VOCs-mediated hormonal signaling and crosstalk with plant growth promoting microbes

References

• Asari S, Matzen S, Petersen MA, et al. Multiple effects of Bacillus amyloliquefaciens volatile compounds: plant growth promotion and growth inhibition of phytopathogens. FEMS Microbiol Ecol. 2016;92:fiw070.
   PubMed Web of Science ®Google Scholar
• Ho YN, Mathew DC, Huang CC. Plant-microbe ecology: interactions of plants and symbiotic microbial communities. In: Yousaf Z. editor. Plant ecology – traditional approaches to recent trends. Rijeka: InTech;2017. p. 93–119.
   Google Scholar
• Lugtenberg B, Rozen DE, Kamilova F. Wars between microbes on roots and fruits. F1000 Res. 2017;6:343.
   PubMedGoogle Scholar
• Bulgarelli D, Rott M, Schlaeppi K, et al. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 2012;488:91–95.
   PubMed Web of Science ®Google Scholar
• Kandel SL, Firrincieli A, Joubert PM, et al. An in vitro study of biocontrol and plant growth promotion potential of Salicaceae endophytes. Front Microbiol. 2017;8:386.
   PubMed Web of Science ®Google Scholar
• Lundberg DS, Lebeis SL, Paredes SH, et al. Defining the core Arabidopsis thaliana root microbiome. Nature 2012;488:86–90.
   PubMed Web of Science ®Google Scholar
• Vejan P, Abdullah R, Khadiran T, et al. Role of plant growth promoting rhizobacteria in agricultural sustainability-a review. Molecules 2016;21:E573.
   PubMed Web of Science ®Google Scholar
• Amavizca E, Bashan Y, Ryu CM, et al. Enhanced performance of the microalga Chlorella sorokiniana remotely induced by the plant growth-promoting bacteria Azospirillum brasilense and Bacillus pumilus. Sci Rep. 2017;7:41310.
   PubMed Web of Science ®Google Scholar
• Gao QM, Zhu SF, Kachroo P, et al. Signal regulators of systemic acquired resistance. Front Plant Sci. 2015;6:228.
   PubMed Web of Science ®Google Scholar
• Meldau DG, Meldau S, Hoang LH, et al. Dimethyl disulfide produced by the naturally associated bacterium Bacillus sp. B55 promotes Nicotiana attenuate growth by enhancing sulfur nutrition. Plant Cell 2013;25:2731–2747.
   PubMed Web of Science ®Google Scholar
• Soleimani M, Shamsbakhsh M, Taghavi M, et al. Biological control of stem and root-rot of wheat caused by Biopolaris spp. by using antagonistic bacteria, fluorescent Pseudomonas and Bacillus spp. Jo F Biol Sci. 2005;5:347–353.
   Google Scholar
• Zhang HM, Sun Y, Xie XT, et al. A soil bacterium regulates plant acquisition of iron via deficiency-inducible mechanisms. Plant J. 2009;58:568–577.
   PubMed Web of Science ®Google Scholar
• Denance N, Sanchez-Vallet A, DGoffner D, et al. Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs. Front Plant Sci. 2013;4:155.
   PubMed Web of Science ®Google Scholar
• Dodds PN, Rathjen JP. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet. 2010;11:539–548.
   PubMed Web of Science ®Google Scholar
• Bailly A, Weisskopf L. Mining the volatilomes of plant-associated microbiota for new biocontrol solutions. Front Microbiol. 2017;8:1638.
   PubMed Web of Science ®Google Scholar
• Casarrubia S, Sapienza S, Fritz H, et al. Ecologically different fungi affect Arabidopsis development: contribution of soluble and volatile compounds. PLoS One 2016;11:e0168236.
   PubMed Web of Science ®Google Scholar
• Cordovez V, Mommer L, Moisan K, et al. Plant phenotypic and transcriptional changes induced by volatiles from the fungal root pathogen Rhizoctonia solani. Front Plant Sci. 2017;8:1262.
   PubMed Web of Science ®Google Scholar
• Dutta S, Mehrotra RC, Paul S, et al. Remarkable preservation of terpenoids and record of volatile signalling in plant-animal interactions from Miocene amber. Sci Rep. 2017;7:10940.
   PubMed Web of Science ®Google Scholar
• Hacquard S. Commentary: microbial small talk: volatiles in fungal-bacterial interactions. Front Microbiol. 2017;8:1.
   PubMed Web of Science ®Google Scholar
• Kwon YS, Ryu CM, Lee S, et al. Proteome analysis of Arabidopsis seedlings exposed to bacterial volatiles. Planta 2010;232:1355–1370.
   PubMed Web of Science ®Google Scholar
• Ossowicki A, Jafra S, Garbeva P. The antimicrobial volatile power of the rhizospheric isolate Pseudomonas donghuensis P482. PLoS One 2017;12:e0174362.
   PubMed Web of Science ®Google Scholar
• Radhakrishnan R, Hashem A, Abd Allah EF. Bacillus: a biological tool for crop improvement through bio-molecular changes in adverse environments. Front Physiol. 2017;8:667.
   PubMed Web of Science ®Google Scholar
• Rybakova D, Rack-Wetzlinger U, Cernava T, et al. Aerial warfare: a volatile dialogue between the plant pathogen Verticillium longisporum and its antagonist Paenibacillus polymyxa. Front Plant Sci. 2017;8:1294.
   PubMed Web of Science ®Google Scholar
• Ryu CM, Farag MA, Hu CH, et al. Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci U S A 2003;100:4927–4932.
   PubMed Web of Science ®Google Scholar
• Schmidt R, de Jager V, Zuhlke D, et al. Fungal volatile compounds induce production of the secondary metabolite Sodorifen in Serratia plymuthica PRI-2C. Sci Rep. 2017;7:862.
   PubMed Web of Science ®Google Scholar
• Schmidt R, Etalo DW, de Jager V, et al. Microbial small talk: volatiles in fungal-bacterial interactions. Front Microbiol. 2016;6:1495.
   PubMed Web of Science ®Google Scholar
• Tahir HAS, Gu Q, Wu H, et al. Bacillus volatiles adversely affect the physiology and ultra-structure of Ralstonia solanacearum and induce systemic resistance in tobacco against bacterial wilt. Sci Rep. 2017;7:40481.
   PubMed Web of Science ®Google Scholar
• Tahir HAS, Gu Q, Wu HJ, et al. Plant growth promotion by volatile organic compounds produced by Bacillus subtilis SYST2. Front Microbiol. 2017;8:171.
   PubMed Web of Science ®Google Scholar
• Tahir HAS, Gu Q, Wu H, et al. Effect of volatile compounds produced by Ralstonia solanacearum on plant growth promoting and systemic resistance inducing potential of Bacillus volatiles. BMC Plant Biol. 2017;17:133.
   PubMed Web of Science ®Google Scholar
• Zamioudis C, Mastranesti P, Dhonukshe P, et al. Unraveling root developmental programs initiated by beneficial Pseudomonas spp. bacteria. Plant Physiol. 2013;162:304–318.
   PubMed Web of Science ®Google Scholar
• Lemfack MC, Gohlke BO, Toguem SMT, et al. mVOC 2.0: a database of microbial volatiles. Nucleic Acids Res. 2018;46:D1261–D1265.
   PubMed Web of Science ®Google Scholar
• Lemfack MC, Nickel J, Dunkel M, et al. mVOC: a database of microbial volatiles. Nucl Acids Res. 2014;42:D744–D748.
   PubMed Web of Science ®Google Scholar
• Maffei ME. Sites of synthesis, biochemistry and functional role of plant volatiles. S. Afr J Bot. 2010;76:612–631.
   Web of Science ®Google Scholar
• Maffei ME, Gertsch J, Appendino G. Plant volatiles: production, function and pharmacology. Nat Prod Rep. 2011;28:1359–1380.
   PubMed Web of Science ®Google Scholar
• Bailly A, Groenhagen U, Schulz S, et al. The inter-kingdom volatile signal indole promotes root development by interfering with auxin signalling. Plant J. 2014;80:758–771.
   PubMed Web of Science ®Google Scholar
• Bitas V, Kim HS, Bennett JW, et al. Sniffing on microbes: diverse roles of microbial volatile organic compounds in plant health. MPMI 2013;26:835–843.
   PubMed Web of Science ®Google Scholar
• Kanchiswamy CN, Malnoy M, Maffei ME. Bioprospecting bacterial and fungal volatiles for sustainable agriculture. Trends Plant Sci. 2015;20:206–211.
   PubMed Web of Science ®Google Scholar
• Han SH, Lee SJ, Moon JH, et al. GacS-dependent production of 2R, 3R-butanediol by Pseudomonas chlororaphis O6 is a major determinant for eliciting systemic resistance against Erwinia carotovora but not against Pseudomonas syringae pv. tabaci in tobacco. Mol Plant Microbe Interact. 2006;19:924–930.
   PubMed Web of Science ®Google Scholar
• Schulz-Bohm K, Geisen S, Wubs ERJ, et al. The prey's scent – volatile organic compound mediated interactions between soil bacteria and their protist predators. Isme J. 2017;11:817–820.
   PubMed Web of Science ®Google Scholar
• Kai M, Haustein M, Molina F, et al. Bacterial volatiles and their action potential. Appl Microbiol Biotechnol. 2009;81:1001–1012.
   PubMed Web of Science ®Google Scholar
• Lee S, Yap M, Behringer G, et al. Volatile organic compounds emitted by Trichoderma species mediate plant growth. Fungal Biol Biotechnol. 2016;3:7.
   PubMedGoogle Scholar
• Minerdi D, Bossi S, Maffei ME, et al. Fusarium oxysporum and its bacterial consortium promote lettuce growth and expansin A5 gene expression through microbial volatile organic compound (MVOC) emission. FEMS Microbiol Ecol. 2011;76:342–351.
   PubMed Web of Science ®Google Scholar
• Park YS, Dutta S, Ann M, et al. Promotion of plant growth by Pseudomonas fluorescens strain SS101 via novel volatile organic compounds. Biochem Biophys Res Commun. 2015;461:361–365.
   PubMed Web of Science ®Google Scholar
• Piechulla B, Degenhardt J. The emerging importance of microbial volatile organic compounds. Plant Cell Environ. 2014;37:811–812.
   PubMed Web of Science ®Google Scholar
• Raya-Gonzalez J, Velazquez-Becerra C, Barrera-Ortiz S, et al. N,N-dimethyl hexadecylamine and related amines regulate root morphogenesis via jasmonic acid signaling in Arabidopsis thaliana. Protoplasma 2017;254:1399–1410.
   PubMed Web of Science ®Google Scholar
• Shikano I, Rosa C, Tan CW, et al. Tritrophic interactions: microbe-mediated plant effects on insect herbivores. Annu Rev Phytopathol. 2017;55:313–331.
   PubMed Web of Science ®Google Scholar
• Bunge M, Araghipour N, Mikoviny T, et al. On-line monitoring of microbial volatile metabolites by proton transfer reaction-mass spectrometry. Appl Environ Microbiol. 2008;74:2179–2186.
   PubMed Web of Science ®Google Scholar
• Del Giudice L, Massardo DR, Pontieri P, et al. The microbial community of vetiver root and its involvement into essential oil biogenesis. Environ Microbiol. 2008;10:2824–2841.
   PubMed Web of Science ®Google Scholar
• Hung R, Lee S, Bennett JW. Arabidopsis thaliana as a model system for testing the effect of Trichoderma volatile organic compounds. Fungal Ecol. 2013;6:19–26.
   Web of Science ®Google Scholar
• Junker RR, Loewel C, Gross R, et al. Composition of epiphytic bacterial communities differs on petals and leaves. Plant Biol. 2011;13:918–924.
   PubMed Web of Science ®Google Scholar
• Kai M, Crespo E, Cristescu SM, et al. Serratia odorifera: analysis of volatile emission and biological impact of volatile compounds on Arabidopsis thaliana. Appl Microbiol Biotechnol. 2010;88:965–976.
   PubMed Web of Science ®Google Scholar
• Karamanoli K, Menkissoglu-Spiroudi U, Bosabalidis AM, et al. Bacterial colonization of the phyllosphere of nineteen plant species and antimicrobial activity of their leaf secondary metabolites against leaf associated bacteria. Chemoecology 2005;15:59–67.
   Web of Science ®Google Scholar
• Kai M, Piechulla B. Plant growth promotion due to rhizobacterial volatiles-an effect of CO2? FEBS Lett. 2009;583:3473–3477.
   PubMed Web of Science ®Google Scholar
• Farag MA, Ryu CM, Sumner LW, et al. GC-MS SPME profiling of rhizobacterial volatiles reveals prospective inducers of growth promotion and induced systemic resistance in plants. Phytochemistry 2006;67:2262–2268.
   PubMed Web of Science ®Google Scholar
• Ryu CM, Farag MA, Hu CH, et al. Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol. 2004;134:1017–1026.
   PubMed Web of Science ®Google Scholar
• Spinelli F, Cellini A, Vanneste JL, et al. Emission of volatile compounds by Erwinia amylovora: biological activity in vitro and possible exploitation for bacterial identification. Trees 2012;26:141–152.
   Web of Science ®Google Scholar
• Zhang H, Kim MS, Sun Y, et al. Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter HKT1. MPMI 2008;21:737–744.
   PubMed Web of Science ®Google Scholar
• Cellini A, Biondi E, Blasioli S, et al. Early detection of bacterial diseases in apple plants by analysis of volatile organic compounds profiles and use of electronic nose. Ann Appl Biol. 2016;168:409–420.
   Web of Science ®Google Scholar
• Fincheira P, Venthur H, Mutis A, et al. Growth promotion of Lactuca sativa in response to volatile organic compounds emitted from diverse bacterial species. Microbiol Res. 2016;193:39–47.
   PubMedGoogle Scholar
• Paul D, Park KS. Identification of volatiles produced by Cladosporium cladosporioides CL-1, a fungal biocontrol agent that promotes plant growth. Sensors 2013;13:13969–13977.
   PubMed Web of Science ®Google Scholar
• Naznin HA, Kiyohara D, Kimura M, et al. Systemic resistance induced by volatile organic compounds emitted by plant growth-promoting fungi in Arabidopsis thaliana. PLoS One 2014;9:e86882.
   PubMed Web of Science ®Google Scholar
• Splivallo R, Novero M, Bertea CM, et al. Truffle volatiles inhibit growth and induce an oxidative burst in Arabidopsis thaliana. New Phytol. 2007;175:417–424.
   PubMed Web of Science ®Google Scholar
• Ledger T, Rojas S, Timmermann T, et al. Volatile-mediated effects predominate in Paraburkholderia phytofirmansgrowth promotion and salt stress tolerance of Arabidopsis thaliana. Front Microbiol. 2016;7:1838.
   PubMed Web of Science ®Google Scholar
• Kishimoto K, Matsui K, Ozawa R. Volatile 1-octen-3-ol induces a defensive response in Arabidopsis thaliana. J Gen Plant Pathol. 2007;73:35.
   Google Scholar
• Chitarra GS, Abee T, Rombouts FM, et al. Germination of Penicillium paneum conidia is regulated by 1-octen-3-ol, a volatile self-inhibitor. Appl Environ Microbiol. 2004;70:2823–2829.
   PubMed Web of Science ®Google Scholar
• Gutierrez-Luna FM, Lopez-Bucio J, Altamirano-Hernandez J, et al. Plant growth-promoting rhizobacteria modulate root-system architecture in Arabidopsis thaliana through volatile organic compound emission. Symbiosis 2010;51:75–83.
   Web of Science ®Google Scholar
• Zhou JY, Li X, Zheng JY, et al. Volatiles released by endophytic Pseudomonas fluorescens promoting the growth and volatile oil accumulation in Atractylodes lancea. Plant Physiol Bioch. 2016;101:132–140.
   PubMed Web of Science ®Google Scholar
• De Vrieze M, Pandey P, Bucheli TD, et al. Volatile organic compounds from native potato-associated Pseudomonas as potential anti-oomycete agents. Front Microbiol. 2015;6:1295.
   PubMed Web of Science ®Google Scholar
• Blom D, Fabbri C, Connor EC, et al. Production of plant growth modulating volatiles is widespread among rhizosphere bacteria and strongly depends on culture conditions. Environ Microbiol. 2011;13:3047–3058.
   PubMed Web of Science ®Google Scholar
• Rudrappa T, Biedrzycki ML, Kunjeti SG, et al. The rhizobacterial elicitor acetoin induces systemic resistance in Arabidopsis thaliana. Commun Integr Biol. 2010;3:130–138.
   PubMedGoogle Scholar
• Song GC, Ryu CM. Two volatile organic compounds trigger plant self-defense against a bacterial pathogen and a sucking insect in cucumber under open field conditions. IJMS 2013;14:9803–9819.
   Google Scholar
• Contreras-Cornejo HA, Macias-Rodriguez L, Cortes-Penagos C, et al. Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiol. 2009;149:1579–1592.
   PubMed Web of Science ®Google Scholar
• Zhang H, Kim MS, Krishnamachari V, et al. Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 2007;226:839–851.
   PubMed Web of Science ®Google Scholar
• Minerdi D, Bossi S, Gullino ML, et al. Volatile organic compounds: a potential direct long-distance mechanism for antagonistic action of Fusarium oxysporum strain MSA 35. Environ Microbiol. 2009;11:844–854.
   PubMed Web of Science ®Google Scholar
• Ulloa-Benitez A, Medina-Romero YM, Sanchez-Fernandez RE, et al. Phytotoxic and antimicrobial activity of volatile and semi-volatile organic compounds from the endophyte Hypoxylon anthochroum strain Blaci isolated from Bursera lancifolia (Burseraceae). J Appl Microbiol. 2016;121:380–400.
   PubMed Web of Science ®Google Scholar
• Bailly A. The modulating effect of bacterial volatiles on plant growth: current knowledge and future challenges. Plant Signal Behav. 2012;7:79–85.
   PubMedGoogle Scholar
• Bhattacharyya D, Garladinne M, Lee YH. Volatile indole produced by Rhizobacterium Proteus vulgaris JBLS202 stimulates growth of Arabidopsis thaliana through auxin, cytokinin, and brassinosteroid pathways. J Plant Growth Regul. 2015;34:158–168.
   Web of Science ®Google Scholar
• Kai M, Piechulla B. Impact of volatiles of the rhizobacteria Serratia odorifera on the moss Physcomitrellapatens. Plant Signal Behav. 2010;5:444–446.
   PubMedGoogle Scholar
• Lo Cantore P, Giorgio A, Iacobellis NS. Bioactivity of volatile organic compounds produced by Pseudomonas tolaasii. Front Microbiol. 2015;6:1082.
   PubMed Web of Science ®Google Scholar
• Groenhagen U, Baumgartner R, Bailly A, et al. Production of bioactive volatiles by different Burkholderia ambifaria strains. J Chem Ecol. 2013;39:1343–1345.
   Web of Science ®Google Scholar
• Astrom B. Role of bacterial cyanide production in differential reaction of plant cultivars to deleterious rhizosphere Pseudomonads. Plant Soil 1991;133:93–100.
   Web of Science ®Google Scholar
• Blom D, Fabbri C, Eberl L, et al. Volatile-mediated killing of Arabidopsis thaliana by bacteria is mainly due to hydrogen cyanide. Appl Environ Microbiol. 2011;77:1000–1008.
   PubMed Web of Science ®Google Scholar
• Flores-Vargas RD, O'Hara GW. Isolation and characterization of rhizosphere bacteria with potential for biological control of weeds in vineyards. J Appl Microbiol. 2006;100:946–954.
   PubMed Web of Science ®Google Scholar
• Kremer RJ, Souissi T. Cyanide production by rhizobacteria and potential for suppression of weed seedling growth. Curr Microbiol. 2001;43:182–186.
   PubMed Web of Science ®Google Scholar
• Zeller SL, Brandl H, Schmid B. Host-plant selectivity of rhizobacteria in a crop/weed model system. PLoS One 2007;2:e846.
   PubMed Web of Science ®Google Scholar
• Weise T, Kai M, Piechulla B. Bacterial ammonia causes significant plant growth inhibition. PLoS One 2013;8:e63538.
   PubMed Web of Science ®Google Scholar
• Gusarov I, Nudler E. NO-mediated cytoprotection: instant adaptation to oxidative stress in bacteria. Proc Natl Acad Sci U S A 2005;102:13855–13860.
   PubMed Web of Science ®Google Scholar
• Sasaki Y, Oguchi H, Kobayashi T, et al. Nitrogen oxide cycle regulates nitric oxide levels and bacterial cell signaling. Sci Rep. 2016;6:22038
   PubMed Web of Science ®Google Scholar
• Shatalin K, Gusarov I, Avetissova E, et al. Bacillus anthracis-derived nitric oxide is essential for pathogen virulence and survival in macrophages. Proc Natl Acad Sci U S A 2008;105:1009–1013.
   PubMed Web of Science ®Google Scholar
• Mirabella R, Rauwerda H, Allmann S, et al. WRKY40 and WRKY6 act downstream of the green leaf volatile E-2-hexenal in Arabidopsis. Plant J. 2015;83:1082–1096.
   PubMed Web of Science ®Google Scholar
• Choi HK, Song GC, Yi HS, et al. Field evaluation of the bacterial volatile derivative 3-pentanol in priming for induced resistance in pepper. J Chem Ecol. 2014;40:882–892.
   PubMed Web of Science ®Google Scholar
• Felten J, Kohler A, Morin E, et al. The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in poplar and Arabidopsis through auxin transport and signaling. Plant Physiol. 2009;151:1991–2005.
   PubMed Web of Science ®Google Scholar
• El-Hasan A, Buchenauer H. Actions of 6-Pentyl-alpha-pyrone in controlling seedling blight incited by Fusarium moniliforme and inducing defence responses in maize. J Phytopathol. 2009;157:697–707.
   Web of Science ®Google Scholar
• Garnica-Vergara A, Barrera-Ortiz S, Munoz-Parra E, et al. The volatile 6-pentyl-2H-pyran-2-one from Trichoderma atroviride regulates Arabidopsis thaliana root morphogenesis via auxin signaling and ETHYLENE INSENSITIVE 2 functioning. New Phytol. 2016;209:1496–1512.
   PubMed Web of Science ®Google Scholar
• Kottb M, Gigolashvili T, Grosskinsky DK, et al. Trichoderma volatiles effecting Arabidopsis: from inhibition to protection against phytopathogenic fungi. Front Microbiol. 2015;6:995.
   PubMed Web of Science ®Google Scholar
• Wenke K, Wanke D, Kilian J, et al. Volatiles of two growth-inhibiting rhizobacteria commonly engage AtWRKY18 function. Plant J. 2012;70:445–459.
   PubMed Web of Science ®Google Scholar
• De Munk WJ. Bud necrosis, a storage disease in tulips. 111. The influence of ethylene and mites. Neth J Plant Pathol. 1972;78:168–178.
   Google Scholar
• Graham JH, Linderman RG. Ethylene production by ectomycorrhizal fungi, Fusarium oxysporum f. sp. pini, and by aseptically synthesized ectomycorrhizae and Fusarium-infected Douglas-fir roots. Can J Microbiol. 1980;26:1340–1347.
   PubMed Web of Science ®Google Scholar
• Spinelli F, Noferini M, Vanneste JL, et al. Potentials of the electronic nose for the diagnosis of bacterial and fungal diseases in fruit trees. EPPO Bull. 2010;40:59–67.
   Google Scholar
• Splivallo R, Fischer U, Gobel C, et al. Truffles regulate plant root morphogenesis via the production of auxin and ethylene. Plant Physiol. 2009;150:2018–2029.
   PubMed Web of Science ®Google Scholar
• Hunziker L, Bonisch D, Groenhagen U, et al. Pseudomonas strains naturally associated with potato plants produce volatiles with high potential for inhibition of phytophthora infestans. Appl Environ Microbiol. 2015;81:821–830.
   PubMed Web of Science ®Google Scholar
• Velazquez-Becerra C, Macias-Rodriguez LI, Lopez-Bucio J, et al. A volatile organic compound analysis from Arthrobacter agilis identifies dimethylhexadecylamine, an amino-containing lipid modulating bacterial growth and Medicago sativa morphogenesis in vitro. Plant Soil 2011;339:329–340.
   Web of Science ®Google Scholar
• Vaishnav A, Kumari S, Jain S, et al. PGPR-mediated expression of salt tolerance gene in soybean through volatiles under sodium nitroprusside. J Basic Microbiol. 2016;56:1274–1288.
   PubMed Web of Science ®Google Scholar
• Vespermann A, Kai M, Piechulla B. Rhizobacterial volatiles affect the growth of fungi and Arabidopsis thaliana. Appl Environ Microbiol. 2007;73:5639–5641.
   PubMed Web of Science ®Google Scholar
• Vaishnav A, Kumari S, Jain S, et al. Putative bacterial volatile-mediated growth in soybean (Glycine max L. Merrill) and expression of induced proteins under salt stress. J Appl Microbiol. 2015;119:539–551.
   PubMed Web of Science ®Google Scholar
• Macias-Rubalcava ML, Hernandez-Bautista BE, Oropeza F, et al. Allelochemical effects of volatile compounds and organic extracts from Muscodor yucatanensis, a tropical endophytic fungus from Bursera simaruba. J Chem Ecol. 2010;36:1122–1131.
   PubMed Web of Science ®Google Scholar
• Santoro MV, Zygadlo J, Giordano W, et al. Volatile organic compounds from rhizobacteria increase biosynthesis of essential oils and growth parameters in peppermint (Mentha piperita). Plant Physiol Bioch. 2011;49:1177–1182.
   PubMed Web of Science ®Google Scholar
• Audrain B, Farag MA, Ryu CM, et al. Role of bacterial volatile compounds in bacterial biology. FEMS Microbiol Rev. 2015;39:222–233.
   PubMed Web of Science ®Google Scholar
• D'Alessandro M, Erb M, Ton J, et al. Volatiles produced by soil-borne endophytic bacteria increase plant pathogen resistance and affect tritrophic interactions. Plant Cell Environ. 2014;37:813–826.
   PubMed Web of Science ®Google Scholar
• Ditengou FA, Muller A, Rosenkranz M, et al. Volatile signalling by sesquiterpenes from ectomycorrhizal fungi reprogrammes root architecture. Nat Commun. 2015;6:6279.
   PubMed Web of Science ®Google Scholar
• Piechulla B, Lemfack MC, Kai M. Effects of discrete bioactive microbial volatiles on plants and fungi. Plant Cell Environ. 2017;40:2042–2067.
   PubMed Web of Science ®Google Scholar
• Chung JH, Song GC, Ryu CM. Sweet scents from good bacteria: case studies on bacterial volatile compounds for plant growth and immunity. Plant Mol Biol. 2016;90:677–687.
   PubMed Web of Science ®Google Scholar
• Farag MA, Song GC, Park YS, et al. Biological and chemical strategies for exploring inter- and intra-kingdom communication mediated via bacterial volatile signals. Nat Protoc. 2017;12:1359–1377.
   PubMed Web of Science ®Google Scholar
• Imam J, Variar M., Shukla P. Role of enzymes and proteins in plant-microbe interaction: A study of M. oryzae versus rice. In: Shukla P, Pletschke BI. editors. Advances in enzyme biotechnology. New Delhi: Springer India; 2013. p. 137–145.
   Google Scholar
• Kai M, Effmert U, Piechulla B. Bacterial-plant-interactions: approaches to unravel the biological function of bacterial volatiles in the rhizosphere. Front Microbiol. 2016;7:108.
   PubMedGoogle Scholar
• Werner S, Polle A, Brinkmann N. Belowground communication: impacts of volatile organic compounds (VOCs) from soil fungi on other soil-inhabiting organisms. Appl Microbiol Biotechnol. 2016;100:8651–8665.
   PubMed Web of Science ®Google Scholar
• Delory BM, Delaplace P, Fauconnier ML, et al. Root-emitted volatile organic compounds: can they mediate belowground plant-plant interactions? Plant Soil. 2016;402:1–26.
   Web of Science ®Google Scholar
• Rasmann S, Bennett A, Biere A, et al. Root symbionts: powerful drivers of plant above- and belowground indirect defenses. Insect Sci. 2017;24:947–960.
   PubMed Web of Science ®Google Scholar
• Huang XF, Chaparro JM, Reardon KF, et al. Rhizosphere interactions: root exudates, microbes, and microbial communities. Botany 2014;92:267–275.
   Web of Science ®Google Scholar
• Imam J, Singh PK, Shukla P. Plant microbe interactions in post genomic era: perspectives and applications. Front Microbiol. 2016;7:1488.
   PubMed Web of Science ®Google Scholar
• Huang CJ, Tsay JF, Chang SY, et al. Dimethyl disulfide is an induced systemic resistance elicitor produced by Bacillus cereus C1L. Pest Manage Sci. 2012;68:1306–1310.
   PubMed Web of Science ®Google Scholar
• Cheng X, Cordovez V, Etalo DW, et al. Role of the GacS sensor kinase in the regulation of volatile production by plant growth-promoting Pseudomonas fluorescens SBW25. Front Plant Sci. 2016;7:1706.
   PubMed Web of Science ®Google Scholar
• Cho SM, Kang BR, Han SH, et al. 2R,3R-butanediol, a bacterial volatile produced by Pseudomonas chlororaphis O6, is involved in induction of systemic tolerance to drought in Arabidopsis thaliana. MPMI 2008;21:1067–1075.
   PubMed Web of Science ®Google Scholar
• Choudhary DK, Johri BN. Interactions of Bacillus spp. and plants-with special reference to induced systemic resistance (ISR). Microbiol Res. 2009;164:493–513.
   PubMed Web of Science ®Google Scholar
• Imam J, Nitin M. Toppo NN ea. A comprehensive overview on application of bioinformatics and computational statistics in rice genomics toward an amalgamated approach for improving acquaintance base. In: Kavi Kishor. PB, Bandopadhyay R, Suravajhala P, editors. Agricultural bioinformatics. New Delhi: Springer India; 2014. p. 89–107.
   Google Scholar
• Park CH, Kim TW, Son SH, et al. Brassinosteroids control AtEXPA5 gene expression in Arabidopsis thaliana. Phytochemistry. 2010;71:380–387.
   PubMed Web of Science ®Google Scholar
• Martinez-Medina A, Van Wees SCM, Pieterse CMJ. Airborne signals from Trichoderma fungi stimulate iron uptake responses in roots resulting in priming of jasmonic acid-dependent defences in shoots of Arabidopsis thaliana and Solanum lycopersicum. Plant Cell Environ. 2017;40:2691–2705.
   PubMed Web of Science ®Google Scholar
• Sanchez-Lopez AM, Bahaji A, De Diego N, et al. Arabidopsis responds to Alternaria alternata volatiles by triggering plastid phosphoglucose isomerase-independent mechanisms. Plant Physiol. 2016;172:1989–2001.
   PubMed Web of Science ®Google Scholar
• Bitas V, McCartney N, Li N, et al. Fusarium oxysporum volatiles enhance plant growth via affecting auxin transport and signaling. Front Microbiol. 2015;6:1248.
   PubMed Web of Science ®Google Scholar
• Sanchez-Lopez AM, Baslam M, De Diego N, et al. Volatile compounds emitted by diverse phytopathogenic microorganisms promote plant growth and flowering through cytokinin action. Plant Cell Environ. 2016;39:2592–2608.
   PubMed Web of Science ®Google Scholar
• Delaplace P, Delory BM, Baudson C, et al. Influence of rhizobacterial volatiles on the root system architecture and the production and allocation of biomass in the model grass Brachypodium distachyon (L.) P. Beauv. BMC Plant Biol. 2015;15:195.
   PubMed Web of Science ®Google Scholar
• Rijavec T, Lapanje A. Hydrogen cyanide in the rhizosphere: not suppressing plant pathogens, but rather regulating availability of phosphate. Front Microbiol. 2016;7:1785.
   PubMed Web of Science ®Google Scholar
• Lisjak M, Teklic T, Wilson ID. ea. Hydrogen sulfide: environmental factor or signalling molecule? Plant Cell Environ. 2013;36:1607–1616.
   PubMed Web of Science ®Google Scholar
• Garcia-Mata C, Lamattina L. Hydrogen sulphide, a novel gasotransmitter involved in guard cell signalling. New Phytol. 2010;188:977–984.
   PubMed Web of Science ®Google Scholar
• Jin ZP, Shen J, Qiao Z, et al. Hydrogen sulfide improves drought resistance in Arabidopsis thaliana. Biochem Biophys Res Commun. 2011;414:481–486.
   PubMed Web of Science ®Google Scholar
• Jia H, Hu Y, Fan T, et al. Hydrogen sulfide modulates actin-dependent auxin transport via regulating ABPs results in changing of root development in Arabidopsis. Sci Rep. 2015;5:8251.
   PubMed Web of Science ®Google Scholar
• Rushton P, Somssich I, Ringler P, et al. WRKY transcription factors. Trends Plant Sci. 2010;15:247–258.
   PubMed Web of Science ®Google Scholar
• Wenke K, Piechulla B. The effects of volatile metabolites from rhizobacteria on Arabidopsis thaliana. In: Maheshwari DK, Saraf M, A. A, editors. Bacteria in agrobiology: crop productivity. Berlin Heidelberg: Springer Berlin Heidelberg; 2013. p. 379–400.
   Google Scholar
• Fiddaman PJ, Rossall S. Effect of substrate on the production of antifungal volatiles from Bacillus subtilis. J Appl Bacteriol. 1994;76:395–405.
   PubMedGoogle Scholar
• ]Jishma P, Hussain N, Chellappan R, et al. Strain-specific variation in plant growth promoting volatile organic compounds production by five different Pseudomonas spp. as confirmed by response of Vigna radiata seedlings. J Appl Microbiol. 2017;123:204–216.
   Web of Science ®Google Scholar
• Colcombet J, Hirt H. Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. Biochem J. 2008;413:217–226.
   PubMed Web of Science ®Google Scholar
• Mauch-Mani B, Baccelli I, Luna E, et al. Defense priming: an adaptive part of induced resistance. Annu Rev Plant Biol. 2017;68:485–512.
   PubMed Web of Science ®Google Scholar
• Zhang SQ, Klessig DF. MAPK cascades in plant defense signaling. Trends Plant Sci. 2001;6:520–527.
   PubMed Web of Science ®Google Scholar
• Meng XZ, Zhang SQ. MAPK cascades in plant disease resistance signaling. Annu Rev Phytopathol. 2013;51:245–266.
   PubMed Web of Science ®Google Scholar
• Hamel LP, Nicole MC, Duplessis S, et al. Mitogen-activated protein kinase signaling in plant-interacting fungi: distinct messages from conserved messengers. Plant Cell 2012;24:1327–1351.
   PubMed Web of Science ®Google Scholar
• Yuan GL, Li HJ, Yang WC. The integration of Gβ and MAPK signaling cascade in zygote development. Sci Rep. 2017;7:8732.
   PubMed Web of Science ®Google Scholar
• Xu J, Zhang S. Mitogen-activated protein kinase cascades in signaling plant growth and development. Trends Plant Sci. 2015;20:56–64.
   PubMed Web of Science ®Google Scholar
• van Loon LC, Bakker PA, Pieterse CM. Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol. 1998;36:453–483.
   PubMed Web of Science ®Google Scholar
• Van der Does D, Leon-Reyes A, Koornneef A, et al. Salicylic acid suppresses jasmonic acid signaling downstream of SCFCOI1-JAZ by targeting GCC promoter motifs via transcription factor ORA59. Plant Cell 2013;25:744–761.
   PubMed Web of Science ®Google Scholar
• Leng YQ, Zhong SB. The role of mitogen-activated protein (MAP) kinase signaling components in the fungal development, stress response and virulence of the fungal cereal pathogen Bipolaris sorokiniana. PLoS One 2015;10:e0128291.
   PubMed Web of Science ®Google Scholar
• Nie PP, Li X, Wang SN, et al. Induced Systemic Resistance against Botrytis cinerea by Bacillus cereus AR156 through a JA/ET- and NPR1-dependent signaling pathway and activates PAMP-triggered immunity in Arabidopsis. Front Plant Sci. 2017;8:238.
   PubMed Web of Science ®Google Scholar
• Wang D, Pajerowska-Mukhtar K, Culler AH, et al. Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr Biol. 2007;17:1784–1790.
   PubMed Web of Science ®Google Scholar
• Wasternack C. Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot. 2007;100:681–697.
   PubMed Web of Science ®Google Scholar
• Wasternack C, Hause B. Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. Ann Bot. 2013;111:1021–1058.
   PubMed Web of Science ®Google Scholar
• Antico CJ, Colon C, Banks T, et al. Insights into the role of jasmonic acid-mediated defenses against necrotrophic and biotrophic fungal pathogens. Front Biol. 2012;7:48–56.
   Google Scholar
• Kuhn H, Lorek J, Kwaaitaal M, et al. Key components of different plant defense pathways are dispensable for powdery mildew resistance of the Arabidopsismlo2 mlo6 mlo12 triple mutant. Front Plant Sci. 2017;8:1006.
   PubMed Web of Science ®Google Scholar
• McSteen P, Zhao Y. Plant hormones and signaling: common themes and new developments. Dev Cell 2008;14:467–473.
   PubMed Web of Science ®Google Scholar
• Spaepen S, Vanderleyden J, Remans R. Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev. 2007;31:425–448.
   PubMed Web of Science ®Google Scholar
• Shaharoona B, Imran M, Arshad M, et al. Manipulation of ethylene synthesis in roots through bacterial ACC deaminase for improving nodulation in legumes. Crit Rev Plant Sci. 2011;30:279–291.
   Web of Science ®Google Scholar
• Iqbal N, Khan NA, Ferrante A, et al. Ethylene role in plant growth, development and senescence: interaction with other phytohormones. Front Plant Sci. 2017;8:475.
   PubMed Web of Science ®Google Scholar
• Khalid A, Akhtar MJ, Mahmood MH, et al. Effect of substrate-dependent microbial ethylene production on plant growth. Microbiology 2006;75:231–236.
   Web of Science ®Google Scholar
• Cristescu SM, De Martinis D, Hekkert ST, et al. Ethylene production by Botrytis cinerea in vitro and in tomatoes. Appl Environ Microbiol. 2002;68:5342–5350.
   PubMed Web of Science ®Google Scholar
• Eckert C, Xu W, Xiong W, et al. Ethylene-forming enzyme and bioethylene production. Biotechnol Biofuels. 2014;7:33.
   PubMed Web of Science ®Google Scholar
• Arshad M, Frankenberger WT. Jr. Microbial production of plant hormones. In: Keister DL, Cregan PB. editors. The rhizosphere and plant growth. The Netherlands: Kluwer Academic Publishers; 1991, p. 327–334.
   Google Scholar
• Leon-Reyes A, Spoel SH, De Lange ES, et al. Ethylene modulates the role of NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 in cross talk between salicylate and jasmonate signaling. Plant Physiol. 2009;149:1797–1809.
   PubMed Web of Science ®Google Scholar
• Cheng X, Etalo DW, van de Mortel JE, et al. Genome-wide analysis of bacterial determinants of plant growth promotion and induced systemic resistance by Pseudomonas fluorescens. Environ Microbiol. 2017;19:4638–4656.
   PubMed Web of Science ®Google Scholar
• Hossain MM, Sultana F, Hyakumachi M. Role of ethylene signalling in growth and systemic resistance induction by the plant growth-promoting fungus Penicillium viridicatum in Arabidopsis. J Phytopathol. 2017;165:432–441.
   Web of Science ®Google Scholar
• Chang C, Stadler R. Ethylene hormone receptor action in Arabidopsis. Bioessays. 2001;23:619–627.
   PubMed Web of Science ®Google Scholar
• Yang YX, Ahammed GJ, Wu CJ, et al. Crosstalk among jasmonate, salicylate and ethylene signaling pathways in plant disease and immune responses. CPPS 2015;16:450–461.
   Google Scholar
• Pieterse CMJ, van Wees SCM, van Pelt JA, et al. A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 1998;10:1571–1580.
   PubMed Web of Science ®Google Scholar
• Lee B, Farag MA, Park HB, et al. Induced resistance by a long-chain bacterial volatile: elicitation of plant systemic defense by a C13 volatile produced by Paenibacillus polymyxa. PLoS One 2012;7:e48744.
   PubMed Web of Science ®Google Scholar
• Noselli S, Perrimon N. Signal transduction. Are there close encounters between signaling pathways? Science 2000;290:68–69.
   PubMed Web of Science ®Google Scholar
• Sukumar P, Legue V, Vayssieres A, et al. Involvement of auxin pathways in modulating root architecture during beneficial plant-microorganism interactions. Plant Cell Environ. 2013;36:909–919.
   PubMed Web of Science ®Google Scholar
• Shi CL, Park HB, Lee JS, et al. Inhibition of primary roots and stimulation of lateral root development in Arabidopsis thaliana by the rhizobacterium Serratia marcescens 90-166 is through both auxin-dependent and -independent signaling pathways. Mol Cells 2010;29:251–258.
   PubMed Web of Science ®Google Scholar
• Contesto C, Milesi S, Mantelin S, et al. The auxin-signaling pathway is required for the lateral root response of Arabidopsis to the rhizobacterium Phyllobacterium brassicacearum. Planta 2010;232:1455–1470.
   PubMed Web of Science ®Google Scholar
• Brunoud G, Wells DM, Oliva M, et al. A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 2012;482:103–106.
   PubMed Web of Science ®Google Scholar
• Ruzicka K, Ljung K, Vanneste S, et al. Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 2007;19:2197–2212.
   PubMed Web of Science ®Google Scholar
• Mantelin S, Desbrosses G, Larcher M, et al. Nitrate-dependent control of root architecture and N nutrition are altered by a plant growth-promoting Phyllobacterium sp. Planta 2006;223:591–603.
   PubMed Web of Science ®Google Scholar
• Ortiz-Castro R, Díaz-Pérez C, Martínez-Trujillo M, et al. Transkingdom signaling based on bacterial cyclodipeptides with auxin activity in plants. Proc Nat Acad Sci U S A 2011;108:7253–7258.
   PubMed Web of Science ®Google Scholar
• Lopez-Bucio J, Millan-Godinez M, Mendez-Bravo A, et al. Cytokinin receptors are involved in alkamide regulation of root and shoot development in Arabidopsis. Plant Physiol. 2007;145:1703–1713.
   PubMed Web of Science ®Google Scholar
• Molina-Favero C, Creus CM, Simontacchi M, et al. Aerobic nitric oxide production by Azospirillum brasilense Sp245 and its influence on root architecture in tomato. MPMI 2008;21:1001–1009.
   PubMed Web of Science ®Google Scholar
• Zamioudis C, Korteland J, Van Pelt JA, et al. Rhizobacterial volatiles and photosynthesis-related signals coordinate MYB72 expression in Arabidopsis roots during onset of induced systemic resistance and iron-deficiency responses. Plant J. 2015;84:309–322.
   PubMed Web of Science ®Google Scholar
• Dobbelaere S, Croonenborghs A, Thys A, et al. Phytostimulatory effect of Azospirillum brasilense wild type and mutant strains altered in IAA production on wheat. Plant Soil. 1999;212:155–164.
   Web of Science ®Google Scholar
• Muller A, Faubert P, Hagen M, et al. Volatile profiles of fungi – chemotyping of species and ecological functions. Fungal Genet Biol. 2013;54:25–33.
   PubMed Web of Science ®Google Scholar
• Weikl F, Ghirardo A, Schnitzler JP, et al. Sesquiterpene emissions from Alternaria alternata and Fusarium oxysporum: effects of age, nutrient availability, and co-cultivation. Sci Rep. 2016;6:22152.
   PubMed Web of Science ®Google Scholar
• De Rybel B, Vassileva V, Parizot B, et al. A novel Aux/IAA28 signaling cascade activates GATA23-dependent specification of lateral root founder cell identity. Curr Biol. 2010;20:1697–1706.
   PubMed Web of Science ®Google Scholar
• Lavenus J, Goh T, Guyomarc'h S, et al. Inference of the Arabidopsis lateral root gene regulatory network suggests a bifurcation mechanism that defines primordia flanking and central zones. Plant Cell 2015;27:1368–1388.
   PubMed Web of Science ®Google Scholar
• Navarro L, Dunoyer P, Jay F, et al. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 2006;312:436–439.
   PubMed Web of Science ®Google Scholar
• Chen Z, Agnew JL, Cohen JD, et al. Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology. Proc Natl Acad Sci USA 2007;104:20131–20136.
   PubMed Web of Science ®Google Scholar
• Grant MR, Jones JDG. Hormone (Dis)harmony moulds plant health and disease. Science 2009;324:750–752.
   PubMed Web of Science ®Google Scholar
• Kazan K, Manners JM. Linking development to defense: auxin in plant-pathogen interactions. Trends Plant Sci. 2009;14:373–382.
   PubMed Web of Science ®Google Scholar
• O'Donnell PJ, Schmelz EA, Moussatche P, et al. Susceptible to intolerance – a range of hormonal actions in a susceptible Arabidopsis pathogen response. Plant J. 2003;33:245–257.
   PubMed Web of Science ®Google Scholar
• Robert-Seilaniantz A, Grant M, Jones JD. Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol. 2011;49:317–343.
   PubMed Web of Science ®Google Scholar
• Spoel SH, Dong XN. Making sense of hormone crosstalk during plant immune responses. Cell Host Microbe. 2008;3:348–351.
   PubMed Web of Science ®Google Scholar
• Lee S, Hung R, Yap M, et al. Age matters: the effects of volatile organic compounds emitted by Trichoderma atroviride on plant growth. Arch Microbiol. 2015;197:723–727.
   PubMed Web of Science ®Google Scholar
• Imam J, Shukla P, Mandal NP, et al. Microbial interactions in plants: perspectives and applications of proteomics. Curr Protein Pept Sci. 2017;18:956–965.
   PubMed Web of Science ®Google Scholar