Abstract
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.
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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 57:4025–4032
Adler LS (2000) The ecological significance of toxic nectar. Oikos 91:409–420
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 30:41–50
Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827
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 19:320–324
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 7:399–403
Atkinson R, Arey J (2003) Atmospheric degradation of volatile organic compounds. Chem Rev 103:4605–4638
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 21:1482–1497
Baas Becking LGM (1934) Geobiologie of inleiding tot de milieukunde. W.P. Van Stockum & Zoon, The Hague
Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681
Banchio E, Xie XT, Zhang HM, Pare PW (2009) Soil bacteria elevate essential oil accumulation and emissions in sweet basil. J Agric Food Chem 57:653–657
Basim E, Basim H, Ozcan M (2006) Antibacterial activities of Turkish pollen and propolis extracts against plant bacterial pathogens. J Food Eng 77:992–996
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 87:2985–2991
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 63:711–718
Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486
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 68:1–13
Bodenhausen N, Horton MW, Bergelson J (2013) Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLoS One 8:e56329
Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat Commun 1:48
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 3:1243–1257
Bruce TJA, Pickett JA (2011) Perception of plant volatile blends by herbivorous insects - Finding the right mix. Phytochemistry 72:1605–1611
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 488:91–95
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 64:807–838
Carter C, Thornburg RW (2004) Is the nectar redox cycle a floral defense against microbial attack? Trends Plant Sci 9:320–324
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 25:493–502
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 15:481–494
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 135:1956–1966
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 21:1067–1075
Clark L, Mason JR (1985) Use of nest material as insecticidal and anti-pathogenic agents by the European Starling. Oecologia 67:169–176
Cowan MM (1999) Plant products as antimicrobial agents. Clin Microbiol Rev 12:564–582
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 55:6300–6308
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 101:13–24
Davis TS, Crippen TL, Hofstetter RW, and Tomberlin JK (2013) Microbial volatile emissions as insect semiochemicals. J Chem Ecol, this volume
de Carvalho C, de Fonseca MMR (2007) Preventing biofilm formation: promoting cell separation with terpenes. FEMS Microbiol Ecol 61:406–413
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 10:2824–2841
Desbrosses GJ, Stougaard J (2011) Root nodulation: A paradigm for how plant-microbe symbiosis influences host developmental pathways. Cell Host Microbe 10:348–358
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 54:2745–2749
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 55:4863–4870
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 10:1040–1049
Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15:167–175
Dobson HEM, Bergström G (2000) The ecology and evolution of pollen odors. Plant Syst Evol 222:63–87
Dudareva N, Negre F, Nagegowda DA, Orlova I (2006) Plant volatiles: Recent advances and future perspectives. Crit Rev Plant Sci 25:417–440
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
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 38:629–640
Fahlgren C, Hagstrom A, Nilsson D, Zweifel UL (2010) Annual variations in the diversity, viability, and origin of airborne bacteria. Appl Environ Microbiol 76:3015–3025
Fall R, Benson AA (1996) Leaf methanol - The simplest natural product from plants. Trends Plant Sci 1:296–301
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
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 volume
Field B, Osbourn AE (2008) Metabolic diversification-independent assembly of operon-like gene clusters in different plants. Science 320:543–547
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 35:833–843
Fridman S, Izhaki I, Gerchman Y, Halpern M (2012) Bacterial communities in floral nectar. Environ Microbiol Rep 4:97–104
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 63:418–428
Galbally IE, Kirstine W (2002) The production of methanol by flowering plants and the global cycle of methanol. J Atmos Chem 43:195–229
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 47:499–507
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 100:8873–8892
Hardoim PR, van Overbeek LS, van Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471
Heil M, Karban R (2010) Explaining evolution of plant communication by airborne signals. Trends Ecol Evol 25:137–144
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 104:5467–5472
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 20:1152–1168
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 186:722–732
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 70:1645–1650
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 31:1003–1021
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 217:767–775
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 153:1293–1310
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 193:997–1008
Hutchinson GE (1957) Concluding remarks. Cold Spring Harb Symp Quant Biol 22:415–427
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 486:207–214
Ibekwe AM, Grieve CM (2004) Changes in developing plant microbial community structure as affected by contaminated water. FEMS Microbiol Ecol 48:239–248
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 49:1770–1774
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 2:53–62
Johnson SN, Nielsen UN (2012) Foraging in the dark - Chemically mediated host plant location by belowground insect herbivores. J Chem Ecol 38:604–614
Jung SC, Martinez-Medina A, Lopez-Raez, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38:651–664
Junker RR, Höcherl N, Blüthgen N (2010) Responses to olfactory signals reflect network structure of flower-visitor interactions. J Anim Ecol 79:818–823
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 13:918–924
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 27:329–341
Kalemba D, Kunicka A (2003) Antibacterial and antifungal properties of essential oils. Curr Med Chem 10:813–829
Karamanoli K, Vokou D, Menkissoglu U, Constantinidou HI (2000) Bacterial colonization of phyllosphere of mediterranean aromatic plants. J Chem Ecol 26:2035–2048
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 15:59–67
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 38:476–485
Karapinar M, Aktug SE (1987) Inhibition of foodborne pathogens by thymol, eugenol, menthol and anethole. Int J Food Microbiol 4:161–166
Kessler D, Baldwin IT (2007) Making sense of nectar scents: the effects of nectar secondary metabolites on floral visitors of Nicotiana attenuata. Plant J 49:840–854
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–C545
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 37:151–157
Knudsen JT, Eriksson R, Gershenzon J, Stahl B (2006) Diversity and distribution of floral scent. Bot Rev 72:1–120
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 21:83–88
Kubo I, Muroi H, Himejima M (1992) Antimicrobial activity of green tea flavor components and their combination effects. J Agric Food Chem 40:245–248
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 1:1–8
Lambais MR, Crowley DE, Cury JC, Bull RC, Rodrigues RR (2006) Bacterial diversity in tree canopies of the Atlantic forest. Science 312:1917
Leitner M, Kaiser R, Hause B, Boland W, Mithofer A (2010) Does mycorrhization influence herbivore-induced volatile emission in Medicago truncatula? Mycorrhiza 20:89–101
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 2
Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883
Lindow SE, Arny DC, Upper CD (1978) Distribution of ice nucleation-active bacteria on plants in nature. Appl Environ Microbiol 36:831–838
Lindström ES, Langenheder S (2012) Local and regional factors influencing bacterial community assembly. Environ Microbiol Rep 4:1–9
Lokvam J, Braddock JF (1999) Anti-bacterial function in the sexually dimorphic pollinator rewards of Clusia grandiflora (Clusiaceae). Oecologia 119:534–540
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 131:240–245
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 488:86
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 41:350–358
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 59:22–27
Matsui K (2006) Green leaf volatiles: hydroperoxide lyase pathway of oxylipin metabolism. Curr Opin Plant Biol 9:274–280
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 1463:20–30
Oldroyd GED (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11:252–263
Osbourn AE, Qi XQ, Townsend B, Qin B (2003) Dissecting plant secondary metabolism - constitutive chemical defences in cereals. New Phytol 159:101–108
Östman Ö, Drakare S, Kritzberg ES, Langenheder S, Logue JB, Lindström ES (2010) Regional invariance among microbial communities. Ecol Lett 13:118–127
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 268:34–39
Papadopoulou K, Melton RE, Leggett M, Daniels MJ, Osbourn AE (1999) Compromised disease resistance in saponin-deficient plants. Proc Natl Acad Sci USA 96:12923–12928
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 54:46–55
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 168:1534–1542
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 36:393–404
Radulovic NS, Blagojevic PD, Stojanovic-Radic ZZ, Stojanovic NM (2013) Antimicrobial plant metabolites: structural diversity and mechanism of action. Curr Med Chem 20:932–952
Raguso RA (2008) Wake up and smell the roses: The ecology and evolution of floral scent. Annu Rev Ecol Evol Syst 39:549–569
Rapparini F, Llusia J, Penuelas J (2008) Effect of arbuscular mycorrhizal (AM) colonization on terpene emission and content of Artemisia annua L. Plant Biol 10:108–122
Reinhold-Hurek B, Hurek T (2011) Living inside plants: bacterial endophytes. Curr Opin Plant Biol 14:435–443
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 448:104–116
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 55:7332–7336
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
Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Pare PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026
Seco R, Penuelas J, Filella I (2007) Short-chain oxygenated VOCs: Emission and uptake by plants and atmospheric sources, sinks, and concentrations. Atmos Environ 41:2477–2499
Shade A, McManus PS, Handelsman J (2013) Unexpected diversity during community succession in the apple flower microbiome. MBio 4:e00602–e00612
Simic N, Palic R, Randjelovic V (2005) Composition and antibacterial activity of Achillea clypeolata essential oil. Flavour Fragr J 20:127–130
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 38:755–767
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 volume
Spor A, Koren O, Ley R (2011) Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol 9:279–290
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 135:47–58
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 71:7245–7252
Tholl D, Lee S (2011) Terpene specialized metabolism in Arabidopsis thaliana. The Arabidopsis book: 9:e0143
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 42:757–771
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 72:1635–1646
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 232:235–243
Tripathi NN, Mishra AK, Tripathi S (2011) Antibacterial potential of plant volatile oils: A review. Proc Nat Acad Sci India B-Biol Sci 81:23–68
Turlings TCJ, Hiltpold I, Rasmann S (2012) The importance of root-produced volatiles as foraging cues for entomopathogenic nematodes. Plant Soil 358:47–56
Ultee A, Kets EPW, Smid EJ (1999) Mechanisms of action of carvacrol on the food-borne pathogen Bacillus cereus. Appl Environ Microbiol 65:4606–4610
Ultee A, Slump RA, Steging G, Smid EJ (2000) Antimicrobial activity of carvacrol toward Bacillus cereus on rice. J Food Prot 63:620–624
Unsicker SB, Kunert G, Gershenzon J (2009) Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Curr Opin Plant Biol 12:479–485
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 50:6371–6377
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 25:1108–1125
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 68:17–24
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 45:108–111
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 64:714–724
Vorholt JA (2012) Microbial life in the phyllosphere. Nat Rev Microbiol 10:828–840
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 94:240–247
Wardhaugh CW, Stork NE, Edwards W, Grimbacher PS (2012) The overlooked biodiversity of flower-visiting invertebrates. PLoS One 7:e45796
Wellner S, Lodders N, Kampfer P (2011) Diversity and biogeography of selected phyllosphere bacteria with special emphasis on Methylobacterium spp. Syst Appl Microbiol 34:621–630
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 56:377–383
Wenke K, Kai M, Piechulla B (2010) Belowground volatiles facilitate interactions between plant roots and soil organisms. Planta 231:499–506
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 70:445–459
Weston LA, Mathesius U (2013) Flavonoids: their structure, biosynthesis and role in the rhizosphere, including allelopathy. J Chem Ecol 39:283–297
Whipps JM, Hand P, Pink D, Bending GD (2008) Phyllosphere microbiology with special reference to diversity and plant genotype. J Appl Microbiol 105:1744–1755
Wiggins P (2004) Effiux pumps: an answer to Gram-negative bacterial resistance? Expert Opin Investg Drugs 13:899–902
Wilson M, Lindow SE (1994) Coexistence among epiphytic bacterial populations mediated through nutritional resource partitioning. Appl Environ Microbiol 60:4468–4477
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 23:841–851
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 50:185–196
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 18:217–226
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 288:3163–3173
Zamioudis C, Pieterse CMJ (2012) Modulation of host immunity by beneficial microbes. Mol Plant-Microbe Interact 25:139–150
Acknowledgments
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.).
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Robert R. Junker and Dorothea Tholl contributed equally to the manuscript.
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Junker, R.R., Tholl, D. Volatile Organic Compound Mediated Interactions at the Plant-Microbe Interface. J Chem Ecol 39, 810–825 (2013). https://doi.org/10.1007/s10886-013-0325-9
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DOI: https://doi.org/10.1007/s10886-013-0325-9