Abstract
It is known that plant and associated bacteria coevolved, but just now the roles of chemical signaling compounds in these intricate relationships have been systematically studied. Many Gram-negative bacteria produce N-acyl-L-homoserine lactones (AHL), chemical signals used in quorum-sensing bacterial communications mechanisms. In recent years, it has been shown that these compounds may also influence the development of plants, acting as allelochemicals, in still not well understood eukaryot-prokaryot interactions. In the present work, a quorum-sensing molecule produced by the tomato associated bacterium Pseudomonas sp. was characterized and its effects on germination and growth of tomato seedlings were accessed. The chemical study of the bacterium extract led to the identification of N-3-oxo-dodecanoyl-L-homoserine lactone (1), using gas chromatography coupled to electron impact mass spectrometry (GC-MS), and ultra-high resolution Qq-time-of-flight mass spectrometry (UHR-QqTOF-MS) equipped with an electrospray ionization source (ESI). The synthetic compound was tested at different concentrations in tomato to evaluate its effects on seed germination and seedlings root growth. Inhibition of tomato seed germination and root growth were observed in the presence of micromolar concentrations of the compound 1. Scanning electron microscopy evidenced morphological alterations on roots in the presence of the compound, with reduction of growth, impaired root hairs development and cracks in the rhizodermis.
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References
Arevalo-Ferro C, Reil G, Görg A, Eberl L, Riedel K (2005) Biofilm formation of Pseudomonas putida IsoF: the role of quorum sensing as assessed by proteomics. Syst Appl Microbiol 28(2):87–114. https://doi.org/10.1016/j.syapm.2004.10.005
Babalola OO (2010) Beneficial bacteria of agricultural importance. Biotechnol Lett 32:1559–1570. https://doi.org/10.1007/s10529-010-0347-0
Bai X, Todd CD, Desikan R, Yongping Y, Hu X (2012) N-3-oxo-decanoyl-L-homoserine-lactone activates auxin-induced adventitious root formation via hydrogen peroxide- and nitric oxide-dependent cyclic GMP signaling in mung bean. Plant Physiol 158:725–736. https://doi.org/10.1104/pp.111.185769
Bloemberg GV, Lugtenberg BJJ (2001) Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr Opin Plant Biol 4:343–350
Botelho GR, Mendonça-Hagler LC (2006) Fluorescent pseudomonads associated with the rhizosphere of crops - an overview. Braz J Microbiol 3:401–416. https://doi.org/10.1590/S1517-83822006000400001
Castro-Ortíz R, Trujillo-Martínez M, Bucio-López J (2008) N-acyl-L-homoserine lactones: a class of bacterial quorum sensing signals alter post-embryonic root development in Arabidopsis thaliana plant. Plant Cell Environ 31:1497–1509
Cataldi TRI, Bianco G, Abate S (2009) Accurate mass analysis of -acyl-homoserine-lactones and cognate lactone-opened compounds in bacterial isolates of PAO1 by LC-ESI-LTQ-FTICR-MS. Int J Mass Spectrom 44(2):182–192
Cataldi TRI, Bianco G, Frommberger M, Schmitt-Kopplin P (2004) Direct analysis of selected N-acyl-L-homoserine lactones by gas chromatography/mass spectrometry. Rapid Commun Mass Spectrom 18(12):1341–1344. https://doi.org/10.1002/rcm.1480
Cha C, Gao P, Chen YC, Shaw PD, Farrand SK (1998) Production of acyl-homoserine lactone quorum sensing signals by gram-negative plant-associated bacteria. Mol Plant-Microbe Interact 11:1119–1129
Delatorre CA, Silva AA (2008) Arabidopsis thaliana: a small plant a big role. Rev Ciên Agrár 31:58–67
de Salamone IG, Hynes RK, Nelson LM (2001) Cytokinin production by plant growth promoting rhizobacteria and selected mutants. Can J Microbiol 47:404–411. https://doi.org/10.1139/cjm-47-5-404
Federle MJ, Bassler BL (2003) Interspecies communication in bacteria. J Clin Invest 112:1291–1298
Ferreira AG, Borghetti F (2004) Germinação: do básico ao aplicado. Porto Alegre, Artmed
Gomila M, Peña A, Mulet M, Lalucat J, GarcÃa-Valdés E (2015) Phylogenomics and systematics in Pseudomonas. Front Microbiol 6. https://doi.org/10.3389/fmicb.2015.00214
Hartmann A, Schikora A (2012) Quorum sensing of bacteria and trans-Kingdom interactions of N-Acyl homoserine lactones with eukaryotes. J Chem Ecol 38(6):704–713
Joseph C, Phillips D (2003) Metabolites from soil bacteria affect plant water relations. Plant Physiol Biochem 41:189–192
Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–132
Laue BE, Jiang Y, Chhabra SR, Jacob S, Stewart GS, Hardman A, Downie JA, O'Gara F, Williams P (2000) The biocontrol strain Pseudomonas fluorescens F113 produces the Rhizobium small bacteriocin, N-(3-hydroxy-7-cis-tetradecenoyl)homoserine lactone, via HdtS, a putative novel N-acylhomoserine lactone synthase. Microbiology 146:2469–2480. https://doi.org/10.1099/00221287-146-10-2469
Lee J, Zhang L (2015) The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein Cell 6(1):26–41. https://doi.org/10.1007/s13238-014-0100-x
Loh J, Pierson EA, Pierson LS III, Stacey G, Chatterjee A (2002) Quorum sensing in plant associated bacteria. Curr Op Plant Biol 5(4):285–290. https://doi.org/10.1016/S1369-5266(02)00274-1
Maguire JD (1962) Speed of germination-aid in selection and evaluation for seedling emergence and vigor. Crop Science, Madison 2:176–177. https://doi.org/10.2135/cropsci1962.0011183X000200020033x
Olher VG, Ferreira NP, Souza AG, Chiavelli LUR, Teixeira AF, Santos WD, Santin SM, Ferrarese Filho O, Silva CC, Pomini AM (2016) Acyl-homoserine lactone from Saccharum × officinarum with stereochemistry-dependent growth regulatory activity. J Nat Prod 79(5):1316–1321. https://doi.org/10.1021/acs.jnatprod.5b01075
Oliveira ALM, Santos OJAP, Marcelino PRF, Milani KML, Zuluaga MYA, Zucareli C, Gonçalves LSA (2017) Maize inoculation with Azospirillum brasillense Ab-V5 cells enriched with exopolysaccharides and polyhydroxybutyrate results in high productivity under low N fertilizer input. Front Microbiol 8:1837
Palmer AG, Senechal AC, Mukherjee A, Ané JM, Blackwell HE (2014) Plant responses to bacterial N-acyl-L-homoserine lactones are dependent on enzymatic degradation to L-homoserine. ACS Chem Biol 9:1834–1845. https://doi.org/10.1021/cb500191a
Palmer AG, Mukherjee A, Stacy DM, Lazar S, Ané JM, Blackwell HE (2016) Interkingdom responses to bacterial quorum sensing signals regulate frequency and rate of nodulation in legume-rhizobia symbiosis. Chembiochem 17:2199–2205
Scagliola M, Pii Y, Mimmo T, Cesco S, Ricciuti P, Crecchio C (2016) Characterization of plant growth promoting traits of bacterial isolates from the rhizosphere of barley (Hordeum vulgare L.) and tomato (Solanum lycopersicon L.) grown under Fe sufficiency and deficiency. Plant Physiol Biochem 107:187–196. https://doi.org/10.1016/j.plaphy.2016.06.002
Schenk ST, Schikora A (2015) AHL-priming functions via oxylipin and salicylic acid. Front Plant Sci 5. https://doi.org/10.3389/fpls.2014.00784
Schenk ST, Stein E, Kogel KH, Schikora A (2012) Arabidopsis growth and defense are modulated by bacterial quorum sensing molecules. Plant Signal Behav 7:178–181. https://doi.org/10.4161/psb.18789
Schenk ST, Hernandez-Reyes C, Samans B, Stein E, Neumann C, Schikora M, Reichelt M, Mithöfer A, Becker A, Kogel K, Schikora A (2014) N-acyl-homoserine lactone primes plants for cell wall reinforcement and induces resistance to bacterial pathogens via the salicylic acid/oxylipin pathway. Plant Cell 26:2708–2723. https://doi.org/10.1105/tpc.114.126763
Schikora A, Schenk ST, Stein E, Molitor A, Zuccaro A, Kogel KH (2011) N-acyl-homoserine lactone confers resistance towards biotrophic and hemibiotrophic pathogens via altered activation of AtMPK6. Plant Physiol 157:1407–1418. https://doi.org/10.1104/pp.111.180604
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
Veliz-Vallejos DF, van Noorden GE, Yuan M, Mathesius U (2014) A Sinorhizobium meliloti-specific N-acyl homoserine lactone quorum-sensing signal increases nodule numbers in Medicago truncatula independent of autoregulation. Front Plant Sci 5:551–564. https://doi.org/10.3389/fpls.2014.00551
Von Rad UV, Klein I, Kottova J, Zazimalova E, Fekete A, Hartmann A, Opplin-Schimitt P, Durner J (2008) Response of Arabidopsis thaliana to N-hexanoyl-DL-homoserine-lactone, a bacterial quorum sensing molecule produced in the rhizosphere. Planta 229:73–85
Wei H-L, Zhang L-Q (2006) Quorum-sensing system influences root colonization and biological control ability in Pseudomonas fluorescens 2P24. Antonie Van Leeuwenhoek 89(2):267–280
Whitehead NA, Barnard AML, Slater H, Simpson NJL, Salmond GPC (2001) Quorum sensing in gram negative bacteria. FEMS Microbiol Rev 25:365–404
Wood DW, Pierson LS III (1996) The PhI gene of Pseudomonas aureofaciens 30-84 is responsible for the production of a diffusible signal required for phenazine antibiotic production. Gene 168:49–53
Xu Q, Adyatni I, Reuhs B (2018) Effect of processing methods on the quality of tomato products. Food Nutr Sci 9:86–98. https://doi.org/10.4236/fns.2018.92007
Zhang Z, Pierson LS (2001) A second quorum-sensing system regulates cell surface properties but not phenazine antibiotic production inPseudomonas aureofaciens. Appl Environ Microbiol 67(9):4305–4315
Zhang F, Shen J, Zhang J, Zuo Y, Li L, Chen X (2010) Rhizosphere processes and management for improving nutrient use efficiency and crop productivity: implications for China. Adv Agron 107:1–32. https://doi.org/10.1016/S0065-2113(10)07001-X
Zuluaga MYA (2016) Caracterização bioquímica e molecular de bactérias diazotróficas isoladas de tomate (Solanum lycopersicum) e lulo (Solanum quitoense): influência do efeito rizosfera. Dissertation Master’s Degree in Biotechnology. State University of Londrina, Londrina, Paraná, Brazil. (http://www.bibliotecadigital.uel.br/document/?code=vtls000210152).
Acknowledgements
This work was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenadoria de Aperfeiçoamento de Pessoal de Nível Superior (Capes), and Fundação Araucária de Apoio ao Desenvolvimento Científico e Tecnológico do Paraná (1.094.4056; conv. 02/2017).
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Ferreira, N.P., Ximenez, G.R., Chiavelli, L.U.R. et al. Acyl-Homoserine Lactone from Plant-Associated Pseudomonas sp. Influences Solanum lycopersicum Germination and Root Growth. J Chem Ecol 46, 699–706 (2020). https://doi.org/10.1007/s10886-020-01186-2
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DOI: https://doi.org/10.1007/s10886-020-01186-2