Biocommunication of Plants pp 327-347 | Cite as
Bacterial Volatiles Mediating Information Between Bacteria and Plants
Abstract
At present, more than 400 volatiles are known to appear in bacterial headspace samples, but more are expected as more bacteria will be investigated and several identification technologies will be applied. A comprehensive list of bacteria and their respective effects on plants were presented. The volatiles emitted from Serratia plymuthica HRO-C48 and Stenotrophomonas maltophilia R3089 retarded leaf and root development of Arabidopsis thaliana starting at day 2 of cocultivation, while first signs of activation of stress promoters appeared already after 18 h. Most A. thaliana ecotypes reacted similar to the volatiles of S. plymuthica, but a stronger root growth inhibition was observed for the accession C24. β-Phenyl-ethanol was identified as one compound of the S. plymuthica volatile mixture inhibiting the growth of Arabidopsis thaliana.
Keywords
Evans Blue Dual Culture Volatile Emission Dual Culture Assay Thaliana EcotypeReferences
- Allardyce RA, Langford VS, Hill AL, Murdoch DR (2006) Detection of volatile metabolites produced by bacterial growth in blood culture media by selected ion flow tube mass spectrometry (SIFT-MS). J Microbiol Methods 65:361–365PubMedCrossRefGoogle Scholar
- Arthur CL, Pawliszyn J (1990) Solid phase microextraction with thermal desorption using fused silica optical fibers. Anal Chem 62:2145–2148CrossRefGoogle Scholar
- Bais HP, Fall R, Vivanco JM (2004) Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol 134:307–319PubMedCrossRefGoogle 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 57:653–657PubMedCrossRefGoogle Scholar
- Berg G, Roskot N, Steidle A, Eberl L, Zock A, Smalla K (2002) Plant-dependent genotypic and phenotypic diversity of antagonistic rhizobacteria isolated from different Verticillium host plants. Appl Environ Microbiol 68:3328–3338PubMedCrossRefGoogle Scholar
- Bloemberg GV, Wijfjes AHM, Lamers GEM, Stuurman N, Lugtenberg BJJ (2000) Simultaneous imaging of Pseudomonas fluorescens WCS365 populations expressing three different autofluorescent proteins in the rhizosphere: new perspectives for studying microbial communities. Mol Plant Microbe Interact 13:1170–1176PubMedCrossRefGoogle Scholar
- Blom D, Fabbri C, Eberl L, Weisskopf L (2011) Volatile-mediated killing of Arabidopsis thaliana by bacteria is mainly mediated due to hydrogen cyanide. Appl Environ Microbiol 77:1000–1008PubMedCrossRefGoogle Scholar
- Blumer C, Haas D (2000) Mechanism, regulation, and ecological role of bacterial cyanide biosynthesis. Arch Microbiol 173:170–177PubMedCrossRefGoogle Scholar
- Boland W, Ney P, Jaenicke L, Gassmann G (1984) A “closed-loop-stripping” technique as a versatile tool for metabolic studies of volatiles. In: Schreier P (ed) Analysis of volatiles. Walter De Gruyter & Co, D-Berlin, New York, pp 371–380Google Scholar
- Britto DT, Kronzucker HJ (2002) NH4—toxicity in higher plants: a critical review. J Plant Physiol 159:567–584CrossRefGoogle Scholar
- Bunge M, Araghipour N, Mikoviny T, Dunkl J, Schnitzhofer R, Hansel A, Schinner F, Wisthaler A, Margesin R, Märk TD (2008) On-line monitoring of microbial volatile metabolites by proton transfer reaction-mass spectrometry. Appl Environ Microbiol 74:2179–2186PubMedCrossRefGoogle Scholar
- Carroll W, Lenney W, Wang TS, Spanel P, Alcock A, Smith D (2005) Detection of volatile compounds emitted by Pseudomonas aeruginosa using selected ion flow tube mass spectrometry. Pediatr Pulmonol 39:452–456PubMedCrossRefGoogle Scholar
- Cho SM, Kang BR, Han SH, Anderson AJ, Park JY, Lee YH, Cho BH, Yang KY, Ryu CM, Kim YC (2008) 2R,3R-Butanediol, a bacterial volatile produced by Pseudomonas chlororaphis O6, is involved in induction of systemic tolerance to drought in Arabidopsis thaliana. Mol Plant–Microbe Interact 21:1067–1075PubMedCrossRefGoogle Scholar
- Chuankun X, Minghe M, Leming Z, Kegin Z (2004) Soil volatile fungistasis and volatile fungistatic compounds. Soil Biol Biochem 36:1997–2004CrossRefGoogle Scholar
- Dickschat JS, Wenzel SC, Bode HB, Müller R, Schulz S (2004) Biosynthesis of volatiles by the myxobacterium Myxococcus Xanthus. Chem Biol Chem 5:778–787Google Scholar
- Dickschat JS, Martens R, Brinkhoff T, Simon M, Schulz S (2005) Volatiles released by a Streptomyces species isolated from the North Sea. Chem Biodivers 2:837–865PubMedCrossRefGoogle Scholar
- Dugravot S, Grolleau F, Macherel D, Rochetaing A, Hue B, Stankiewicz M, Huignard J, Lapied B (2003) Dimethyl disulfide exerts insecticidal neurotoxicity through mitochondrial dysfunction and activation of insect KATP channels. J Neurophysiol 90:259–270PubMedCrossRefGoogle Scholar
- Ercolini D, Russo F, Nasi A, Ferranti P, Villani F (2009) Mesophilic and psychrotrophic bacteria from meat and their spoilage potential in vitro and in beef. Appl Environ Microbiol 75:1990–2001PubMedCrossRefGoogle Scholar
- Ezquer I, Li J, Ovecka M, Baroja-Fernandez E, Munoz FJ, Montero M, Diaz de Cerio J, Hildago M, Sesma MT, Bahaji A, Etxeberria E, Pozueta-Romero J (2010) Microbial volatile emissions promote accumulation of exceptionally high levels of starch in leaves of mono- and dicotyledonous plants. Plant Cell Physiol 51:1674–1693PubMedCrossRefGoogle Scholar
- Farag MA, Ryu CM, Summer 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
- Fiddaman PJ, Rossall S (1994) Effect of substrate on the production of antifungal volatiles from Bacillus Subtilis. J Appl Bacteriol 76:395–405PubMedCrossRefGoogle Scholar
- Gautier H, Auger J, Legros C, Lapied B (2008) Calcium-activated potassium channels in insect pacemaker neurons as unexpected target site for the novel fumigant dimethyl disulfide. J Pharmacol Exp Ther 324:149–159PubMedCrossRefGoogle Scholar
- Gerber NN, Lechevalier HA (1965) Geosmin, an earthy-smelling substance isolated from actinomycetes. Appl Microbiol 13:935–938PubMedGoogle Scholar
- Gust B, Challis GL, Fowler K, Kieser T, Chater KF (2003) PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc Natl Acad Sci USA 100:1541–1546PubMedCrossRefGoogle Scholar
- Kai M, Piechulla B (2009) Plant growth promotions due to rhizobacterial volatiles—an effect of CO2? FEBS Lett 583:3473–3477PubMedCrossRefGoogle 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 187:351–360PubMedCrossRefGoogle Scholar
- Kai M, Vespermann A, Piechulla B (2008) The growth of fungi and Arabidopsis thaliana is influenced by bacterial volatiles. Plant Signal Behav 3:1–3CrossRefGoogle Scholar
- Kai M, Crespo E, Cristescu SM, Harren FJM, Piechulla B (2010) Serratia odorifera: analysis of volatile emission and biological impact of volatile compounds on Arabidopsis thaliana. Appl Microbiol Biotechnol 88:965–976PubMedCrossRefGoogle Scholar
- Kataoka H, Lord HL, Pawliszyn J (2000) Applications of solid-phase microextraction in food analysis. J Chromatogr A 880:35–62PubMedCrossRefGoogle Scholar
- Kim M, Ahn JW, Jin UH, Choi D, Paek KH, Pai HS (2003) Activation of the programmed cell death pathway by inhibition of proteasome function in plants. J Biol Chem 278:19406–19415PubMedCrossRefGoogle Scholar
- Kirsch C, Logemann E, Lippok B, Schmelzer E, Hahlbrock K (2001) A highly specific pathogen-responsive promoter element from the immediate-early activated CMPG1 gene in Petroselinum crispum. Plant J 26:1–12CrossRefGoogle Scholar
- Kurze S, Dahl R, Bahl H, Berg G (2001) Biological control of soil-borne pathogens in strawberry by Serratia plymuthica HRO-C48. Plant Dis 85:529–534CrossRefGoogle Scholar
- Kwon YS, Ryu CM, Lee S, Park HB, Han KS, Lee JH, Lee K, Chung WS, Jeong MJ, Kim HK, Bae DW (2010) Proteome analysis of Arabidopsis seedlings exposed to bacterial volatiles. Planta 232:1355–1370PubMedCrossRefGoogle Scholar
- Larsen TO, Frisvad JC (1994) A simple method for collection of volatile metabolites from fungi based on diffusive sampling from Petri dishes. J Microbiol Methods 19:297–305CrossRefGoogle Scholar
- Losada M, Arnon DJ (1963) Selective inhibitors of photosynthesis. In: Hochster RM and Quasted JH (eds), Metabolic Inhibitors, vol 2. Academic, New York, pp 503–611Google Scholar
- Mayr D, Margesin R, Klingsbichel E, Hartungen E, Jenewein D, Märk TD Schinner F und (2003) Rapid detection of meat spoilage by measuring volatile organic compounds by using proton transfer reaction mass spectrometry. Appl Environ Microbiol 69:4697–4705PubMedCrossRefGoogle Scholar
- Ohme-Takagi M, Shinsi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7:173–182PubMedGoogle Scholar
- Pollak FC, Berger RG (1996) Geosmin and related volatiles in bioreactor-cultured Streptomyces citreus CBS 109.60. Appl Environ Microbiol 62:1295–1299PubMedGoogle Scholar
- Preti G, Thaler E, Hanson CW, Troy M, Eades J, Gelperin A (2009) Volatile compounds characteristic of sinus-related bacteria and infected sinus mucus: analysis by solid-phase microextraction and gas chromatography–mass spectrometry. J Chromatogr B 877:2011CrossRefGoogle Scholar
- Raaijmakers JM, Vlami M, de Sou JT (2002) Antibiotic production by bacterial biocontrol agents. Antonie Van Leeuwenhoek 81:537–547PubMedCrossRefGoogle Scholar
- Rudrappa T, Splaine RE, Biedrzycki ML, Bais HP (2008) Cyanogenic Pseudomonads influence multitrophic interactions in the rhizosphere. PLoS One 30:3(4), e2073Google Scholar
- Rudrappa T, Biedrzycki ML, Kunjeti SG, Donofrio NM, Czymmek KJ, Paré PW, Bais HP (2010) The rhizobacterial elicitor acetoin induces systemic resistance in Arabidopsis thaliana. Commun Integr Biol 3:130–138PubMedCrossRefGoogle Scholar
- Rushton PJ, Reinstädler A, Lipka V, Lippok B, Somssich IE (2002) Synthetic plant promoters containing defined regulatory elements provide novel insights into pathogen- and wound-induced signaling. Plant Cell 14:749–762PubMedCrossRefGoogle Scholar
- Ryu CM, Farag MA, Hu CH, Reddy MS, Wie HX, Pare PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci USA 100:4927–4932PubMedCrossRefGoogle Scholar
- 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
- Schöller CEG, Molin S, Wilkins K (1997) Volatile metabolites from some gram-negative bacteria. Chemosphere 35:1487–1495PubMedCrossRefGoogle Scholar
- Schreier P (1980) Wine aroma composition: identification of additional volatile constituents in red wine. J Agric Food Chem 28:926–928CrossRefGoogle Scholar
- Schulz S, Fuhlendorff J, Reichenbach H (2004) Identification and synthesis of volatiles released by the myxobacterium Chondromyces crocatus. Tetrahedron 60:3863–3872CrossRefGoogle Scholar
- Stotzky G, Schenck S (1976) Volatile organic compounds and microorganisms. CRC Critical Rev Microbiol 4:333–382CrossRefGoogle Scholar
- Thorn RMS, Reynolds DM, Greenman J (2010) Multivariate analysis of bacterial volatile compound profiles for discrimination between selected species and strains in vitro. J Microbiol Methods 84:258–264PubMedCrossRefGoogle Scholar
- Urbach G (1997) The flavour of milk and dairy products: II. Cheese: contribution of volatile compounds. Intern J Dairy Technol 50:79–89CrossRefGoogle Scholar
- Valverde C, Haas D (2008) Small RNAs controlled by two-component systems. Adv Exp Med Biol 631:54–79Google Scholar
- Vergnais L, Masson F, Montel MC, Berdagué JL, Talon R (1998) Evaluation of solid-phase microextraction for analysis of volatile metabolites produced by Staphylococci. J Agric Food Chem 46:228–234PubMedCrossRefGoogle Scholar
- Vespermann A, Kai M, Piechulla B (2007) Rhizobacterial volatiles affect the growth of fungi and Arabidopsis thaliana. Appl Environ Microbiol 73:5639–5641PubMedCrossRefGoogle Scholar
- von Reuß S, Kai M, Piechulla B, Francke W (2010) Octamethylbicyclo(3.2.1)octadienes from Serratia odorifera. Angew Chem Int Ed 49:2009–2010CrossRefGoogle Scholar
- Walch-Liu P, Liu LH, Remans T, Tester M, Forde BG (2006) Evidence that l-glutamate can act as endogenous signal to modulate root growth and branching in Arabidopsis thaliana. Plant Cell Physiol 47:1045–1057PubMedCrossRefGoogle Scholar
- Walker TS, Bais HP, Deziel E, Schweitzer HP, Rahme LG, Fall R, Vivanco JM (2004) Pseudomonas aeruginosa-plant root interactions. Pathogenicity, biofilm formations, and root exudation. Plant Physiol 134:3210–3331CrossRefGoogle Scholar
- Weingart H, Völksch B (1997) Ethylene production by Pseudomonas syringae pathovars in vitro and in planta. Appl Environ Microbiol 63:156–161PubMedGoogle Scholar
- Xie X, Zhang H, Pare PW (2009) Sustained growth promotion in Arabidopsis with long-term exposure to the beneficial soil bacterium Bacillus subtilis (GB03). Plant Signal Behav 4:948–953PubMedCrossRefGoogle 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 226:839–851PubMedCrossRefGoogle Scholar
- Zhang H, Kim MS, Sun Y, Dowd SE, Shi H, Pare PW (2008a) Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter HKT1. Mol Plant–Microbe Interact 21:737–744PubMedCrossRefGoogle Scholar
- Zhang H, Xie X, Kim MS, Kornyeyev DA, Holaday S, Pare RW (2008b) Soil bacterium augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant J 56:264–273PubMedCrossRefGoogle Scholar
- Zhang H, Sun Y, Xie X, Kim MS, Dowd SE, Pare RW (2009) A soil bacterium regulates plant acquisition of iron via deficiency-inducible mechanisms. Plant J 58:568–577PubMedCrossRefGoogle Scholar
- Zhang H, Murzello C, Sun Y, Kim MS, Xie X, Jeter RM, Zak JC, Dowd SE, Pare PW (2010) Choline and osmotic-stress tolerance induced by the soil microbe Bacillus subtilis (GB03). Mol Plant–Microbe Interact 23:1097–1104PubMedCrossRefGoogle Scholar
- Zhu J, Bean HD, Kuo YM, Hill JE (2010) Fast detection of volatile organic compounds from bacterial cultures by secondary electrospray ionization–mass spectrometry. J Clin Microbiol 48:4426–4431PubMedCrossRefGoogle Scholar
- Zoller HF, Mansfield Clark W (1921) The production of volatile fatty acids by bacteria of the dysentery group. J Gen Physiol 3:325–330PubMedCrossRefGoogle Scholar
- Zou CS, Mo MH, Gu YQ, Zhou JP, Zhang KQ (2007) Possible contribution of volatile-producing bacteria in soil fungistasis. Soil Biol Biochem 39:2371–2379CrossRefGoogle Scholar