoczek A, Lamparski R, Bocianowski J, Kotwica K, Delaney KJ (2011) Fusarium infection in maize: Volatile induction of infected and neighboring uninfected plants has the potential to attract a pest cereal leaf beetle, Oulema melanopus. J Plant Physiol 168:1534–1542PubMedCrossRefGoogle Scholar
  107. Pineda A, Soler R, Weldegergis BT, Shimwela MM, Van Loon JJA, Dicke M (2013) Non-pathogenic rhizobacteria interfere with the attraction of parasitoids to aphid-induced plant volatiles via jasmonic acid signalling. Plant Cell Environ 36:393–404PubMedCrossRefGoogle Scholar
  108. Radulovic NS, Blagojevic PD, Stojanovic-Radic ZZ, Stojanovic NM (2013) Antimicrobial plant metabolites: structural diversity and mechanism of action. Curr Med Chem 20:932–952PubMedGoogle Scholar
  109. Raguso RA (2008) Wake up and smell the roses: The ecology and evolution of floral scent. Annu Rev Ecol Evol Syst 39:549–569CrossRefGoogle Scholar
  110. Rapparini F, Llusia J, Penuelas J (2008) Effect of arbuscular mycorrhizal (AM) colonization on terpene emission and content of Artemisia annua L. Plant Biol 10:108–122PubMedCrossRefGoogle Scholar
  111. Reinhold-Hurek B, Hurek T (2011) Living inside plants: bacterial endophytes. Curr Opin Plant Biol 14:435–443PubMedCrossRefGoogle Scholar
  112. Ro DK, Ehlting J, Keeling CI, Lin R, Mattheus N, Bohlmann J (2006) Microarray expression profiling and functional characterization of AtTPS genes: Duplicated Arabidopsis thaliana sesquiterpene synthase genes At4g13280 and At4g13300 encode root-specific and wound-inducible (Z)-γ-bisabolene synthases. Arch Biochem Biophys 448:104–116PubMedCrossRefGoogle Scholar
  113. Rossi PG, Bao L, Luciani A, Panighi J, Desjobert JM, Costa J, Casanova J, Bolla JM, Berti L (2007) (E)-Methylisoeugenol and elemicin: antibacterial components of Daucus carota L. essential oil against Campylobacter jejuni. J Agric Food Chem 55:7332–7336PubMedCrossRefGoogle Scholar
  114. 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 100:4927–4932PubMedCrossRefGoogle Scholar
  115. Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Pare PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026PubMedCrossRefGoogle Scholar
  116. Seco R, Penuelas J, Filella I (2007) Short-chain oxygenated VOCs: Emission and uptake by plants and atmospheric sources, sinks, and concentrations. Atmos Environ 41:2477–2499CrossRefGoogle Scholar
  117. Shade A, McManus PS, Handelsman J (2013) Unexpected diversity during community succession in the apple flower microbiome. MBio 4:e00602–e00612PubMedCrossRefGoogle Scholar
  118. Simic N, Palic R, Randjelovic V (2005) Composition and antibacterial activity of Achillea clypeolata essential oil. Flavour Fragr J 20:127–130CrossRefGoogle Scholar
  119. Soler R, Van der Putten WH, Harvey JA, Vet LEM, Dicke M, Bezemer TM (2012) Root herbivore effects on aboveground multitrophic interactions: Patterns, processes, and mechanisms. J Chem Ecol 38:755–767PubMedCrossRefGoogle Scholar
  120. Song YY, Ye M, Li CY, Wang RL, Wei XC, Luo SM and Zeng RS (2013) Priming of anti-herbivore defense in tomato by arbuscular mycorrhizal fungus and involvement of the jasmonate pathway. J Chem Ecol, this volumeGoogle Scholar
  121. Spor A, Koren O, Ley R (2011) Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol 9:279–290PubMedCrossRefGoogle Scholar
  122. Steeghs M, Bais HP, de Gouw J, Goldan P, Kuster W, Northway M, Fall R, Vivanco JM (2004) Proton-transfer-reaction mass spectrometry as a new tool for real time analysis of root-secreted volatile organic compounds in Arabidopsis. Plant Physiol 135:47–58PubMedCrossRefGoogle Scholar
  123. Sy A, Timmers ACJ, Knief C, Vorholt JA (2005) Methylotrophic metabolism is advantageous for Methylobacterium extorquens during colonization of Medicago truncatula under competitive conditions. Appl Environ Microbiol 71:7245–7252PubMedCrossRefGoogle Scholar
  124. Tholl D, Lee S (2011) Terpene specialized metabolism in Arabidopsis thaliana. The Arabidopsis book: 9:e0143Google Scholar
  125. Tholl D, Chen F, Petri J, Gershenzon J, Pichersky E (2005) Two sesquiterpene synthases are responsible for the complex mixture of sesquiterpenes emitted from Arabidopsis flowers. Plant J 42:757–771PubMedCrossRefGoogle Scholar
  126. Tholl D, Sohrabi R, Huh J-H, Lee S (2011) The biochemistry of homoterpenes – Common constituents of floral and herbivore-induced plant volatile bouquets. Phytochemistry 72:1635–1646PubMedCrossRefGoogle Scholar
  127. Toome M, Randjarv P, Copolovici L, Niinemets U, Heinsoo K, Luik A, Noe SM (2010) Leaf rust induced volatile organic compounds signalling in willow during the infection. Planta 232:235–243PubMedCrossRefGoogle Scholar
  128. Tripathi NN, Mishra AK, Tripathi S (2011) Antibacterial potential of plant volatile oils: A review. Proc Nat Acad Sci India B-Biol Sci 81:23–68Google Scholar
  129. Turlings TCJ, Hiltpold I, Rasmann S (2012) The importance of root-produced volatiles as foraging cues for entomopathogenic nematodes. Plant Soil 358:47–56CrossRefGoogle Scholar
  130. Ultee A, Kets EPW, Smid EJ (1999) Mechanisms of action of carvacrol on the food-borne pathogen Bacillus cereus. Appl Environ Microbiol 65:4606–4610PubMedGoogle Scholar
  131. Ultee A, Slump RA, Steging G, Smid EJ (2000) Antimicrobial activity of carvacrol toward Bacillus cereus on rice. J Food Prot 63:620–624PubMedGoogle Scholar
  132. Unsicker SB, Kunert G, Gershenzon J (2009) Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Curr Opin Plant Biol 12:479–485PubMedCrossRefGoogle Scholar
  133. Utama IMS, Wills RBH, Ben-Yehoshua S, Kuek C (2002) In vitro efficacy of plant volatiles for inhibiting the growth of fruit and vegetable decay microorganisms. J Agric Food Chem 50:6371–6377PubMedCrossRefGoogle Scholar
  134. Vaughan MM, Wang Q, Webster FX, Kiemle D, Hong YJ, Tantillo DJ, Coates RM, Wray AT, Askew W, O’Donnell C et al (2013) Formation of the unusual semivolatile diterpene rhizathalene by the Arabidopsis class I terpene synthase TPS08 in the root stele is involved in defense against belowground herbivory. Plant Cell 25:1108–1125PubMedCrossRefGoogle Scholar
  135. Velickovic DT, Randjelovic NV, Ristic MS, Velickovic AS, Smelcerovic AA (2003) Chemical constituents and antimicrobial activity of the ethanol extracts obtained from the flower, leaf and stem of Salvia officinalis L. J Serbian Chem Soc 68:17–24CrossRefGoogle Scholar
  136. Vilela GR, de Almeida GS, D’Arce M, Moraes MHD, Brito JO, da Silva M, Silva SC, Piedade SMD, Calori-Domingues MA, da Gloria EM (2009) Activity of essential oil and its major compound, 1,8-cineole, from Eucalyptus globulus Labill., against the storage fungi Aspergillus flavus Link and Aspergillus parasiticus Speare. J Stored Prod Res 45:108–111CrossRefGoogle Scholar
  137. Vokou D, Vareli K, Zarali E, Karamanoli K, Constantinidou HIA, Monokrousos N, Halley JM, Sainis I (2012) Exploring biodiversity in the bacterial community of the mediterranean phyllosphere and its relationship with airborne bacteria. Microb Ecol 64:714–724PubMedCrossRefGoogle Scholar
  138. Vorholt JA (2012) Microbial life in the phyllosphere. Nat Rev Microbiol 10:828–840PubMedCrossRefGoogle Scholar
  139. Walsh SE, Maillard JY, Russell AD, Catrenich CE, Charbonneau DL, Bartolo RG (2003) Activity and mechanisms of action of selected biocidal agents on Gram-positive and -negative bacteria. J Appl Microbiol 94:240–247PubMedCrossRefGoogle Scholar
  140. Wardhaugh CW, Stork NE, Edwards W, Grimbacher PS (2012) The overlooked biodiversity of flower-visiting invertebrates. PLoS One 7:e45796PubMedCrossRefGoogle Scholar
  141. Wellner S, Lodders N, Kampfer P (2011) Diversity and biogeography of selected phyllosphere bacteria with special emphasis on Methylobacterium spp. Syst Appl Microbiol 34:621–630PubMedCrossRefGoogle Scholar
  142. Wenda-Piesik A, Piesik D, Ligor T, Buszewski B (2010) Volatile organic compounds (VOCs) from cereal plants infested with crown rot: their identity and their capacity for inducing production of VOCs in uninfested plants. Int J Pest Manage 56:377–383CrossRefGoogle Scholar
  143. Wenke K, Kai M, Piechulla B (2010) Belowground volatiles facilitate interactions between plant roots and soil organisms. Planta 231:499–506PubMedCrossRefGoogle Scholar
  144. Wenke K, Wanke D, Kilian J, Berendzen K, Harter K, Piechulla B (2012) Volatiles of two growth-inhibiting rhizobacteria commonly engage AtWRKY18 function. Plant J 70:445–459PubMedCrossRefGoogle Scholar
  145. Weston LA, Mathesius U (2013) Flavonoids: their structure, biosynthesis and role in the rhizosphere, including allelopathy. J Chem Ecol 39:283–297PubMedCrossRefGoogle Scholar
  146. Whipps JM, Hand P, Pink D, Bending GD (2008) Phyllosphere microbiology with special reference to diversity and plant genotype. J Appl Microbiol 105:1744–1755PubMedCrossRefGoogle Scholar
  147. Wiggins P (2004) Effiux pumps: an answer to Gram-negative bacterial resistance? Expert Opin Investg Drugs 13:899–902CrossRefGoogle Scholar
  148. Wilson M, Lindow SE (1994) Coexistence among epiphytic bacterial populations mediated through nutritional resource partitioning. Appl Environ Microbiol 60:4468–4477PubMedGoogle Scholar
  149. Wright GA, Schiestl FP (2009) The evolution of floral scent: the influence of olfactory learning by insect pollinators on the honest signalling of floral rewards. Funct Ecol 23:841–851CrossRefGoogle Scholar
  150. Yadav RKP, Karamanoli K, Vokou D (2005) Bacterial colonization of the phyllosphere of Mediterranean perennial species as influenced by leaf structural and chemical features. Microb Ecol 50:185–196PubMedCrossRefGoogle Scholar
  151. Yadav RKP, Papatheodorou EM, Karamanoli K, Constantinidou HIA, Vokou D (2008) Abundance and diversity of the phyllosphere bacterial communities of Mediterranean perennial plants that differ in leaf chemistry. Chemoecology 18:217–226CrossRefGoogle Scholar
  152. Yeo YS, Nybo SE, Chittiboyina AG, Weerasooriya AD, Wang YH, Gongora-Castillo E, Vaillancourt B, Buell CR, DellaPenna D, Celiz MD et al (2013) Functional identification of valerena-1,10-diene synthase, a terpene synthase catalyzing a unique chemical cascade in the biosynthesis of biologically active sesquiterpenes in Valeriana officinalis. J Biol Chem 288:3163–3173PubMedCrossRefGoogle Scholar
  153. Zamioudis C, Pieterse CMJ (2012) Modulation of host immunity by beneficial microbes. Mol Plant-Microbe Interact 25:139–150PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Department of Organismic BiologyUniversity SalzburgSalzburgAustria
  2. 2.Department of Biological SciencesVirginia TechBlacksburgUSA

Personalised recommendations