Abstract
Volatile substances are a very effective way to transmit information over long distances, especially for stationary plants. Just like the atmosphere, belowground habitats are full of volatile, biogenic signaling compounds that may have a drastic direct or indirect effect on intra-/interacting partners. For the first time, this study gives a deep insight into the extremely inhibitory effects of mixtures of volatiles from the rhizobacteria Serratia plymuthica and Stenotrophomonas maltophilia on the model plant Arabidopsis thaliana. The massive impairment of growth and the systematic production of hydrogen peroxide lead to complete death of the plant seedling, most likely due to nonspecific secondary result of the volatile compounds, whereas specific changes in transcription were initiated at an earlier time. In addition, an ecological relationship and the involvement of factors of the classic response to pathogens have been demonstrated on the basis of natural variants and mutants of A. thaliana, respectively. This work reveals fundamental insights into a new type of stress-initiating signals, which should also be taken into consideration when there is direct contact with the pathogens. Here the term mVAMP (microbial volatile-associated molecular pattern) has been suggested to indicate specifically acting volatile substances from microorganisms.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Alström S, Burns RG (1989) Cyanide production by rhizobacteria as a possible mechanism of plant growth inhibition. Biol Fertil Soils 7:232–238
Arthur CL, Pawliszyn J (1990) Solid phase microextraction with thermal desorption using fused silica optical fibers. Anal Chem 62:2145–2148
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266
Baldwin IT, Halitschke R, Paschold A, von Dahl CC, Preston CA (2006) Volatile signaling in plant-plant interactions: “Talking Trees” in the genomics era. Science 311:812–815
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
Barber DA, Martin JK (1976) The release of organic substances by cereal roots into soil. New Phytol 76:69–80
Berardini TZ, Mundodi S, Reiser R, Huala E, Garcia-Hernandez M, Zhang P, Mueller LM, Yoon J, Doyle A, Lander G, Moseyko N, Yoo D, Xu I, Zoeckler B, Montoya M, Miller N, Weems D, Rhee SY (2004) Functional annotation of the Arabidopsis genome using controlled vocabularies. Plant Physiol 135:1–11
Berg G, Marten P, Ballin G (1996) Stenotrophomonas maltophilia in the rhizosphere of oilseed rape – occurrence, characterization and interaction with phytopathogenic fungi. Microbiol Res 151:1–9
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 68:3328–3338
Bernier SP, Létoffé S, Delepierre M, Ghigo JM (2011) Biogenic ammonia modifies antibiotic resistance in physically separated bacteria. Mol Microbiol 81(3):705–716
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 13:1170–1176
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(3):1000–1008
Blumer C, Haas D (2000) Mechanism, regulation, and ecological role of bacterial cyanide biosynthesis. Arch Microbiol 173:170–177
Boland W, Ney P, Jaenicke L, Gassmann G (1984) A “closed-loop-stripping” technique as a versatile tool for metabolic studies of volatiles. In: Scheuer P (ed) Analysis of volatiles. De Gruyter, Berlin, pp 371–380
Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406
Britto DT, Kronzucker HJ (2002) NH4 – toxicity in higher plants: a critical review. J Plant Physiol 159:567–584
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 74:2179–2186
Chatzinotas A, Schäwe R, Saleem M, Fetzer J, Harms H (2011) Microbial model systems and ecological theory: how does increasing environmental stress affect microbial interactions and ecosystems services. VAAM-Tagung in Karlsruhe, 3–6 April 2011
Chen H, Lai Z, Shi J, Xiao Y, Chen Z, Xu X (2010) Roles of Arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress. BMC Plant Biol 10:281. doi:10.1186/1471-2229-10-281
Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814
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 21:1067–1075
Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833
Desikan R, Reynolds A, Hancock JT, Neil SJ (1998) Hairpin and hydrogen peroxide both initiate programmed cell death but have differential effects on gene expression in Arabidopsis suspension cultures. Biochem J 330:115–120
Dickschat JS, Martens R, Brinkhoff T, Simon M, Schulz S (2005) Volatiles released by a Streptomyces species isolated from the North Sea. Chem Biodivers 2:837–865
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 90:259–270
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 75:1990–2001
Etschmann MMW, Bluemke W, Sell D, Schrader J (2002) Biotechnological production of 2-phenylethanol. Appl Microbiol Biotechnol 59:1–8
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 51:1674–1693
Fiddaman PJ, Rossall S (1994) Effect of substrate on the production of antifungal volatiles from Bacillus subtilis. J Appl Bacteriol 76:395–405
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 324:149–159
Gerber NN, Lechevalier HA (1965) Geosmin, an earthy-smelling substance isolated from actinomycetes. Appl Microbiol 13:935–938
Goda H, Sasaki E, Akiyama K, Maruyama-Nakashita A, Nakabayashi K, Li W, Ogawa M, Yamauchi Y, Preston J, Aoki K, Kiba T, Takatsuto S, Fujioka S, Asami T, Nakano T, Kato H, Mizuno T, Sakakibara H, Yamaguchi S, Nambara E, Kamiya Y, Takahashi H, Hirai MY, Sakurai T, Shinozaki K, Saito K, Yoshida S, Shimada Y (2008) The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access. Plant J 55:526–542
Hématy K, Cherk C, Somerville S (2009) Host–pathogen warfare at the plant cell wall. Curr Opin Plant Biol 12:406–413
Hennig L, Menges M, Murray JA, Gruissem W (2003) Arabidopsis transcript profiling on Affymetrix GeneChip arrays. Plant Mol Biol 53:457–465
Kai M, Piechulla B (2009) Plant growth promotions due to rhizobacterial volatiles – an effect of CO2? FEBS Lett 583:3473–3477
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
Kai M, Haustein M, Molina F, Petri A, Scholz B, Piechulla B (2009a) Bacterial volatiles and their action potential. Appl Microbiol Biotechnol 81:1001–1012
Kai M, Wenke K, Piechulla B (2009b) Flüchtige metabolite als infochemikalien: duftstoffe im erdreich. BIUZ 39:3–9
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 88:965–976
Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, Batistic O, D’Angelo C, Bornberg-Bauer E, Kudla J, Harter K (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J 50:347–363
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 278:19406–19415
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 26:1–12
Kurze S, Dahl R, Bahl H, Berg G (2001) Biological control of soil-borne pathogens in strawberry by Serratia plymuthica HRO-C48. Plant Dis 85:529–534
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 232:1355–1370
Lamp C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251–275
Losada M, Arnon DJ (1963) Selective inhibitors of photosynthesis. In: Hochster RM, Quastel JH (eds) Metabolic inhibitors, vol 2. Academic, New York, pp 503–611
Lotze MT, Zeh HJ, Rubartelli A, Sparvero LJ, Amoscato AA, Washburn NR, Devera ME, Liang X, Tör M, Billiar T (2007) The grateful dead: damage associated molecular pattern molecules and reduction/oxidation regulate immunity. Immunol Rev 220:60–81
Mangelsen E, Kilian J, Berendzen KW, Kolukisaoglu UH, Harter K, Jansson C, Wanke D (2008) Phylogenetic and comparative gene expression analysis of barley (Hordeum vulgare) WRKY transcription factor family reveals putatively retained functions between monocots and dicots. BMC Genomics 9:194
Mayr D, Margesin R, Klingsbichel E, Hartungen E, Jenewein D, Märk TD, Schinner F (2003) Rapid detection of meat spoilage by measuring volatile organic compounds by using proton transfer reaction mass spectrometry. Appl Environ Microbiol 69:4697–4705
Meyers BC, Morgante M, Michelmore RW (2002) TIR-X and TIR-NBS proteins: two new families related to disease resistance TIR-NBS-LRR proteins encoded in Arabidopsis and other plant genomes. Plant J 32:77–92
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498
Müller C, Hilker M (2000) The effect of a green leaf volatile on host plant finding by larvae of a herbivorous insect. Naturwissenschaften 87:216–219
Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot 53:1237–1242
O’Connor TR, Dyreson C, Wyrick JJ (2005) Athena: a resource for rapid visualization and systematic analysis of Arabidopsis promoter sequences. Bioinformatics 21:4411–4413
Pacioni G (1991) Effects of Tuber metabolites on the rhizospheric environment. Mycol Res 95:1355–1358
Pandey SP, Roccaro M, Schön M, Logemann E, Somssich IE (2010) Transcriptional reprogramming regulated by WRKY18 and WRKY40 facilitates powdery mildew infection of Arabidopsis. Plant J 64:912–923
Piechulla B, Pott MB (2003) Plant scents-mediators of inter- and intra-organismic communication. Planta 217:687–689
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
Robert HS, Quint A, Brand D, Vivian-Smith A, Offringa R (2009) BTB AND TAZ DOMAIN scaffold proteins perform a crucial function in Arabidopsis development. Plant J 58:109–121
Rossel JB, Wilson PB, Hussain D, Woo NS, Gordon MJ, Mewett OP, Howell KA, Whelan J, Kazan K, Pogson BJ (2007) Systemic and intracellular response to photooxidative stress in Arabidopsis. Plant Cell 19:4091–4110
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 3:130–138
Rushton PJ, Reinstadler 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 14:749–762
Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:247–258
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 100:4927–4932
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
Sakamoto H, Araki T, Meshi T, Iwabuchi M (2000) Expression of a subset of the Arabidopsis Cys(2)/His(2)-type zinc-finger protein gene family under water stress. Gene 248:23–32
Schreier P (1980) Wine aroma composition: identification of additional volatile constituents in red wine. J Agric Food Chem 28:926–928
Schulz S, Fuhlendorff J, Reichenbach H (2004) Identification and synthesis of volatiles released by the myxobacterium Chondromyces crocatus. Tetrahedron 60:3863–3872
Shang Y, Yan L, Liu ZQ, Cao Z, Mei C, Xin Q, Wu FQ, Wang XF, Du SY, Jiang T, Zhang XF, Zhao R, Sun HL, Liu R, Yu YT, Zhang DP (2010) The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition. Plant Cell 22:1909–1935
Shen QH, Saijo Y, Mauch S, Biskup C, Bieri S, Keller B, Seki H, Ulker B, Somssich IE, Schulze-Lefert P (2007) Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 315:1098–1103
Stall RE, Hall CB, Cook AA (1972) Relationship of ammonia to necrosis of pepper leaf tissue during colonization by Xanthomonas vesicatoria. Phytopathology 62:882–886
Stotzky G, Schenck S (1976) Volatile organic compounds and microorganisms. CRC Crit Rev Microbiol 4:333–382
Strittmatter G, Gheysen G, Gianinazzi-Pearson V, Hahn K, Niebel A, Rohde W, Tacke E (1996) Infections with various types of organisms stimulate transcription from a short promoter fragment of the potato gst1 gene. Mol Plant Microbe Interact 9:68–73
Swarbreck D, Wilks C, Lamesch P, Berardini TZ, Garcia-Hernandez M, Foerster H, Li D, Meyer T, Muller R, Ploetz L, Radenbaugh A, Singh S, Swing V, Tissier C, Zhang P, Huala E (2008) The Arabidopsis Information Resource (TAIR): gene structure and function annotation. Nucleic Acids Res 36:D1009–D1014
Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914–939
Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants, H2O2 accumulation in papillae and hypersensitive response during barley-powdery mildew interaction. Plant J 11:1187–1194
Urbach G (1997) The flavour of milk and dairy products: II. Cheese: contribution of volatile compounds. Int J Dairy Technol 50:79–89
van Dam NM, Qiu BL, Hordijk CA, Vet LEM, Jansen JJ (2010) Identification of biologically relevant compounds in aboveground and belowground induced volatile blends. J Chem Ecol 36(9):1006–1016
Vespermann A, Kai M, Piechulla B (2007) Rhizobacterial volatiles affect the growth of fungi and Arabidopsis thaliana. Appl Environ Microbiol 73:5639–5641
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(8):1045–1057
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 134:3210–3331
Wang Z, Cao G, Wang X, Miao J, Liu X, Chen Z, Qu LJ, Gu H (2008) Identification and characterization of COI1-dependent transcription factor genes involved in JA-mediated response to wounding in Arabidopsis plants. Plant Cell Rep 27:125–135
Wanke D, Berendzen K, Kilian J, Harter K (2009) Insights into the Arabidopsis abiotic stress response from the AtGenExpress expression profile dataset. In: Hirt H (ed) Plant stress biology. Wiley-VCH, Weinheim, pp 199–225
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
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 (2012a) Transcriptional response of Arabidopsis seedlings to rhizobacterial, growth inhibiting volatiles. Plant J 70(3):445–459
Wenke K, Weise T, Warnke R, Valverde C, Wanke D, Kai M, Piechulla B (2012b) Bacterial volatiles mediating information between bacteria and plants. In: Witzany G, Baluska F (eds) Bio-communication of plants. Springer, Heidelberg
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 4:948–953
Xu X, Chen C, Fan B, Chen Z (2006) Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors. Plant Cell 18:1310–1326
Zangerl AR, Berenbaum MR (2009) Effects of florivory on floral volatile emissions and pollination success in the wild parsnip. Arthropod Plant Interact 3:181–191
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
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 21:737–744
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 56:264–273
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 58:568–577
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 23:1097–1104
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Wenke, K., Piechulla, B. (2013). The Effects of Volatile Metabolites from Rhizobacteria on Arabidopsis thaliana . In: Maheshwari, D., Saraf, M., Aeron, A. (eds) Bacteria in Agrobiology: Crop Productivity. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-37241-4_16
Download citation
DOI: https://doi.org/10.1007/978-3-642-37241-4_16
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-37240-7
Online ISBN: 978-3-642-37241-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)