Skip to main content
Log in

Belowground volatiles facilitate interactions between plant roots and soil organisms

  • Review
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Many interactions between organisms are based on the emission and perception of volatiles. The principle of using volatile metabolites as communication signals for chemo-attractant or repellent for species-specific interactions or mediators for cell-to-cell recognition does not stop at an apparently unsuitable or inappropriate environment. These infochemicals do not only diffuse through the atmosphere to process their actions aboveground, but belowground volatile interactions are similarly complex. This review summarizes various eucaryotes (e.g., plant (roots), invertebrates, fungi) and procaryotes (e.g., rhizobacteria) which are involved in these volatile-mediated interactions. The soil volatiles cannot be neglected anymore, but have to be considered in the future as valuable infochemicals to understand the entire integrity of the ecosystems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Abbreviations

VOC:

Volatile organic compound

References

  • Almenar E, Auras R, Wharton P, Rubino M, Harte B (2007) Release of acetaldehyde from β-cyclodextrins inhibits postharvest decay fungi in vitro. J Agric Food Chem 55:7205–7212

    Article  PubMed  CAS  Google Scholar 

  • Aochi YO, Farmer WJ (2005) Impact of soil microstructure on the molecular transport dynamics of 1, 2-dichlorethane. Geoderma 127:137–153

    Article  CAS  Google Scholar 

  • Aratchige NS, Lesna I, Sabelis MW (2004) Below-ground plant parts emit herbivore-induced volatiles: olfactory responses of a predatory mite to tulip bulb infested by rust mites. Exp Appl Acarol 33:21–30

    Article  PubMed  CAS  Google Scholar 

  • Asensio D, Penuelas J, Filella I, Llusia J (2007) On-line screening of soil VOCs exchange responses to moisture, temperature and root presence. Plant Soil 291:249–261

    Article  CAS  Google Scholar 

  • Banchio E, Xie X, Zhang H, Pare PW (2009) Soil bacteria elevate essential oil accumulation and emissions in sweet basil. J Agric Food Chem 57:653–657

    Article  PubMed  CAS  Google Scholar 

  • Barber DA, Martin JK (1976) The release of organic substances by cereal roots into soil. New Phytol 76:69–80

    Article  CAS  Google Scholar 

  • Bauske EM, Rodríguez-Kábana R, Estaun V, Kloepper JW, Robertson DG, Weaver CF, King PS (1994) Management of Meloidogyne incognita on cotton by use of botanical aromatic compounds. Nematropica 24:143–150

    Google Scholar 

  • Bécard G, Piché Y (1989) Fungal growth stimulation by CO2 and root exudates in vesicular–arbuscular mycorrhizal symbiosis. Appl Environ Microbiol 55:2320–2325

    PubMed  Google Scholar 

  • Bertin C, Ynag X, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83

    Article  CAS  Google Scholar 

  • Bertoli A, Pistelli L, Morelli I, Fraternale D, Giamperi L, Ricci D (2004) Volatile constituents of different parts (roots, stems and leaves) of Smyrnium olusatrum L. Flavour Fragr J 19:522–525

    Article  CAS  Google Scholar 

  • Boff MIC, Zoon FC, Smits PH (2001) Orientation of Heterorhabditis megidis to insect hosts and plant roots in a Y-tube sand olfactometer. Entomologia Experimentalis et Applicata 98:329–337

    Article  Google Scholar 

  • Borg–Karlson AK, Englund FO, Unelius CR (1994) Dimethyloligosulphide, major volatiles released from Sauromatum guttatum and Phallus impudicus. Phytochem 35:321–323

    Article  Google Scholar 

  • Branson TF (1982) Olfactory response of larvae of Diabrotica virgifera virgifera to plant roots. Entomol Appl 31:303–307

    Article  Google Scholar 

  • Breheret S, Talou T, Rapior S, Bessiere JM (1999) Geosmin, a sesquiterpenoid compound responsible for the musty-earthy odor of Cortinarius herculeus, Cystoderma amianthinum, and Cy. carcharias. Mycologia 91:117–120

    Article  CAS  Google Scholar 

  • Buzzini P, Gasparetti C, Turchetti B, Cramarossa MR, Vaughan-Martini A, Martini A, Pagnoni UM, Forti L (2005) Production of volatile organic compounds (VOCs) by yeasts isolated from the ascocarps of black (Tuber melanosporum Vitt.) and white (Tuber magnatum Pico) truffles. Arch Microbiol 184:187–193

    Article  PubMed  CAS  Google Scholar 

  • Carson JF, Wong FF (1961) The volatile flavour components of onions. J Agric Food Chem 9:140–143

    Article  CAS  Google Scholar 

  • Chaurasia B, Pandey A, Palni LMS, Trivedi P, Kumar B, Colvin N (2005) Diffusible and volatile compounds produced by an antagonistic Bacillus subtilis strain cause structural deformations in pathogenic fungi in vitro. Microbiol Res 160:75–81

    Article  PubMed  CAS  Google Scholar 

  • Cheng SS, Liu JY, Chang EH, Chang ST (2008) Antifungal activity of cinnamaldehyde and eugenol congeners against wood-rot fungi. Bioresour Technol 99:5145–5149

    Article  PubMed  CAS  Google Scholar 

  • Chitarra GS, Abee T, Rombouts FM, Posthumus MA, Dijksterhuis J (2004) Germination of Penicillium paneum conidia is regulated by 1-octen-3-ol, a volatile self-inhibitor. Appl Environ Microbiol 70:2823–2829

    Article  PubMed  CAS  Google Scholar 

  • Chuankun X, Minghe M, Leming Z, Keqin Z (2004) Soil volatile fungistasis and volatile fungistatic compounds. Soil Biol Biochemi 36:1997–2004

    Article  CAS  Google Scholar 

  • Cobb FW Jr, Krstic M, Zavarin E, Barber HW Jr (1968) Inhibitory effects of volatile oleoresin components on Fomes annosus and four Ceratocystis species. Phytopathol 58:1327–1335

    CAS  Google Scholar 

  • Darriet P, Pons M, Lamy S, Dubourdieu D (2000) Identification and quantification of geosmin, a powerful earthy odorant contaminating wines. J Agric Food Chem 48:4835–4838

    Article  PubMed  CAS  Google Scholar 

  • Dickschat JS, Wenzel SC, Bode HB, Müller R, Schulz S (2004) Biosynthesis of volatiles by the myxobacterium Myxococcus xanthus. Chem Bio Chem 5:778–787

    PubMed  CAS  Google Scholar 

  • Dickschat JS, Bode HB, Mahmud T, Müller R, Schulz S (2005a) A novel type of geosmin biosynthesis in myxobacteria. J Org Chem 70:5174–5182

    Article  PubMed  CAS  Google Scholar 

  • Dickschat JS, Martens T, Brinkhoff T, Simon M, Schulz S (2005b) Volatiles Released by a Streptomyces species isolated from the North Sea. Chem Biodivers 2:837–865

    Article  PubMed  CAS  Google Scholar 

  • Doane JF, Lee YW, Klinger J, Westcott ND (1975) The orientation response of Ctenicera destructor and other wireworms (Coleoptera: Elateridae) to germinating grain and to carbon dioxide. Can Entomol 107:1233–1252

    Article  Google Scholar 

  • Duponnois R, Kisa M (2006) The possible role of trehalose in the mycorrhiza helper bacterium effect. Can J Bot 84:1005–1008

    Article  Google Scholar 

  • Dusenbery DB (1987) Theoretical range over which bacteria and nematodes could use carbon dioxide to locate plant roots. J Chem Ecol 13:1617–1624

    Article  Google Scholar 

  • Effmert U, Buss D, Rohrbeck D, Piechulla B (2006) Localization of the synthesis and emission of scent compounds within the flower. In: Dudareva N, Pichersky E (eds) Floral scents. CRC Press Taylor and Francis Group, London, pp 105–124

    Google Scholar 

  • Farag MA, Ryu CM, Sumner LW, Pare PW (2006) GC-MS SPME profiling of rhizobacterial volatiles reveals prospective inducers of growth promotion and induces systemic resistance in plants. Phytochem 67:2262–2268

    Article  CAS  Google Scholar 

  • Fernando WGD, Ramarathnam R, Krishnamoorthy AS, Syvchuk SC (2005) Identification and use of potential bacterial organic antifungal volatiles in biocontrol. Soil Biol Biochem 37:955–964

    Article  CAS  Google Scholar 

  • Fiddaman PJ, Rossall S (1993) The production of antifungal volatiles by Bacillus subtilis. J Appl Microbiol 74:119–126

    Article  CAS  Google Scholar 

  • Fiddaman PJ, Rossall S (1994) Effect of substrate on the production of antifungal volatiles from Bacillus subtilis. J Appl Microbiol 76:395–405

    Article  CAS  Google Scholar 

  • Gerber NN (1968) Geosmin, from microorganisms, is trans-1, 10-dimethyltrans-9-decalol. Tetrahedr Lett 25:2971–2974

    Article  Google Scholar 

  • Gerber NN, Lechevalier HA (1965) Geosmin, an earthy-smelling substance isolated from Actinomycetes. Appl Microbiol 13:935–938

    PubMed  CAS  Google Scholar 

  • Gioacchini AM, Menotta M, Guescini M, Saltarelli R, Ceccaroli P, Amicucci A, Barbieri e, Giomaro G, Stocchi V (2008) Geographical traceability of Italien white truffle (Tuber magnatum Pico) by the analysis of volatile organic compounds. Rapid Commun Mass Spectrom 22:3147–3153

    Article  PubMed  CAS  Google Scholar 

  • Gu Y, Mo M, Zhou J, Zou C, Zhang K (2007) Evaluation and identification of potential organic nematicidal volatiles from soil bacteria. Soil Biol Biochem 39:2567–2575

    Article  CAS  Google Scholar 

  • Guerin PM, Ryan MF (1980) Insecticidal effect of trans-2-nonenal, a constituent of carrot root. Experientia 36:1387–1388

    Article  CAS  Google Scholar 

  • Guerin PM, Ryan MF (1984) Relationship between root volatiles of some carrot cultivars and their resistance to the carrot fly, Psila rosae. Entomol Exp Appl 36:217–224

    Article  CAS  Google Scholar 

  • Hammer KA, Carson CF, Riley TV (2003) Antifungal activity of the components of Melaleuca alternifolia (tea tree oil). J Appl Microbiol 95:853–860

    Article  PubMed  CAS  Google Scholar 

  • Hayes TS, Randle PE, Last FT (1969) The nature of the microbial stimulus affecting sporophore formation in Agaricus bisporus (Lange) Sing. Ann Appl Biol 64:177–187

    Article  Google Scholar 

  • Hayward S, Muncey AE, James AE, Halsall CJ, Hewitt CN (2001) Monoterpene emissions from soil in a sitka spruce forest. Atmos Environ 35:4081–4087

    Article  CAS  Google Scholar 

  • Huber DPW, Philippe RN, Madilao LL, Sturrock RN, Bohlmann J (2005) Changes in anatomy and terpene chemistry in roots of Douglas-fir seedlings following treatment with methyl jasmonate. Tree Physiol 25:1075–1083

    PubMed  CAS  Google Scholar 

  • Humphris SN, Bruce A, Buultjens E, Wheatley RE (2002) The effects of volatile microbial secondary metabolites on the protein synthesis in Serpula lacrymans. FEMS Microbiol Lett 210:215–219

    Article  PubMed  CAS  Google Scholar 

  • Hynes J, Muller CT, Jones TH, Boddy L (2007) Changes in volatile production during the course of fungal mycelial interactions between Hypholoma fasciculare and Resinicium bicolor. J Chem Ecol 33:43–57

    Article  PubMed  CAS  Google Scholar 

  • Izaguirre G, Hwang CJ, Krasner SW, McGuire MJ (1982) Geosmin and 2-methylisoborneol from Cyanobacteria in three water supply systems. Appl Environ Microbiol 43:708–714

    PubMed  CAS  Google Scholar 

  • Johnson SN, Gregory PJ (2006) Chemically mediated host-plant location and selection by root-feeding insects. Physiol Entomol 31:1–13

    Article  CAS  Google Scholar 

  • Johnson SN, Zhang XX, Crawford JW, Gregory PJ, Hix NJ, Jarvis SC, Murray PJ, Young IM (2006) Effects of carbon dioxide on the searching behavior of the root-feeding clover weevil Sitona Lepidus (Coleoptera: Curculionidae). Bulletin Entomol Res 96:361–366

    CAS  Google Scholar 

  • Jones OT, Coaker TH (1977) Oriented responses of carrot fly larvae Psila rosae, to plant odours, carbon dioxide and carrot root volatiles. Physiol Entomol 2:189–197

    Article  CAS  Google Scholar 

  • Kai M, Piechulla B (2009) Plant growth promotions due to rhizobacterial volatiles—an effect of CO2? FEBS Lett 583:3473–3477

    Article  PubMed  CAS  Google Scholar 

  • Kai M, Effmert U, Berg G, Piechulla B (2007) Volatiles of bacterial antagonists inhibit mycelial growth of the plant pathogen Rhizoctonia solani. Arch Microbiol 187:351–360

    Article  PubMed  CAS  Google Scholar 

  • Kai M, Haustein M, Molina F, Petri A, Scholz B, Piechulla B (2009) Bacterial volatiles and their action potential. Appl Microbiol Biotechnol 81:1001–1012

    Article  PubMed  CAS  Google Scholar 

  • Kalemba D, Kusewicz D, Swider K (2002) Antimicrobial properties of the essential oil of Artimisia asiatica Nakai. Phytotherapy Res 16:288–291

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Klinger J (1959) Die Bedeutung der Kohlendioxyd-Ausscheidung der Wurzeln für die Orientierung der Larven von Otiorrhynchus sulcatus F. und anderer bodenbewohnender phytophager Insektenarten. doi:10.3929/ethz-a-000139365

  • Klinger J (1963) Die Orientierung von Ditylenchus dipsaci in gemessenen künstlichen und biologischen CO2-Gradienten. Nematologica 9:185–199

    Article  Google Scholar 

  • Kokalis-Burelle N, Martinez-Ochoa N, Rodríguez-Kabana R, Kloepper JW (2002) Development of multicomponent transplant mixes for suppression of Meloidogyne incognita on tomato (Lycopersicum esculentum). J Nematol 34:362–369

    PubMed  CAS  Google Scholar 

  • Krupa S, Fries N (1971) Studies on ectomycorrhizae of pine. I. Production of volatile organic compounds. Can J Bot 49:1425–1431

    Article  CAS  Google Scholar 

  • Laothawornkitkul J, Taylor JE, Pail ND, Hewitt CN (2009) Biogenic volatile organic compounds in the earth system. New Phytol 183:27–51

    Article  PubMed  CAS  Google Scholar 

  • Lin C, Owen S, Pefiuelas J (2007) Volatile organic compounds in the roots and rhizosphere of Pinus spp. Soil Biol Biochem 39:951–960

    Article  CAS  Google Scholar 

  • Mackie A, Wheatley RE (1999) Effects and incidence of volatile organic compound interactions between soil bacterial and fungal isolates. Soil Biol Biochem 31:375–385

    Article  CAS  Google Scholar 

  • Matsumoto Y (1970) Volatile organic sulfur compounds as insect attractants with special reference to host selection. In: Wood DL, Silverstein RM, Nakajima M (eds) Control of insect behavior by natural products. Academic Press, New York, pp 133–160

    Google Scholar 

  • Mattheis JP, Roberts RG (1992) Identification of geosmin as a volatile metabolite of Penicillium expansum. Appl Environ Microbiol 58:3170–3172

    PubMed  CAS  Google Scholar 

  • McLoughlin E, Rhodes AH, Owen SM, Semple KT (2009) Biogenic volatile organic compounds as a potential stimulator for organic contaminant degradation by soil organisms. Environ Pollut 157:86–94

    Article  PubMed  CAS  Google Scholar 

  • Medsker LL, Jenkins D, Thomas JF (1968) Odorous compounds in natural waters. An earthy-smelling compound associated with blue-green algae and actinomycetes. Environ Sci Technol 2:461–464

    Article  CAS  Google Scholar 

  • Melin E, Krupa S (1971) Studies on ectomycorrhizae of pine II. Growth inhibition of mycorrhizal fungi by volatile organic constituents of Pinus silvestris (Scots Pine) roots. Physiol Plantarum 25(3):337–340

    Article  CAS  Google Scholar 

  • Menotta M, Gioacchini AM, Amicucci A, Buffalini M, Sisti D, Stocchi V (2004) Headspacce solid-phase microextraction with gas chromatography and mass spectrometry in the investigation of volatile organic compounds in an ectomycorrhizae synthesis system. Rapid Commun Mass Spectrom 18:206–210

    Article  PubMed  CAS  Google Scholar 

  • Minerdi D, Bossi S, Gullino ML, Garibaldi A (2009) Volatile organic compounds: a potential direct long-distance mechanism for antagonistic action of Fusarium oxysporum strain MSA 35. Environ Microbiol 11:844–854

    Article  PubMed  CAS  Google Scholar 

  • Muller WH, Muller CH (1964) Volatile growth inhibitors produced by Salvia species. Bull Torrey Bot Club 91:327–330

    Article  CAS  Google Scholar 

  • 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 67:468–478

    Article  PubMed  CAS  Google Scholar 

  • Nardi S, Concheri G, Pizzeghello D, Sturaro A, Rella R, Parvoli G (2000) Soil organic matter mobilization by root exudates. Chemosphere 41:653–658

    Article  PubMed  CAS  Google Scholar 

  • Neveu N, Grandgirard J, Nenon JP, Cortesero AM (2002) Systemic release of herbivore-induced plant volatiles by turnips infested by concealed root-feeding larvae Delia radicum L. J Chem Ecol 28:1717–1732

    Article  PubMed  CAS  Google Scholar 

  • Nordlander G, Eidmann HH, Jacobsson U, Nordenhem H, Sjödin K (1986) Orientation of the pine weevil Hylobius abietis to underground sources of host volatiles. Entomol Exp Appl 41:91–100

    Article  Google Scholar 

  • Oka Y, Nacar S, Putievsky E, Ravid U, Yaniv Z, Spiegel Y (2000) Nematicidal activity of essential oils and their components against the root-knot nematode. Phytopathology 90:710–715

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Oyedemi SO, Okoh AI, Mabinya LV, Pirochenva G, Afolayan AJ (2009) The proposed mechanism of bactericidal action of eugenol, α-terpineol and γ-terpinene against Listeria monocytogenes, Streptococcus pyogenes, Proteus vulgaris and Escherichia coli. African J Biotechnol 8:1280–1286

    CAS  Google Scholar 

  • Paavolainen L, Kitunen V, Smolander A (1998) Inhibition of nitrification in forest soil by monoterpenes. Plant Soil 205:147–154

    Article  CAS  Google Scholar 

  • Paim U, Beckel WE (1963) The carbon dioxide related behaviour of the adults of Orthosoma brunneum. Can J Zool 42:295–304

    Article  Google Scholar 

  • Park MJ, Gwak KS, Yang I, Kim KW, Jeung EB, Chang JW, Choi IG (2009) Effect of citral, eugenol, nerolidol and α-terpineol on the ultrastructural changes of Trichophyton mentagrophytes. Fitoterapia 80(5):290–296

    Article  PubMed  CAS  Google Scholar 

  • Pline M, Dusenbery DB (1987) Responses of plant-parasitic nematode Meloidogyne incognita to carbon dioxide determined by video camera–computer tracking. J Chem Ecol 13:873–888

    Article  Google Scholar 

  • Rasman S, Turlings TCJ (2008) First insights into specificity of belowground tritrophic interactions. Oikos 117:362–369

    Article  Google Scholar 

  • Rasman S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737

    Article  CAS  Google Scholar 

  • Reinecke A, Müller F, Hilker M (2008) Attractiveness of CO2 released by root respiration fades on the background of root exudates. Basic Appl Ecol 9:568–576

    Article  CAS  Google Scholar 

  • Rhodes AH, Owen SM, Semple KT (2007) Biodegradation of 2, 4-dichlorophenol in the presence of volatile organic compounds in soils under different vegetation types. FEMS Microbiol Lett 269:323–330

    Article  PubMed  CAS  Google Scholar 

  • Rohloff J (2002) Volatiles from rhizomes of Rhodiola rosea L. Phytochem 59:655–661

    Article  CAS  Google Scholar 

  • Roshchina VV, Roshchina VD (1993) The excretory function of higher plants. Springer, Berlin

    Google Scholar 

  • Ryan MF, Guerin PM (1982) Behavioural responses of the carrot fly larvae, Psila rosae, to carrot root volatiles. Physiol Ent 7:315–324

    Article  CAS  Google Scholar 

  • Ryu CM, Farag AF, Hu C, Reddy MS, Wei H, Pare PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proceed Natl Acad Sci USA 100:4927–4932

    Article  CAS  Google Scholar 

  • Ryu CM, Farag AF, Hu C, Reddy MS, Kloepper JW, Pare PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026

    Article  PubMed  CAS  Google Scholar 

  • Scher FM, Kloepper JW, Singleton CA (1985) Chemotaxis of fluorescent Pseudomonas spp. to soybean seed exudates in vitro and in soil. Can J Microbiol 31:570–574

    Article  Google Scholar 

  • Schulz S, Dickschat JS (2007) Bacterial volatiles: the smell of small organisms. Nat Prod Rep 24:814–842

    Article  PubMed  CAS  Google Scholar 

  • Selander J, Havukkala I, Kalo P (1976) Olfactory behaviour of Hylobius abietis L. (Col., Curculionidae). II. Response to 3-carene and α-terpineol during three stages of its life cycle. Ann Ent Fenn 42:63–66

    CAS  Google Scholar 

  • Smith RH (1965) Effect of monoterpene vapors on the western pine beetle. J Econ Entomol 58:509–510

    CAS  Google Scholar 

  • Splivallo R, Novero M, Bertea CM, Bossi S, Bonfante P (2007) Truffle volatiles inhibit growth and induce an oxidative burst in Arabidopsis thaliana. New Phytol 175:417–424

    Article  PubMed  CAS  Google Scholar 

  • Splivallo R, Bossi S, Maffei M, Bonfante P (2009a) Discrimination of truffle fruiting body versus mycelial aromas by stir bar sorptive extraction. Phytochemistry 68(20):2584–2598

    Article  CAS  Google Scholar 

  • Splivallo R, Fischer U, Göbel C, Feussner I, Karlovsky P (2009b) Truffles regulate root morphogenesis via the production of auxin and ethylene. Plant Physiol 150:2018–2029

    Article  PubMed  CAS  Google Scholar 

  • Spörle J, Becker H, Allen NS, Gupta MP (1991) Occurrence of (-) geosmin and other terpenoids in an axenic culture of the liverwort Symphyogyna brongniartii. Z Naturforsch 46C:183–188

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Stotzky G, Schenck S (1976) Volatile organic compounds and microorganisms. Critical Rev Microbiol 4:333–382

    Article  CAS  Google Scholar 

  • Strobel GA, Dirkse E, Sears J, Markworth C (2001) Volatile antimicrobials from Muscodor albus, a novel endophytic fungus. Microbiol 147:2943–2950

    CAS  Google Scholar 

  • Sutherland ORW (1972) Olfactory responses of Costelytra zealandica (Coleoptera: Melolonthinae) larvae to grass root odours. New Zealand J Sci 15:165–172

    Google Scholar 

  • Tapia T, Perich F, Pardo F, Palma G, Quiroz A (2007) Identification of volatiles from differently aged red clover (Trifolium pratense) root extracts and behavioural responses of clover root borer (Hylastinus obscurus) (Marsham) (Coleoptera: Scolytidae) to them. Biochem Systemat Ecol 35:61–67

    Article  CAS  Google Scholar 

  • van Tol RWHM, van der Sommen ATC, Boff MIC, van Bezooijen J, Sabelis MW, Smits PH (2001) Plants protect their roots by alerting the enemies of grubs. Ecol Lett 4:292–294

    Article  Google Scholar 

  • Vespermann A, Kai M, Piechulla B (2007) Rhizobacterial volatiles affect the growth of fungi and Arabidopsis thaliana. Appl Environ Microbiol 73:5639–5641

    Article  PubMed  CAS  Google Scholar 

  • Vilela GR, de Almeida GS, D’Arce MABR, Moraes MHD, Brito JO, da Silva MFGF, Silva SC, de Stefano Piedade SM, 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 Products Res 45:108–111

    Article  CAS  Google Scholar 

  • Viles AL, Reese RN (1996) Allelopathic potential of Echinacea angustifolia DC. Environ Exp Bot 36:39–43

    Article  Google Scholar 

  • Weissteiner S, Schütz S (2006) Are different volatile pattern influencing host plant choice of belowground living insects. Mitt Dtsch Ges Allg Angew Ent 15:51–55

    Google Scholar 

  • Wheatley RE (2002) The consequences of volatile organic compound mediated bacterial and fungal interactions. Antonie van Leeuwenhoek 81:357–364

    Article  PubMed  CAS  Google Scholar 

  • Witcosky JJ, Schowalter TD, Hansen EM (1987) Host-derived attractants for the beetles Hylastes nigrinus (Coleoptera: Scolytidae) and Steremnius carinatus (Coleoptera: Curculionidae). Environ Entomol 16:1310–1313

    CAS  Google Scholar 

  • Wolfson JL (1987) Impact of Rhizobium nodules on Sitona hispidulus, the clover root curculio. Entomol Exp Appl 43:237–243

    Article  Google Scholar 

  • Yamamoto Y, Tanaka K, Komori N (1994) Volatile compounds excreted by myxobacteria isolated from lake water and sediments. Jpn J Limnol 55:241–245

    Article  CAS  Google Scholar 

  • Zak JC, Willig MR, Moorhead DL, Wildmann HG (1994) Functional diversity of microbial communities: a quantitative approach. Soil Biol Biochem 26:1101–1108

    Article  Google Scholar 

  • 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 226:839–851

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Xie X, Kim MS, Kornyeyev DA, Holaday s, Pare PW (2008) Soil bacteria augments photosynthetic capacity by increasing photosynthetic efficiency and chlorophyll content in Arabidopsis. Plant J 56:264–273

    Article  PubMed  CAS  Google Scholar 

  • Zou CS, Mo MH, Gu YQ, Zhou JP, Zhang KQ (2007) Possible contributions of volatile-producing bacteria to soil fungistasis. Soil Biol Biochem 39:2371–2379

    Article  CAS  Google Scholar 

Download references

Acknowledgment

The authors thank the DFG for financial support to BP (Pi 153/26-1). We apologize that not all papers presenting additional information to this topic were cited due to space limitations.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Birgit Piechulla.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 63.5 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wenke, K., Kai, M. & Piechulla, B. Belowground volatiles facilitate interactions between plant roots and soil organisms. Planta 231, 499–506 (2010). https://doi.org/10.1007/s00425-009-1076-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-009-1076-2

Keywords

Navigation