Abstract
Key message
Our results show that Sorghum bicolor is able to recognize bacteria through its volatile compounds and differentially respond to beneficial or pathogens via eliciting nutritional or defense adaptive traits.
Abstract
Plants establish beneficial, harmful, or neutral relationships with bacteria. Plant growth promoting rhizobacteria (PGPR) emit volatile compounds (VCs), which may act as molecular cues influencing plant development, nutrition, and/or defense. In this study, we compared the effects of VCs produced by bacteria with different lifestyles, including Arthrobacter agilis UMCV2, Bacillus methylotrophicus M4-96, Sinorhizobium meliloti 1021, the plant pathogen Pseudomonas aeruginosa PAO1, and the commensal rhizobacterium Bacillus sp. L2-64, on S. bicolor. We show that VCs from all tested bacteria, except Bacillus sp. L2-64, increased biomass and chlorophyll content, and improved root architecture, but notheworthy A. agilis induced the release of attractant molecules, whereas P. aeruginosa activated the exudation of growth inhibitory compounds by roots. An analysis of the expression of iron-transporters SbIRT1, SbIRT2, SbYS1, and SbYS2 and genes related to plant defense pathways COI1 and PR-1 indicated that beneficial, pathogenic, and commensal bacteria could up-regulate iron transporters, whereas only beneficial and pathogenic species could induce a defense response. These results show how S. bicolor could recognize bacteria through their volatiles profiles and highlight that PGPR or pathogens can elicit nutritional or defensive traits in plants.
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References
Abadía J, Vázquez S, Rellán-Álvarez R, El-Jendoubi H, Abadía A, Álvarez-Fernández A, López-Millán AF (2011) Towards a knowledge-based correction of Fe chlorosis. Plant Physiol Biochem 49:471–482. https://doi.org/10.1016/j.plaphy.2011.01.02
Aka RJN, Babalola OO (2016) Effect of bacterial inoculation of strains of Pseudomonas aeruginosa, Alcaligenes feacalis and Bacillus subtilis on germination, growth and heavy metal (Cd, Cr, and Ni) uptake of Brassica juncea. Int J Phytorem 18:200–209. https://doi.org/10.1080/15226514.2015.1073671
Attila C, Ueda A, Cirillo SLG, Cirillo JD, Chen W, Wood TK (2008) Pseudomonas aeruginosa PAO1 virulence factors and poplar tree response in the rhizosphere. Microb Biotechnol 1:17–29. https://doi.org/10.1111/j.1751-7915.2007.00002.x
Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681. https://doi.org/10.1111/j.1365-3040.2009.01926.x
Bailly A, Weisskopf L (2012) The modulating effect of bacterial volatiles on plant growth: current knowledge and future challenges. Plant Signal Behav 7:79–85. https://doi.org/10.4161/psb.7.1.18418
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. https://doi.org/10.1146/annurev.arplant.57.032905.105159
Bakker PA, Berendsen RL, Doornbos RF, Wintermans PC, Pieterse CM (2013) The rhizosphere revisited: root microbiomics. Front Plant Sci 4:165. https://doi.org/10.3389/fpls.2013.00165
Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486. https://doi.org/10.1016/j.tplants.2012.04.001
Bertin C, Yang X, Weston LA (2003) The role of root exudates and allelochemicals. Plant Soil 256:67–83. https://doi.org/10.1023/A:1026290508166
Blom D, Fabbri C, Eberl L, Weisskopf L (2011a) Volatile-mediated killing of Arabidopsis thaliana by bacteria is mainly due to hydrogen cyanide. Appl Environ Microb 77:1000–1008. https://doi.org/10.1128/AEM.01968-10
Blom D, Fabbri C, Connor EC, Schiestl FP, Klauser DR, Boller T, Eberl L, Weisskopf L (2011b) 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
Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco JM (2008) Root exudates regulate soil fungal community composition and diversity. Appl Environ Microb 74:738–744. https://doi.org/10.1128/AEM.02188-07
Castulo-Rubio DY, Alejandre-Ramírez NA, Orozco-Mosqueda MC, Santoyo G, Macías-Rodríguez LI, Valencia-Cantero E (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
Curie C, Panaviene Z, Loulergue C, Dellaporta SL, Briat JF, Walker EL (2001) Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409:346–349. https://doi.org/10.1038/35053080
DiDonato RJ, Roberts LA, Sanderson T, Eisley RB, Walker EL (2004) Arabidopsis yellow stripe-like2 (YSL2): a metal-regulated gene encoding a plasma membrane transporter of nicotianamine–metal complexes. Plant J 39:403–414. https://doi.org/10.1111/j.1365-313X.2004.02128.x
Eide D, Broderius M, Fett J, Guerinot ML (1996) A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci USA 93:5624–5628
Eng BH, Guerinot ML, Eide D, Saier MH Jr (1998) Sequence analyses and phylogenetic characterization of the ZIP family of metal ion transport proteins. J Membr Biol 166:1–7. https://doi.org/10.1007/s002329900442
Enomoto Y, Goto F (2013) Long-distance signaling of iron deficiency in plants. In: Baluska F (ed) Long-distance systemic signaling and communication in plants. Springer, Berlin, pp 167–188
García-Gutiérrez L, Zeriouh H, Romero D, Cubero J, Vicente A, Pérez-García A (2013) The antagonistic strain Bacillus subtilis UMAF6639 also confers protection to melon plants against cucurbit powdery mildew by activation of jasmonate and salicylic acid-dependent defence responses. Microb Biotechnol 6:264–274. https://doi.org/10.1111/1751-7915.12028
Gutiérrez-Luna FM, López-Bucio J, Altamirano-Hernández J, Valencia-Cantero E, de la Cruz HR, Macías-Rodríguez L (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
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontolia Electronica 4:1–9
Ishimaru Y, Suzuki M, Tsukamoto T, Suzuki K, Nakazono M, Kobayashi T, Wada Y, Watanabe S, Matsuhashi S, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2006) Rice plants take up Fe as an Fe3+-phytosiderophore and as Fe2+. Plant J 45:335–346. https://doi.org/10.1111/j.1365-313X.2005.02624.x
Kai M, Piechulla B (2009) Plant growth promotion due to rhizobacterial volatiles—an effect of CO2? FEBS Lett 583:3473–3477. https://doi.org/10.1016/j.febslet.2009.09.053
Khara E, Arora NK (2010) Effect of indole-3-acetic acid (IAA) produced by Pseudomonas aeruginosa in suppression of charcoal rot disease of chickpea. Curr Microbiol 61:64–68. https://doi.org/10.1007/s00284-009-9577-6
Kieu PN, Aznar A, Segond D, Rigault M, Simond-Côte E, Kunz C, Soulie MC, Expert D, Dellagi A (2012) Iron deficiency affects plant defence responses and confers resistance to Dickeya dadantii and Botrytis cinerea. Mol Plant Pathol 13:816–827. https://doi.org/10.1111/j.1364-3703.2012.00790.x
Kobayashi T, Nakanishi Itai R, Senoura T, Oikawa T, Ishimaru Y, Ueda M, Nakanishi H, Nishizawa NK (2016) Jasmonate signaling is activated in the very early stages of iron deficiency responses in rice roots. Plant Mol Biol 91:533–547. https://doi.org/10.1007/s11103-016-0486-3
Koen E, Trapet P, Brulé D, Kulik A, Klinguer A, Atauri-Miranda L, Meunier-Prest R, Boni G, Glauser G, Mauch-Mani B, Wendehenne D, Besson-Bard A (2014) β-aminobutyric acid (BABA)-induced resistance in Arabidopsis thaliana: link with iron homeostasis. Mol Plant Microb Int 27:1226–1240. https://doi.org/10.1094/MPMI-05-14-0142-R
Koike S, Inoue H, Mizuno D, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2004) OsYSL2 is a rice metal-nicotianamine transporter that is regulated by iron and expressed in the phloem. Plant J 39:415–424. https://doi.org/10.1111/j.1365-313X.2004.02146.x
Liu G, Greenshields DL, Sammynaiken R, Hirji RN, Selvaraj G, Wei Y (2007) Targeted alterations in iron homeostasis underlie plant defense responses. J Cell Sci 120:596–605. https://doi.org/10.1242/jcs.001362
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
López A, Ming DS, Towers GN (2002) Antifungal activity of benzoic acid derivatives from Piper lanceaefolium. J Nat Prod 65:62–64. https://doi.org/10.1021/np010410g
Masalha J, Kosegarten H, Elmaci O, Mengel K (2000) The central role of microbial activity for iron acquisition in maize and sunflower. Biol Fertil Soils 30:433–4399. https://doi.org/10.1007/s003740050021
Mathesius U, Mulders S, Gao M, Teplitski M, Caetano-Anollés G, Rolfe BG, Bauer WD (2003) Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Natl Acad Sci USA 100:1444–1449. https://doi.org/10.1073/pnas.262672599
Ohkama-Ohtsu N, Wasaki J (2010) Recent progress in plant nutrition research: cross-talk between nutrients, plant physiology and soil microorganisms. Plant Cell Physiol 51:1255–1264. https://doi.org/10.1093/pcp/pcq095
Orozco-Mosqueda MC, Macías-Rodríguez LI, Santoyo G, Farías-Rodríguez R, Valencia-Cantero E (2013a) Medicago truncatula increases its iron-uptake mechanisms in response to volatile organic compounds produced by Sinorhizobium meliloti. Folia Microbiol 58:579–585. https://doi.org/10.1007/s12223-013-0243-9
Orozco-Mosqueda MC, Velázquez-Becerra C, Macías-Rodríguez LI, Santoyo G, Flores-Cortez I, Alfaro-Cuevas R, Valencia-Cantero E (2013b) Arthrobacter agilis UMCV2 induces iron acquisition in Medicago truncatula (strategy I plant) in vitro via dimethylhexadecylamine emission. Plant Soil 362:51–66. https://doi.org/10.1007/s11104-012-1263-y
Ortiz-Castro R, Díaz-Pérez C, Martínez-Trujillo M, del Río RE, Campos-García J, López-Bucio J (2011) Transkingdom signaling based on bacterial cyclodipeptides with auxin activity in plants. Proc Natl Acad Sci USA 108:7253–7258. https://doi.org/10.1073/pnas.1006740108
Park ES, Moon WS, Song MJ, Kim MN, Chung KH, Yoon JS (2001) Antimicrobial activity of phenol and benzoic acid derivatives. Int Biodeter Biodegr 47:209–214. https://doi.org/10.1016/S0964-8305(01)00058-0
Peña-Uribe CA, García-Pineda E, Beltrán-Peña E, de la Cruz HR (2012) Oligogalacturonides inhibit growth and induce changes in S6K phosphorylation in maize (Zea mays L. var. Chalqueño). Plant Growth Regul 67:151–159. https://doi.org/10.1007/s10725-012-9672-8
Pérez-Flores P, Valencia-Cantero E, Altamirano-Hernandez J, Pelagio-Flores R, López-Bucio J, García-Juárez P, Macías-Rodríguez L (2017) Bacillus methylotrophicus M4-96 isolated from maize (Zea mays) rhizoplane increases growth and auxin content in Arabidopsis thaliana via emission of volatiles. Protoplasma 6:2201–2213. https://doi.org/10.1007/s00709-017-1109-9
Pieterse CM, Zamioudis C, Berendsen RL, Weller DM, Van Wees SC, Bakker PA (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375. https://doi.org/10.1146/annurev-phyto-082712-102340
Radhamani R, Kannan R, Rakkiyappan P (2016) Leaf chlorophyll meter readings as an indicator for sugarcane yield under iron deficient typic haplustert. Sugar Tech 18:61–66. https://doi.org/10.1007/s12355-014-0363-9
Raya-González J, Velázquez-Becerra C, Barrera-Ortiz S, López-Bucio J, Valencia-Cantero E (2017)) N,N-dimethyl hexadecylamine and related amines regulate root morphogenesis via jasmonic acid signalling in Arabidopsis thaliana. Protoplasma 254:1399–1410
Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Paré PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci USA 100:4927–4932. https://doi.org/10.1073/pnas.0730845100
Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Paré PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026. https://doi.org/10.1104/pp.900104
Salzman RA, Brady JA, Finlayson SA, Buchanan CD, Summer EJ, Sun F, Klein PE, Klein RR, Pratt LH, Cordonnier-Pratt MM, Mullet JE (2005) Transcriptional profiling of sorghum induced by methyl jasmonate, salicylic acid, and aminocyclopropane carboxylic acid reveals cooperative regulation and novel gene responses. Plant Physiol 138:352–368. https://doi.org/10.1104/pp.104.058206
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108. https://doi.org/10.1038/nprot.2008.73
Schuhegger R, Ihring A, Gantner S, Bahnweg G, Knappe C, Vogg G, Hutzler P, Schmid M, Van Breusegem F, Eberl L, Hartmann A, Langebartels C (2006) Induction of systemic resistance in tomato by N-acyl-L-homoserine lactone-producing rhizosphere bacteria. Plant Cell Environ 29:909–918. https://doi.org/10.1111/j.1365-3040.2005.01471.x
Sen S, Kundu S, Dutta SK (2016) Proteomic analysis of JAZ interacting proteins under methyl jasmonate treatment in finger millet. Plant Physiol Biochem 108:79–89. https://doi.org/10.1016/j.plaphy.2016.05.033
Shi S, Richardson AE, O’Callaghan M, DeAngelis KM, Jones EE. Stewart A, Firestone MK, Condron LM (2011) Effects of selected root exudate components on soil bacterial communities. FEMS Microbiol Ecol 77:600–610. https://doi.org/10.1111/j.1574-6941.2011.01150.x
Starkey M, Rahme LG (2009) Modeling Pseudomonas aeruginosa pathogenesis in plant hosts. Nat Protoc 4:117–124. https://doi.org/10.1038/nprot.2008.224
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
Tusnady GE, Simon I (2001) The HMMTOP transmembrane topology prediction server. Bioinformatics 17:849–850. https://doi.org/10.1093/bioinformatics/17.9.849
Valencia-Cantero E, Hernández-Calderón E, Velázquez-Becerra C, López-Meza JE, Alfaro-Cuevas R, López-Bucio J (2007) Role of dissimilatory fermentative iron-reducing bacteria in Fe uptake by common bean (Phaseolus vulgaris L.) plants grown in alkaline soil. Plant Soil 291:263–273. https://doi.org/10.1007/s11104-007-9191-y
Velázquez-Becerra C, Macías-Rodríguez LI, López-Bucio J, Altamirano-Hernández J, Flores-Cortez I, Valencia-Cantero E (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
Vert G, Grotz N, Dédaldéchamp F, Gaymard F, Guerinot ML, Briat JF, Curie C (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14:1223–1233. https://doi.org/10.1105/tpc.001388
Weisskopf L, Le Bayon RC, Kohler F, Page V, Jossi M, Gobat JM, Aragno M (2008) Spatio-temporal dynamics of bacterial communities associated with two plant species differing in organic acid secretion: a one-year microcosm study on lupin and wheat. Soil Biol Biochem 40:1772–1780. https://doi.org/10.1016/j.soilbio.2008.02.018
Wildermuth MC (2006) Variations on a theme: synthesis and modification of plant benzoic acids. Curr Opin Plant Biol 9:288–296. https://doi.org/10.1016/j.pbi.2006.03.006
Yuan J, Zhang N, Huang Q, Raza W, Li R, Vivanco JM, Shen Q (2015) Organic acids from root exudates of banana help root colonization of PGPR strain Bacillus amyloliquefaciens. NJN-6. Sci Rep 5:13438. https://doi.org/10.1038/srep13438
Zamioudis C, Korteland J, Van Pelt JA, Hamersveld M, Dombrowski N, Bai Y, Hanson J, Van Verk MC, Ling HQ, Schulze-Lefert P, Pieterse CM (2015) Rhizobacterial volatiles and photosynthesis-related signals coordinate MYB72 expression in Arabidopsis roots during onset of induced systemic resistance and iron-deficiency responses. Plant J 84:309–322. https://doi.org/10.1111/tpj.12995
Zhang H, Kim MS, Krishnamachari V, Payton P, Sun Y, Grimson M, Farag MA, Ryu CM, Allen R, Melo IS, Paré PW (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
Zhang H, Sun Y, Xie X, Kim MS, Dowd SE, Paré PW (2009) A soil bacterium regulates plant acquisition of iron via deficiency-inducible mechanisms. Plant J 58:568–577. https://doi.org/10.1111/j.1365-313X.2009.03803.x
ZhongQun H, Junan Z, HaoRu T, Zhi H (2012) Different vegetables crops in response to allelopathic of hot pepper root exudates. World Appl Sci J 19:1289–1294. https://doi.org/10.5829/idosi.wasj.2012.19.09.1886
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We thank the Coordinación de la Investigación Científica UMSNH (México, grant 2.22) for providing financial support.
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EHC: data collection, data analysis and interpretation, drafting the article; MEAG: data collection; DYCR: data collection; LMR: data collection, data analysis and interpretation; VMR: data collection; GS: data analysis and interpretation; JLB: data analysis and interpretation, Drafting the article and EVC: conception or design of the work, data analysis and interpretation, final approval of the version to be published.
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Erasto Hernández-Calderón and Maria Elizabeth Aviles-Garcia have contributed equally to this work.
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Hernández-Calderón, E., Aviles-Garcia, M.E., Castulo-Rubio, D.Y. et al. 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 (2018). https://doi.org/10.1007/s11103-017-0694-5
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DOI: https://doi.org/10.1007/s11103-017-0694-5
Keywords
- Rhizhosphere
- Root exudates
- Volatile compounds
- Plant defense
- Jasmonic acid