Abstract
Microbial volatile organic compounds (mVOCs) play important roles in inter- and intra-kingdom interactions, and they are also important as signal molecules in physiological processes acting either as plant growth-promoting or negatively modulating plant development. We investigated the effects of mVOCs emitted by PGPR vs non-PGPR from avocado trees (Persea americana) on growth of Arabidopsis thaliana seedlings. Chemical diversity of mVOCs was determined by SPME–GC–MS; selected compounds were screened in dose–response experiments in A. thaliana transgenic lines. We found that plant growth parameters were affected depending on inoculum concentration. Twenty-six compounds were identified in PGPR and non-PGPR with eight of them not previously reported. The VOCs signatures were differential between those groups. 4-methyl-2-pentanone, 1-nonanol, 2-phenyl-2-propanol and ethyl isovalerate modified primary root architecture influencing the expression of auxin- and JA-responsive genes, and cell division. Lateral root formation was regulated by 4-methyl-2-pentanone, 3-methyl-1-butanol, 1-nonanol and ethyl isovalerate suggesting a participation via JA signalling. Our study revealed the differential emission of volatiles by PGPR vs non-PGPR from avocado trees and provides a general view about the mechanisms by which those volatiles influence plant growth and development. Rhizobacteria strains and mVOCs here reported are promising for improvement the growth and productivity of avocado crop.
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References
Ahmad M, Zahir ZA, Khalid M et al (2013) Efficacy of Rhizobium and Pseudomonas strains to improve physiology, ionic balance and quality of mung bean under salt-affected conditions on farmer’s fields. Plant Physiol Biochem PPB 63:170–176. https://doi.org/10.1016/j.plaphy.2012.11.024
Anzola JM, Sieberer T, Ortbauer M et al (2010) Putative Arabidopsis transcriptional adaptor protein (PROPORZ1) is required to modulate histone acetylation in response to auxin. Proc Natl Acad Sci U S A 107:10308–10313. https://doi.org/10.1073/pnas.0913918107
Arora NK, Khare E, Oh JH et al (2008) Diverse mechanisms adopted by fluorescent Pseudomonas PGC2 during the inhibition of Rhizoctonia solani and Phytophthora capsici. World J Microbiol Biotechnol 24:581–585. https://doi.org/10.1007/s11274-007-9505-5
Atkinson JA, Rasmussen A, Traini R et al (2014) Branching Out in Roots: Uncovering Form, Function, and Regulation. Plant Physiol 166:538–550. https://doi.org/10.1104/pp.114.245423
Bailly A, Groenhagen U, Schulz S et al (2014) The inter-kingdom volatile signal indole promotes root development by interfering with auxin signalling. Plant J Cell Mol Biol 80:758–771. https://doi.org/10.1111/tpj.12666
Bais HP, Weir TL, Perry LG et al (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266. https://doi.org/10.1146/annurev.arplant.57.032905.105159
Bhattacharyya D, Garladinne M, Lee YH (2015) Volatile indole produced by Rhizobacterium Proteus vulgaris JBLS202 stimulates growth of Arabidopsis thaliana through auxin, cytokinin, and brassinosteroid pathways. J Plant Growth Regul 34:158–168. https://doi.org/10.1007/s00344-014-9453-x
Blom D, Fabbri C, Connor EC et al (2011) Production of plant growth modulating volatiles is widespread among rhizosphere bacteria and strongly depends on culture conditions. Environ Microbiol 13:3047–3058. https://doi.org/10.1111/j.1462-2920.2011.02582.x
Brock AK, Berger B, Mewis I, Ruppel S (2013) Impact of the PGPB Enterobacter radicincitans DSM 16656 on growth, glucosinolate profile, and immune responses of Arabidopsis thaliana. Microb Ecol 65:661–670. https://doi.org/10.1007/s00248-012-0146-3
Buśko M, Kulik T, Ostrowska A et al (2014) Quantitative volatile compound profiles in fungal cultures of three different Fusarium graminearum chemotypes. FEMS Microbiol Lett 359:85–93. https://doi.org/10.1111/1574-6968.12569
Camarena-Pozos DA, Flores-Núñez VM, López MG et al (2019) Smells from the desert: Microbial volatiles that affect plant growth and development of native and non-native plant species. Plant Cell Environ 42:1368–1380. https://doi.org/10.1111/pce.13476
Campos Ziegenbein F, Hanssen H-P, König WA (2006) Secondary metabolites from Ganoderma lucidum and Spongiporus leucomallellus. Phytochemistry 67:202–211. https://doi.org/10.1016/j.phytochem.2005.10.025
Castulo-Rubio DY, Alejandre-Ramírez NA, del Orozco-Mosqueda M, C, et al (2015) Volatile organic compounds produced by the Rhizobacterium Arthrobacter agilis UMCV2 modulate Sorghum bicolor (strategy II plant) morphogenesis and SbFRO1 transcription in vitro. J Plant Growth Regul 34:611–623. https://doi.org/10.1007/s00344-015-9495-8
Chen Y, Palta JA, Wu P, Siddique KHM (2019) Crop root systems and rhizosphere interactions. Plant Soil 439:1–5. https://doi.org/10.1007/s11104-019-04154-2
Choudhary DK, Sharma KP, Gaur RK (2011) Biotechnological perspectives of microbes in agro-ecosystems. Biotechnol Lett 33:1905–1910. https://doi.org/10.1007/s10529-011-0662-0
Contesto C, Milesi S, Mantelin S et al (2010) The auxin-signaling pathway is required for the lateral root response of Arabidopsis to the rhizobacterium Phyllobacterium brassicacearum. Planta 232:1455–1470. https://doi.org/10.1007/s00425-010-1264-0
Cordovez V, Mommer L, Moisan K, et al (2017) Plant phenotypic and transcriptional changes induced by volatiles from the fungal root pathogen Rhizoctonia solani. Front Plant Sci 8: https://doi.org/10.3389/fpls.2017.01262
Davis TS, Boundy-Mills K, Landolt PJ (2012) Volatile emissions from an epiphytic fungus are semiochemicals for eusocial wasps. Microb Ecol 64:1056–1063. https://doi.org/10.1007/s00248-012-0074-2
De Smet I, Zhang H, Inzé D, Beeckman T (2006) A novel role for abscisic acid emerges from underground. Trends Plant Sci 11:434–439. https://doi.org/10.1016/j.tplants.2006.07.003
Dickschat JS, Martens T, Brinkhoff T, Simon M, Schulz S (2005) Volatiles released by a Streptomyces species isolated from the North Sea. Chem Biodivers 2:837–865. https://doi.org/10.1002/cbdv.200590062
Ditengou FA, Müller A, Rosenkranz M et al (2015) Volatile signalling by sesquiterpenes from ectomycorrhizal fungi reprogrammes root architecture. Nat Commun 6:6279. https://doi.org/10.1038/ncomms7279
Ercolini D, Russo F, Nasi A et al (2009) Mesophilic and Psychrotrophic bacteria from meat and their spoilage potential in vitro and in beef. Appl Environ Microbiol 75:1990–2001. https://doi.org/10.1128/AEM.02762-08
FAO (2021) Food and Agriculture Organization of the United Nations. http://www.fao.org/home/en/. Accessed 12 May 2021
Ferreira CMH, Soares HMVM, Soares EV (2019) Promising bacterial genera for agricultural practices: an insight on plant growth-promoting properties and microbial safety aspects. Sci Total Environ 682:779–799. https://doi.org/10.1016/j.scitotenv.2019.04.225
Fincheira P, Quiroz A (2018) Microbial volatiles as plant growth inducers. Microbiol Res 208:63–75. https://doi.org/10.1016/j.micres.2018.01.002
Fitter A, Williamson L, Linkohr B, Leyser O (2002) Root system architecture determines fitness in an Arabidopsis mutant in competition for immobile phosphate ions but not for nitrate ions. Proc R Soc B Biol Sci 269:2017–2022. https://doi.org/10.1098/rspb.2002.2120
Flores-Félix JD, Silva LR, Rivera LP, et al (2015) Plants probiotics as a tool to produce highly functional fruits: the case of Phyllobacterium and vitamin C in strawberries. PLoS ONE 10: https://doi.org/10.1371/journal.pone.0122281
Garbeva P, Hordijk C, Gerards S, De Boer W (2014) Volatiles produced by the mycophagous soil bacterium Collimonas. FEMS Microbiol Ecol 87:639–649. https://doi.org/10.1111/1574-6941.12252
García-Fraile P, Menéndez E, Rivas R et al (2015) Role of bacterial biofertilizers in agriculture and forestry. AIMS Bioeng 2:183–205. https://doi.org/10.3934/bioeng.2015.3.183
Garnica-Vergara A, Barrera-Ortiz S, Muñoz-Parra E et al (2016) 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 209:1496–1512. https://doi.org/10.1111/nph.13725
Gérard F, Blitz-Frayret C, Hinsinger P, Pagès L (2017) Modelling the interactions between root system architecture, root functions and reactive transport processes in soil. Plant Soil 413:161–180. https://doi.org/10.1007/s11104-016-3092-x
Giehl RFH, von Wirén N (2014) Root nutrient foraging. Plant Physiol 166:509–517. https://doi.org/10.1104/pp.114.245225
Groenhagen U, Baumgartner R, Bailly A et al (2013) Production of bioactive volatiles by different Burkholderia ambifaria strains. J Chem Ecol 39:892–906. https://doi.org/10.1007/s10886-013-0315-y
Guevara-Avendaño E, Bejarano-Bolívar AA, Kiel-Martínez A-L et al (2019) Avocado rhizobacteria emit volatile organic compounds with antifungal activity against Fusarium solani, Fusarium sp. associated with Kuroshio shot hole borer, and Colletotrichum gloeosporioides. Microbiol Res 219:74–83. https://doi.org/10.1016/j.micres.2018.11.009
Gutiérrez-Luna FM, López-Bucio J, Altamirano-Hernández J et al (2010) Plant growth-promoting rhizobacteria modulate root-system architecture in Arabidopsis thaliana through volatile organic compound emission. Symbiosis 51:75–83. https://doi.org/10.1007/s13199-010-0066-2
Hayashi K, Hasegawa J, Matsunaga S (2013) The boundary of the meristematic and elongation zones in roots: endoreduplication precedes rapid cell expansion. Sci Rep 3:2723. https://doi.org/10.1038/srep02723
Hernández-Calderón E, Aviles-Garcia ME, Castulo-Rubio DY et al (2018) Volatile compounds from beneficial or pathogenic bacteria differentially regulate root exudation, transcription of iron transporters, and defense signaling pathways in Sorghum bicolor. Plant Mol Biol 96:291–304. https://doi.org/10.1007/s11103-017-0694-5
Hettinga KA, van Valenberg HJF, Lam TJGM, van Hooijdonk ACM (2008) Detection of mastitis pathogens by analysis of volatile bacterial metabolites. J Dairy Sci 91:3834–3839. https://doi.org/10.3168/jds.2007-0941
Holighaus G, Weißbecker B, von Fragstein M, Schütz S (2014) Ubiquitous eight-carbon volatiles of fungi are infochemicals for a specialist fungivore. Chemoecology 24:57–66. https://doi.org/10.1007/s00049-014-0151-8
Ishimaru Y, Hayashi K, Suzuki T et al (2018) Jasmonic acid inhibits auxin-induced lateral rooting independently of the CORONATINE INSENSITIVE1 receptor. Plant Physiol 177:1704–1716. https://doi.org/10.1104/pp.18.00357
Kanchiswamy CN, Malnoy M, Maffei ME (2015) Chemical diversity of microbial volatiles and their potential for plant growth and productivity. Front Plant Sci 6: https://doi.org/10.3389/fpls.2015.00151
Kumar H, Bajpai VK, Dubey RC et al (2010) Wilt disease management and enhancement of growth and yield of Cajanus cajan (L) var. Manak by bacterial combinations amended with chemical fertilizer. Crop Prot 29:591–598. https://doi.org/10.1016/j.cropro.2010.01.002
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Lavakush YJ, Verma JP et al (2014) Evaluation of PGPR and different concentration of phosphorus level on plant growth, yield and nutrient content of rice (Oryza sativa). Ecol Eng 62:123–128. https://doi.org/10.1016/j.ecoleng.2013.10.013
Lavenus J, Goh T, Roberts I et al (2013) Lateral root development in Arabidopsis: fifty shades of auxin. Trends Plant Sci 18:450–458. https://doi.org/10.1016/j.tplants.2013.04.006
Ledger T, Rojas S, Timmermann T et al (2016) Volatile-mediated effects predominate in Paraburkholderia phytofirmans growth promotion and salt stress tolerance of Arabidopsis thaliana. Front Microbiol 7:1838. https://doi.org/10.3389/fmicb.2016.01838
Lee B, Farag MA, Park HB et al (2012) Induced resistance by a long-chain bacterial volatile: elicitation of plant systemic defense by a C13 volatile produced by Paenibacillus polymyxa. PLoS ONE 7:e48744. https://doi.org/10.1371/journal.pone.0048744
Lemfack MC, Gohlke B-O, Toguem SMT et al (2018) mVOC 2.0: a database of microbial volatiles. Nucleic Acids Res 46:D1261–D1265. https://doi.org/10.1093/nar/gkx1016
Liu Y, Donner E, Lombi E et al (2013) Assessing the contributions of lateral roots to element uptake in rice using an auxin-related lateral root mutant. Plant Soil 372:125–136. https://doi.org/10.1007/s11104-012-1582-z
Lu C, Chen M-X, Liu R, et al (2019) Abscisic acid regulates auxin distribution to mediate maize lateral root development under salt stress. Front Plant Sci 10: https://doi.org/10.3389/fpls.2019.00716
Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Dev Camb Engl 124:33–44
Martínez-Viveros O, Jorquera MA, Crowley DE et al (2010) Mechanisms and practical considerations involved in plant growth promotion by Rhizobacteria. J Soil Sci Plant Nutr 10:293–319. https://doi.org/10.4067/S0718-95162010000100006
Meldau DG, Long HH, Baldwin IT (2012) A native plant growth promoting bacterium, Bacillus sp. B55, rescues growth performance of an ethylene-insensitive plant genotype in nature. Front Plant Sci 3: https://doi.org/10.3389/fpls.2012.00112
Morita T, Tanaka I, Ryuda N et al (2019) Antifungal spectrum characterization and identification of strong volatile organic compounds produced by Bacillus pumilus TM-R. Heliyon 5:e01817. https://doi.org/10.1016/j.heliyon.2019.e01817
Naznin HA, Kiyohara D, Kimura M et al (2014) Systemic resistance induced by volatile organic compounds emitted by plant growth-promoting fungi in Arabidopsis thaliana. PLoS ONE 9:e86882. https://doi.org/10.1371/journal.pone.0086882
Nicholson TP, Rudd BA, Dawson M et al (2001) Design and utility of oligonucleotide gene probes for fungal polyketide synthases. Chem Biol 8:157–178. https://doi.org/10.1016/s1074-5521(00)90064-4
Orman-Ligeza B, Parizot B, Gantet PP et al (2013) Post-embryonic root organogenesis in cereals: branching out from model plants. Trends Plant Sci 18:459–467. https://doi.org/10.1016/j.tplants.2013.04.010
Ortíz-Castro R, Contreras-Cornejo HA, Macías-Rodríguez L, López-Bucio J (2009) The role of microbial signals in plant growth and development. Plant Signal Behav 4:701–712
Ortíz-Castro R, Valencia-Cantero E, López-Bucio J (2008) Plant growth promotion by Bacillus megaterium involves cytokinin signaling. Plant Signal Behav 3:263–265
Park Y-S, Dutta S, Ann M et al (2015) Promotion of plant growth by Pseudomonas fluorescens strain SS101 via novel volatile organic compounds. Biochem Biophys Res Commun 461:361–365. https://doi.org/10.1016/j.bbrc.2015.04.039
Péret B, Larrieu A, Bennett MJ (2009) Lateral root emergence: a difficult birth. J Exp Bot 60:3637–3643. https://doi.org/10.1093/jxb/erp232
Piechulla B, Degenhardt J (2014) The emerging importance of microbial volatile organic compounds. Plant Cell Environ 37:811–812. https://doi.org/10.1111/pce.12254
Piechulla B, Lemfack MC, Kai M (2017) Effects of discrete bioactive microbial volatiles on plants and fungi. Plant Cell Environ 40:2042–2067. https://doi.org/10.1111/pce.13011
Ping L, Boland W (2004) Signals from the underground: bacterial volatiles promote growth in Arabidopsis. Trends Plant Sci 9:263–266. https://doi.org/10.1016/j.tplants.2004.04.008
Qessaoui R, Bouharroud R, Furze JN et al (2019) Applications of new Rhizobacteria Pseudomonas isolates in agroecology via fundamental processes complementing plant growth. Sci Rep 9:12832. https://doi.org/10.1038/s41598-019-49216-8
Raya González J, Velázquez Becerra C, Barrera Ortiz S et al (2017) N, N-dimethyl hexadecylamine and related amines regulate root morphogenesis via jasmonic acid signaling in Arabidopsis thaliana. Protoplasma 254:1399–1410. https://doi.org/10.1007/s00709-016-1031-6
Raya-González J, Ortiz-Castro R, López-Bucio J (2019) Determinate root development in the halted primary root1 mutant of Arabidopsis correlates with death of root initial cells and an enhanced auxin response. Protoplasma 256:1657–1666. https://doi.org/10.1007/s00709-019-01409-8
Raya-González J, Pelagio-Flores R, López-Bucio J (2012) The jasmonate receptor COI1 plays a role in jasmonate-induced lateral root formation and lateral root positioning in Arabidopsis thaliana. J Plant Physiol 169:1348–1358. https://doi.org/10.1016/j.jplph.2012.05.002
Raya-González J, Velázquez-Becerra C, Barrera-Ortiz S et al (2017) N, N-dimethyl hexadecylamine and related amines regulate root morphogenesis via jasmonic acid signaling in Arabidopsis thaliana. Protoplasma 254:1399–1410. https://doi.org/10.1007/s00709-016-1031-6
Robson F, Okamoto H, Patrick E et al (2010) Jasmonate and phytochrome A signaling in Arabidopsis wound and shade responses are integrated through JAZ1 stability. Plant Cell 22:1143–1160. https://doi.org/10.1105/tpc.109.067728
Ryu C-M, Farag MA, Hu C-H et al (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci 100:4927–4932. https://doi.org/10.1073/pnas.0730845100
Santoro MV, Zygadlo J, Giordano W, Banchio E (2011) Volatile organic compounds from rhizobacteria increase biosynthesis of essential oils and growth parameters in peppermint (Mentha piperita). Plant Physiol Biochem PPB 49:1177–1182. https://doi.org/10.1016/j.plaphy.2011.07.016
Schleibinger H, Laussmann D, Brattig C et al (2005) Emission patterns and emission rates of MVOC and the possibility for predicting hidden mold damage? Indoor Air 15(Suppl 9):98–104. https://doi.org/10.1111/j.1600-0668.2005.00349.x
Schulz S, Dickschat JS (2007) Bacterial volatiles: the smell of small organisms. Nat Prod Rep 24:814–842. https://doi.org/10.1039/b507392h
Sharifi R, Ryu C-M (2018) Revisiting bacterial volatile-mediated plant growth promotion: lessons from the past and objectives for the future. Ann Bot 122:349–358. https://doi.org/10.1093/aob/mcy108
Sheoran N, Valiya Nadakkakath A, Munjal V et al (2015) Genetic analysis of plant endophytic Pseudomonas putida BP25 and chemo-profiling of its antimicrobial volatile organic compounds. Microbiol Res 173:66–78. https://doi.org/10.1016/j.micres.2015.02.001
Shi C-L, Park H-B, Lee JS et al (2010) 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 29:251–258. https://doi.org/10.1007/s10059-010-0032-0
Sieberer T, Hauser M-T, Seifert GJ, Luschnig C (2003) PROPORZ1, a putative Arabidopsis transcriptional adaptor protein, mediates auxin and cytokinin signals in the control of cell proliferation. Curr Biol 13:837–842. https://doi.org/10.1016/S0960-9822(03)00327-0
Somova LA, Pechurkin NS, Sarangova AB, Pisman TI (2001) Effect of bacterial population density on germination wheat seeds and dynamics of simple artificial ecosystems. Adv Space Res 27:1611–1615. https://doi.org/10.1016/S0273-1177(01)00257-5
Song GC, Ryu C-M (2013) Two Volatile organic compounds trigger plant self-defense against a bacterial pathogen and a sucking insect in cucumber under open field conditions. Int J Mol Sci 14:9803–9819. https://doi.org/10.3390/ijms14059803
Spaepen S, Vanderleyden J, Okon Y (2009) Chapter 7 Plant growth-promoting actions of rhizobacteria. In: Advances in Botanical Research. Academic Press, 283–320
Stolz JF (2017) Gaia and her microbiome. FEMS Microbiol Ecol 93: https://doi.org/10.1093/femsec/fiw247
Sukumar P, Legué V, Vayssières A et al (2013) Involvement of auxin pathways in modulating root architecture during beneficial plant-microorganism interactions. Plant Cell Environ 36:909–919. https://doi.org/10.1111/pce.12036
Sunesson A, Vaes W, Nilsson C et al (1995) Identification of volatile metabolites from five fungal species cultivated on two media. Appl Environ Microbiol 61:2911–2918
Tahir HAS, Gu Q, Wu H, et al (2017a) Plant growth promotion by volatile organic compounds produced by Bacillus subtilis SYST2. Front Microbiol 8: https://doi.org/10.3389/fmicb.2017.00171
Tahir HAS, Gu Q, Wu H et al (2017b) Effect of volatile compounds produced by Ralstonia solanacearum on plant growth promoting and systemic resistance inducing potential of Bacillus volatiles. BMC Plant Biol 17:133. https://doi.org/10.1186/s12870-017-1083-6
Tanimoto E (2005) Regulation of root growth by plant hormones—roles for auxin and gibberellin. Crit Rev Plant Sci 24:249–265. https://doi.org/10.1080/07352680500196108
Thines B, Katsir L, Melotto M et al (2007) JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448:661–665. https://doi.org/10.1038/nature05960
Toffano L, Fialho MB, Pascholati SF (2017) Potential of fumigation of orange fruits with volatile organic compounds produced by Saccharomyces cerevisiae to control citrus black spot disease at postharvest. Biol Control 108:77–82. https://doi.org/10.1016/j.biocontrol.2017.02.009
Tyagi S, Kim K, Cho M, Lee KJ (2019) Volatile dimethyl disulfide affects root system architecture of Arabidopsis via modulation of canonical auxin signaling pathways. Environ Sustain 2:211–216. https://doi.org/10.1007/s42398-019-00060-6
Tyagi S, Mulla SI, Lee K-J et al (2018) VOCs-mediated hormonal signaling and crosstalk with plant growth promoting microbes. Crit Rev Biotechnol 38:1277–1296. https://doi.org/10.1080/07388551.2018.1472551
Olaf T, Song C, Dickschat JS et al (2017) The ecological role of volatile and soluble secondary metabolites produced by soil bacteria. Trends Microbiol 25:280–292. https://doi.org/10.1016/j.tim.2016.12.002
Tzec-Interián JA, Desgarennes D, Carrión G et al (2020) Characterization of plant growth-promoting bacteria associated with avocado trees (Persea americana Miller) and their potential use in the biocontrol of Scirtothrips perseae (avocado thrips). PLoS ONE 15:e0231215. https://doi.org/10.1371/journal.pone.0231215
Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971. https://doi.org/10.1105/tpc.9.11.1963
Vaishnav A, Kumari S, Jain S et al (2015) Putative bacterial volatile-mediated growth in soybean (Glycine max L. Merrill) and expression of induced proteins under salt stress. J Appl Microbiol 119:539–551. https://doi.org/10.1111/jam.12866
Vejan P, Abdullah R, Khadiran T, et al (2016) Role of plant growth promoting rhizobacteria in agricultural sustainability-a review. Mol Basel Switz 21: https://doi.org/10.3390/molecules21050573
Velázquez-Becerra C, Macías-Rodríguez LI, López-Bucio J et al (2011) 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 339:329–340. https://doi.org/10.1007/s11104-010-0583-z
Weller DM, Landa BB, Mavrodi OV et al (2007) Role of 2,4-diacetylphloroglucinol-producing fluorescent Pseudomonas spp. in the defense of plant roots. Plant Biol Stuttg Ger 9:4–20. https://doi.org/10.1055/s-2006-924473
Wu S, Tohge T, Cuadros-Inostroza Á et al (2018) Mapping the Arabidopsis metabolic landscape by untargeted metabolomics at different environmental conditions. Mol Plant 11:118–134. https://doi.org/10.1016/j.molp.2017.08.012
Xie S-S, Wu H-J, Zang H-Y et al (2014) Plant growth promotion by spermidine-producing Bacillus subtilis OKB105. Mol Plant-Microbe Interact 27:655–663. https://doi.org/10.1094/MPMI-01-14-0010-R
Xu Y-Y, Lu H, Wang X et al (2015) Effect of volatile organic compounds from bacteria on nematodes. Chem Biodivers 12:1415–1421. https://doi.org/10.1002/cbdv.201400342
Yu S-M, Lee YH (2013) Plant growth promoting rhizobacterium Proteus vulgaris JBLS202 stimulates the seedling growth of Chinese cabbage through indole emission. Plant Soil 370:485–495. https://doi.org/10.1007/s11104-013-1652-x
Zhang H, Kim M-S, Krishnamachari V et al (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226:839–851. https://doi.org/10.1007/s00425-007-0530-2
Zou C, Li Z, Yu D (2010) Bacillus megaterium strain XTBG34 promotes plant growth by producing 2-pentylfuran. J Microbiol Seoul Korea 48:460–466. https://doi.org/10.1007/s12275-010-0068-z
Acknowledgements
We thank the Consejo Nacional de Ciencia y Tecnología (CONACYT) for the grants no. PDCPN-2015-882, FORDECyT-PRONACES 292399 and the Asociación de Productores y Empacadores Exportadores de Aguacate de México A.C. (APEAM) for the grant no. 42002. R.G.B thanks APEAM for his postdoctoral fellowship. We thank M. Sc. Diana Yuridia López Ley and M. Sc. Nut Liahut Guin for their technical support in volatiles dose-dependent experiments, providing and maintaining of bacteria strains, and isolation of DNA and amplification of 16S rRNA gene.
Funding
This work was financed by grants from the Asociación de Productores y Empacadores Exportadores de Aguacate de México A.C. (APEAM)-Instituto de Ecología A.C. (INECOL) (grant no. 42002); Consejo Nacional de Ciencia y Tecnología (CONACYT, México, grants PDCPN-2015–882 and FORDECYT-PRONACES 292399).
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R.G.B., D.D. and R.O.C. conceived and designed the experiments; R.G.B. performed experiments; R.G.B. and R.O.C. analyzed the data; G.C. and R.O.C. contributed reagents/materials/analysis tools; R.G.B. and R.O.C. wrote the paper; R.G.B, D.D., R.O.C. and G.C. reviewed and edited the paper. G.C. and R.O.C. applied for funding. J.M.T., E.R.C. and A.L.K.M. provided reagents, material and technical support for GC–MS analysis.
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Fig. S1
Representative images of shoot and root growth of Arabidopsis seedlings in response to avocado rhizobacteria volatiles exposure. Seven-day-old A. thaliana seedlings were co-inoculated with 20 µL of liquid culture of (a) PGPR and (b) non-PGPR strains, containing either 1x104, 1x106 and 1x108 total CFU, or 20 µL of LB medium (0 µM). All assays were performed in triplicates. At least 10 transgenic seedlings were analyzed with a Leica S8 APO stereoscopic microscope. Shoot and root system images were captured with a Sony Cyber-shot DSC-S75 digital camera adapted to the microscope. Scale bar = 500 µm. (PNG 24658 KB)
Fig. S2
Typical total ion chromatograms (TICs) of VOCs detected in the headscape of Petri dishes from PGPR and non-PGPR strains from avocado rhizosphere. Eight sterilized sedes of A. thaliana were germinated and grown in one half of the plate. After seven days, A. thaliana seedlings were co-inoculated in the second compartment with 20 μL of the selected bacterial strains. All assays were performed in triplicates. Seven days after inoculation, SPME fibers were introduced and kept for 2 hours into the headspace of Petri plates. The captured volatiles were analyzed by GC-MS, which was performed independently for A. thaliana-bacteria co-culture, and for plant and bacteria grown alone, and for culture media. (PNG 4688 KB)
Fig. S3
Fig. S3 Effect of selected pure VOCs on Arabidopsis biomass parameters. Six compounds were selected for growth promotion assays: 2-phenyl-2-propanol, ethyl isovalerate, 1-nonanol, 3-octanone, 3-methyl-1-butanol and 4-methyl-2-pentanone. The pure VOCs were screened at three different concentrations: 25, 50 and 100 µM. In vitro plant growth-promotion assays were performed by using seven-days-old A. thaliana seedlings, which were exposed to 25 µL of each different dilution of the standard compounds (dissolved in water), and 25 µL of only water as negative control applied to a sterile filter paper (diameter of 1.85 cm) in the other side of the two-compartment plate. The experiments were performed in triplicate. After seven days of individual mVOC exposition, (a) shoot fresh weight and (b) root fresh weight were measured. Data points represent mean of eight seedlings (three replicates) ± SD (n=24). Dashed red line indicates control average. Different letters indicate statistical difference at P<0.05. (PNG 914 KB)
Fig. S4
Representative images of shoot and root growth of Arabidopsis seedlings in response to pure VOCs treatment. Seven days-old A. thaliana seedlings were exposed to three different concentrations (25, 50 and 100 µM) of the six pure compounds selected: a) 4-Methyl-2-pentanone, b) 3-Methyl-1-butanol, c) 3-Octanone, d) 1-Nonanol, e) 2-Phenyl-2-propanol, f) Ethyl isovalerate. All assays were performed in triplicates. After seven days of mVOCs exposition, at least 10 transgenic seedlings were analyzed with a stereoscopic microscope. Shoot and root system images were captured with a digital camera adapted to the microscope. Scale bar = 500 µm. (PNG 21797 KB)
Fig. S5
GUS activity detected in shoot and lateral roots of DR5::uidA and PRZ1::uidAPRZ1::uidA transgenic lines in a dose-response volatile assays. Expression of (a) DR5::uidA and (b) PRZ1::uidA gene constructs was evaluated in response to exposure of transgenic lines at three different concentrations (25, 50 and 100 µM) of each of the six pure compounds (2-phenyl-2-propanol, ethyl isovalerate, 1-nonanol, 3-octanone, 3-methyl-1-butanol and 4-methyl-2-pentanone) selected for this experiment. The experiments were performed by triplicate. After seven days of individual mVOC exposition, A. thaliana seedlings expressing the uidA reporter gene were incubated at 37 °C in GUS reaction buffer (0.5 mg/mL of 5-bromo-4-chloro-3-indolyl-β-D-glucuronide in 100 mM sodium phosphate, pH 7) overnight. The stained seedlings were cleared and photographed. Photographs are representative of at least eighteen stained seedlings. Scale bar = 500 µm. (PNG 10493 KB)
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Gamboa-Becerra, R., Desgarennes, D., Molina-Torres, J. et al. Plant growth-promoting and non-promoting rhizobacteria from avocado trees differentially emit volatiles that influence growth of Arabidopsis thaliana. Protoplasma 259, 835–854 (2022). https://doi.org/10.1007/s00709-021-01705-2
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DOI: https://doi.org/10.1007/s00709-021-01705-2