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Journal of Plant Growth Regulation

, Volume 37, Issue 3, pp 859–866 | Cite as

Effect of Azospirillum brasilense Sp245 Lipopolysaccharides on Wheat Plant Development

  • Estefanía Chávez-Herrera
  • Alma Alejandra Hernández-Esquivel
  • Elda Castro-Mercado
  • Ernesto García-PinedaEmail author
Article
  • 262 Downloads

Abstract

Lipopolysaccharides (LPS) are integral and essential constituents of the outer membranes of Gram-negative bacteria that have been extensively investigated in relation to the activation of plant defense responses. In the present study, we evaluated the effect of exogenously applied Azospirillum brasilense LPS on wheat plant development, including plant aging, spike formation and size, as well as grain yield and grain chemical composition. Experiments were performed in plants cultivated in pots under greenhouse conditions. Plants were sprayed with two LPS concentrations (2 and 5 µg/mL) once a week over 3 months. LPS administration increased leaf length, especially the second leaf. Although spike formation was accelerated, spike length was reduced compared to untreated controls, and both responses were dependent on LPS concentration. Plant aging was also accelerated, and the dry weight of plants increased when treated with 5 µg/mL LPS. Moreover, the impact of exogenous LPS treatment on the protein, starch, and lipid content in grains was relatively negligible. Our results showed that A. brasilense LPS affected some aspects of wheat development such as plant aging and spike formation, but not grain chemical composition or grain yield.

Keywords

Lipoplysaccharides Wheat Azospirillum brasilense Spike Rhizobacteria 

Notes

Acknowledgements

This study was supported by the Coordinación de la Investigación Científica, Universidad Michoacana de San Nicolás de Hidalgo, México.

References

  1. Baldani VLD, Alvarez MDB, Baldani JI, Dobereiner J (1986) Establishment of inoculated Azospirillum spp. in the rhizosphere and in roots of field grown wheat and sorghum. Plant Soil 90:35–46CrossRefGoogle Scholar
  2. Balsanelli E, Serrato RV, Baura VA, Sassaki G, Yates MG, Rigo LU, Pedrosa FO, Souza EM, Monteiro RA (2010) Herbaspirillum seropedicae rfbB and rfbC genes are required for maize colonization. Environ Microbiol 12:2233–2244PubMedGoogle Scholar
  3. Bashan Y, Holguin G, de-Bashan LE (2004) Azospirillum-plant relationships: physiological, molecular, agricultural, and environmental advances (1997–2003). Can J Microbiol 50:521–577CrossRefPubMedGoogle Scholar
  4. Bashan Y, Levanony H, Klein E (1986) Evidence for a weak active external adsorption of Azospirillum brasilense Cd to wheat roots. J Gen Microbiol 132:3069–3073Google Scholar
  5. Beets C, Huang J-C, Madala NE, Dubery IA (2012) Biosynthesis of camalexin in Arabidopsis thaliana in response to lipopolysaccharide elicitation: a gene-to-metabolite study. Planta 236:261–272CrossRefPubMedGoogle Scholar
  6. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein using the principles of protein dye-binding. Anal Biochem 72:248–254CrossRefPubMedPubMedCentralGoogle Scholar
  7. Choudhary DK, Sharma KP, Gaur RK (2011) Biotechnological perspectives of microbes in agro-ecosystems. Biotechnol Lett 33:1905–1910CrossRefPubMedGoogle Scholar
  8. Coventry HS, Dubery IA (2001) Lipopolysaccharides from Burkholderia cepacia contribute to an enhanced defensive capacity and the induction of pathogenesis-related proteins in Nicotiana tabacum. Physiol Mol Plant Pathol 58:149–158CrossRefGoogle Scholar
  9. De Weger LA, Bakker PAHM., Schippers B, van Loosdrecht MCM, Lugtenberg BJJ (1989) Pseudomonas spp. with mutational changes in the O-antigenic side chain of their lipopolysaccharide are affected in their ability to colonize potato roots. In: Lugtenberg BJJ (ed) Signal molecules in plants and plant-microbe interactions. Springer, Heidelberg, pp 197–202CrossRefGoogle Scholar
  10. Dey R, Pal KK, Bhatt DM, Chauhan SM (2004) Growth promotion and yield enhancement of peanut (Arachis hypogeal L.) by application of plant growth-promoting rhizobacteria. Microbiol Res 159:371–394CrossRefPubMedGoogle Scholar
  11. Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149CrossRefGoogle Scholar
  12. du Jardin P (2015) Plant biostimulants: definition, concept, main categories and regulation. Sci Hort 196:3–14CrossRefGoogle Scholar
  13. Duijff BJ, Gianinazzi-Pearson V, Lemanceau P (1997) Involvement of the outer membrane lipopolysaccharides in the endophytic colonization of tomato roots by biocontrol Pseudomonas fluorescens strain WCS417r. New Phytol 135:325–334CrossRefGoogle Scholar
  14. Eckert B, Weber OB, Kirchhof G, Halbritter A, Stoffels M, Hartmann A (2001) Azospirillum doebereinerae sp. nov., a nitrogen-fixing bacterium associated with the C4-grass Miscanthus. Int J Syst Evol Microbiol 51:17–26CrossRefPubMedGoogle Scholar
  15. Fibach-Paldi S, Burdman S, Okon Y (2012) Key physiological properties contributing to rhizosphere adaptation and plant growth promotion abilities of Azospirillum brasilense. FEMS Microbiol Lett 326:99–108CrossRefPubMedGoogle Scholar
  16. Finnegan T, Steenkamp PA, Piater LA, Dubery IA (2016) The lipopolysaccharide-induced metabolome signature in Arabidopsis thaliana reveals dynamic reprogramming of phytoalexin and phytoanticipin pathways. PLoS ONE 11(9):e0163572CrossRefPubMedPubMedCentralGoogle Scholar
  17. Fomsgaard A, Freudenberg MA, Galanos C (1990) Modification of the silver staining technique to detect lipopolysaccharide in polyacrylamide gels. J Clin Microbiol 28:2627–2631PubMedPubMedCentralGoogle Scholar
  18. Fu ZQ, Dong X (2013) Systemic acquired resistance: turning local infection into global defence. Annu Rev Plant Biol 64:839–863CrossRefPubMedGoogle Scholar
  19. García-Fraile P, Menéndez E, Rivas R (2015) Role of bacterial biofertilizers in agriculture and forestry. AIMS Bioeng 2:183–205CrossRefGoogle Scholar
  20. Gozzo F, Faoro F (2013) Systemic acquired resistance (50 Years after discovery): moving from the lab to the field. J Agric Food Chem 61:12473–12491CrossRefPubMedGoogle Scholar
  21. Hol WHG, Bezemer TM, Biere A (2013) Getting the ecology into interactions between plants and the plant growth-promoting bacterium Pseudomonas fluorescens. Front Plant Sci 4:81CrossRefPubMedPubMedCentralGoogle Scholar
  22. Janeczko A, Biesaga-Koscielniak J, Oklestkova J, Filek M, Dziurka M, Szarek-Lukaszewska G, Koscielniak J (2010) Role of 24-epibrassinolide in wheat production: physiological effects and uptake. J Agr Crop Science 196:311–321Google Scholar
  23. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685CrossRefPubMedGoogle Scholar
  24. Madala NE, Molinaro A, Dubery IA (2012) Distinct carbohydrate and lipid-based molecular patterns within lipopolysaccharides from Burkholderia cepacia contribute to defence-associated differential gene expression in Arabidopsis thaliana. Innate Immun 18:140–154CrossRefPubMedGoogle Scholar
  25. Mishina TE, Zeier J (2007) Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. Plant J 50:500–513CrossRefPubMedGoogle Scholar
  26. Newman MA, Dow JM, Molinaro A, Parrilli M (2007) Priming, induction and modulation of plant defence responses by bacterial lipopolysaccharides. J Endotoxin Res 13:69–84CrossRefPubMedGoogle Scholar
  27. Newman MA, Sundelin T, Nielsen JT, Erbs G (2013) MAMP (microbe-associated molecular pattern) triggered immunity in plants. Front Plant Sci 4:1–14CrossRefGoogle Scholar
  28. Niu L, Liao W (2016) Hydrogen peroxide signaling in plant development and abiotic responses: crosstalk with nitric oxide and calcium. Front Plant Sci 7:230.  https://doi.org/10.3389/fpls.2016.00230 PubMedPubMedCentralCrossRefGoogle Scholar
  29. Okon Y, Labandera-Gonzalez CA (1994) Agronomic applications of Azospirillum: an evaluation of 20 years worldwide field inoculation. Soil Biol Biochem 26:1591–1601CrossRefGoogle Scholar
  30. Pel MJC, Pieterse CMJ (2013) Microbial recognition and evasion of host immunity. J Exp Bot 64:1237–1248CrossRefPubMedGoogle Scholar
  31. Pereg GL, Gilchrist K, Kennedy IR (2000) Mutants with enhanced nitrogenase activity in hydroponic Azospirillum brasilense-wheat associations. Appl Environ Microbiol 66:2175–2184CrossRefGoogle Scholar
  32. Pereg L, de-Bashan LE, Bashan Y (2016) Assessment of affinity and specificity of Azospirillum for plants. Plant Soil 399:389–414CrossRefGoogle Scholar
  33. Perrig D, Boiero ML, Masciarelli OA, Penna C, Ruiz OA, Cassán FD, Luna MV (2007) Plant-growth-promoting compounds produced by two agronomically important strains of Azospirillum brasilense, and implications for inoculant formulation. Appl Microbiol Biotechno l75:1143–1150CrossRefGoogle Scholar
  34. Piater LA, Nurnberger T, Dubery IA (2004) Identification of a lipopolysaccharide responsive erk-like MAP kinase in tobacco leaf tissue. Mol Plant Pathol 5:331–341CrossRefPubMedGoogle Scholar
  35. Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, VanWees SCM, Bakker PAHM. (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375CrossRefPubMedGoogle Scholar
  36. Ranf S, Gisch N, Schäffer M, Illig T, Westphal L, Knirel YA, Sánchez-Carballo PM, Zähringer U, Hückelhoven R, Lee J, Scheel D (2015) A lectin S-domain receptor kinase mediates lipopolysaccharide sensing in Arabidopsis thaliana. Nat Immunol 16:426–433CrossRefPubMedGoogle Scholar
  37. Renukadevi KP, Angayarkanni J, Karunakaran G (2012) Extraction and characterization of lipopolysaccharide from Serratia rubidaea and its cytotoxicity on lung cancer cell line-nci-h69. Acta Tech Corviniensis 2:97–101Google Scholar
  38. Sanabria M, van Heerden H, Dubery IA (2012) Molecular characterization and regulation of a nicotiana tabacum s-domain receptor-like kinase gene induced during an early rapid response to lipopolysaccharides. Gene 501:39–48CrossRefPubMedGoogle Scholar
  39. Sant’Anna FH, Almeida LG, Cecagno R, Reolon LA, Siqueira FM, Machado MR, Vasconcelos AT, Schrank IS (2011) Genomic insights into the versatility of the plant growth-promoting bacterium Azospirillum amazonense. BMC Genom 12:409CrossRefGoogle Scholar
  40. Silipo A, Molinaro A, Sturiale L, Dow JM, Erbs G, Lanzetta R, Newman MA, Parrilli M (2005) The elicitation of plant innate immunity by lipooligosaccharide of Xanthomonas campestri. J Biol Chem 280:33660–33668CrossRefPubMedGoogle Scholar
  41. Tadra-Sfeir MZ, Souza EM, Faoro H, Műller-Santos M, Baura VA, Tuleski TR, Rigo LU, Yates MG, Wassem R, Pedrosa FO, Monteiro RA (2011) Naringenin regulates expression of genes involved in cell wall synthesis in Herbaspirillum seropedicae. Appl Environ Microbiol 77:2180–2183CrossRefPubMedPubMedCentralGoogle Scholar
  42. Takeshita T, Takeda K, Ota S, Yamazaki T, Kawano S (2015) A simple method for measuring the starch and lipid contents in the cell of microalgae. Cytologia 80:475–481CrossRefGoogle Scholar
  43. Trejo A, de-Bashan LE, Hartmann A, Hernandez J-P, Rothballer M, Schmid M, Bashan Y (2012) Recycling waste debris of immobilized microalgae and plant growth-promoting bacteria from wastewater treatment as a resource to improve fertility of eroded desert soil. Environ Exp Bot 75:65–73CrossRefGoogle Scholar
  44. Veresoglou SD, Menexes G (2010) Impact of inoculation with Azospirillum spp. on growth properties and seed yield of wheat: a meta-analysis of studies in the ISI Web of Science from 1981 to 2008. Plant Soil 337:469–480CrossRefGoogle Scholar
  45. Zadoks JC, Changt TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14:415–421CrossRefGoogle Scholar
  46. Zeidler D, Zahringer U, Gerber I, Dubery I, Hartung T, Bors W, Hutzler HH, Durner J (2004) Innate immunity in Arabidopsis thaliana: lipopolysaccharides activate nitric oxide synthase (NOS) and induce defence genes. Proc Natl Acad Sci USA 101:15811–15816CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Instituto de Investigaciones Químico BiológicasUniversidad Michoacana de San Nicolás de HidalgoMoreliaMexico

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