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PLOS ONE  2013 

Activation of the Jasmonic Acid Plant Defence Pathway Alters the Composition of Rhizosphere Bacterial Communities

DOI: 10.1371/journal.pone.0056457

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Jasmonic acid (JA) signalling plays a central role in plant defences against necrotrophic pathogens and herbivorous insects, which afflict both roots and shoots. This pathway is also activated following the interaction with beneficial microbes that may lead to induced systemic resistance. Activation of the JA signalling pathway via application of methyl jasmonate (MeJA) alters the composition of carbon containing compounds released by roots, which are implicated as key determinants of rhizosphere microbial community structure. In this study, we investigated the influence of the JA defence signalling pathway activation in Arabidopsis thaliana on the structure of associated rhizosphere bacterial communities using 16S rRNA gene amplicon pyrosequencing. Application of MeJA did not directly influence bulk soil microbial communities but significant changes in rhizosphere community composition were observed upon activation of the jasmonate signalling pathway. Our results suggest that JA signalling may mediate plant-bacteria interactions in the soil upon necrotrophic pathogen and herbivorous insect attacks.


[1]  Kazan K, Manners JM (2008) Jasmonate signaling: Toward an integrated view. Plant Physiol 146: 1459–1468.
[2]  Laluk K, Mengiste T (2010) Necrotroph attacks on plants: wanton destruction or covert extortion? Arabidopsis Book 8: e0136.
[3]  Van Wees SCM, Van der Ent S, Pieterse CMJ (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11: 443–448.
[4]  McConn M, Creelman RA, Bell E, Mullet JE, Browse J (1997) Jasmonate is essential for insect defense in Arabidopsis. P Natl Acad Sci USA 94: 5473–5477.
[5]  Puthoff DP, Smigocki AC (2007) Insect feeding-induced differential expression of Beta vulgaris root genes and their regulation by defense-associated signals. Plant Cell Rep 26: 71–84.
[6]  Badri DV, Loyola-Vargas VM, Du J, Stermitz FR, Broeckling CD, Iglesias-Andreu L, et al. (2008) Transcriptome analysis of Arabidopsis roots treated with signaling compounds: a focus on signal transduction, metabolic regulation and secretion. New Phytol 179: 209–223.
[7]  Buer CS, Imin N, Djordjevic MA (2010) Flavonoids: New roles for old molecules. J Integr Plant Biol 52: 98–111.
[8]  Faure D, Vereecke D, Leveau JHJ (2009) Molecular communication in the rhizosphere. Plant Soil 321: 279–303.
[9]  Hassan S, Mathesius U (2012) The role of plant flavonoids in root-rhizosphere signalling: opportunities and challenges for improving plant-microbe interactions. J Exp Bot 63: 3429–3444.
[10]  Dennis PG, Miller AJ, Hirsch PR (2010) Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiol Ecol 72: 313–327.
[11]  Doornbos RF, Geraats BPJ, Kuramae EE, Van Loon LC, Bakker PAHM (2011) Effects of jasmonic acid, ethylene, and salicylic acid signaling on the rhizosphere bacterial community of Arabidopsis thaliana. Mol Plant Microb Interact 24: 395–407.
[12]  Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, et al. (2012) Defining the core of Arabidopsis thaliana root microbiome. Nature 488: 86–90.
[13]  Bulgarelli D, Rott M, Schlaeppi K, Ver Loren van Themaat E, Ahmadinejad N, et al. (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488: 91–95.
[14]  Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, et al. (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci U S A 97: 11655–11660.
[15]  Campbell EJ, Schenk PM, Kazan K, Penninckx IAMA, Anderson JP, Maclean DJ, et al. (2003) Pathogen-responsive expression of a putative ATP-binding cassette transporter gene conferring resistance to the diterpenoid sclareol is regulated by multiple defense signaling pathways in Arabidopsis. Plant Physiol 133: 1272–1284.
[16]  Dennis PG, Guo K, Imelfort M, Jensen P, Tyson GW, Rabaey K (2013) Spatial uniformity of microbial diversity in a continuous bioelectrochemical system. Bioresource Technol In press.
[17]  Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman F D, et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7: 335–336.
[18]  Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improved sensitivity and speed of chimera detection. Bioinformatics 27: 2194–2200.
[19]  Bragg L, Stone G, Imelfort M, Hugenholtz P, Tyson GW (2012) Fast, accurate error-correction of amplicon pyrosequences using Acacia. Nat Methods 9: 425–426.
[20]  Simpson EH (1949) Measurement of species diversity. Nature 163: 688.
[21]  Legendre P, Gallagher E (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129: 271–280.
[22]  Zou CS, Mo MH, Gu YQ, Zhou JP, Zhang KQ (2007) Possible contributions of volatile-producing bacteria to soil fungistasis. Soil Biol Biochem 39: 2371–2379.
[23]  Bravo A, Likitvivatanavong S, Gill SS, Soberon M (2011) Bacillus thuringiensis: A story of a successful bioinsecticide. Insect Biochem Molec 41: 423–431.
[24]  Raymond B, Johnston PR, Nielsen-LeRoux C, Lereclus D, Crickmore N (2010) Bacillus thuringiensis: an impotent pathogen? Trends Microbiol 18: 189–194.
[25]  Yu X, Liu T, Liang X, Tang C, Zhu J, Wang S, et al. (2011) Rapid detection of vip1-type genes from Bacillus cereus and characterization of a novel vip binary toxin gene. FEMS Microbiol Lett 325: 30–36.
[26]  Validov S, Kamilova F, Qi S, Stephan D, Wang JJ, Makarova N, et al. (2007) Selection of bacteria able to control Fusarium oxysporum f. sp radicis-lycopersici in stonewool substrate. J Appl Microbiol 102: 461–471.
[27]  Tjamos SE, Flemetakis E, Paplomatas EJ, Katinakis P (2005) Induction of resistance to Verticillium dahliae in Arabidopsis thaliana by the biocontrol agent K-165 and pathogenesis-related proteins gene expression. Mol Plant Microbe Interact 18: 555–561.
[28]  Berry C (2012) The bacterium, Lysinibacillus sphaericus, as an insect pathogen. J Invertebr Pathol 109: 1–10.
[29]  Hu X, Fan W, Han B, Liu H, Zheng D, Li Q, et al. (2008) Complete genome sequence of the mosquitocidal bacterium Bacillus sphaericus C3-41 and comparison with those of closely related Bacillus species. J Bacteriol 190: 2892–2902.
[30]  Rasmann S, Agrawal AA (2008) In defense of roots: A research agenda for studying plant resistance to belowground herbivory. Plant Physiol 146: 875–880.
[31]  van Frankenhuyzen K (2009) Insecticidal activity of Bacillus thuringiensis crystal proteins. J Invertebr Pathol 101: 1–16.
[32]  Abou-Shanab RAI, van Berkum P, Angle JS (2007) Heavy metal resistance and genotypic analysis of metal resistance genes in gram-positive and gram-negative bacteria present in Ni-rich serpentine soil and in the rhizosphere of Alyssum murale. Chemosphere 68: 360–367.
[33]  Yadav S, Kaushik R, Saxena AK, Arora DK (2011) Diversity and phylogeny of plant growth-promoting bacilli from moderately acidic soil. J Basic Microb 51: 98–106.
[34]  Naz I, Bano A (2010) Biochemical, molecular characterization and growth promoting effects of phosphate solubilizing Pseudomonas sp. isolated from weeds grown in salt range of Pakistan. Plant Soil 334: 199–207.
[35]  Sgroy V, Cassan F, Masciarelli O, Del Papa MF, Lagares A, Luna V (2009) Isolation and characterization of endophytic plant growth-promoting (PGPB) or stress homeostasis-regulating (PSHB) bacteria associated to the halophyte Prosopis strombulifera. Appl Microbiol Biot 85: 371–381.
[36]  Stearns JC, Woody OZ, McConkey BJ, Glick BR (2012) Effects of bacterial ACC deaminase on Brassica napus gene expression. Mol Plant Microbe Interact 25: 668–676.
[37]  Viruel E, Lucca ME, Sineriz F (2011) Plant growth promotion traits of phosphobacteria isolated from Puna, Argentina. Arch Microbiol 193: 489–496.
[38]  Achouak W, Normand P, Heulin T (1999) Comparative phylogeny of rrs and nifH genes in the Bacillaceae. Int J Syst Bacteriol 49: 961–967.
[39]  Jin HJ, Tu R, Xu F, Chen SF (2011) Identification of nitrogen-fixing Paenibacillus from different plant rhizospheres and a novel nifH gene detected in the P. stellifer. Microbiology 80: 117–124.
[40]  Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63: 541–556.
[41]  Hein JW, Wolfe GV, Blee KA (2008) Comparison of rhizosphere bacterial communities in Arabidopsis thaliana mutants for systemic acquired resistance. Microb Ecol 55: 333–343.
[42]  Carvalhais LC, Dennis PG, Tyson GW, Schenk PM (2012) Application of metatranscriptomics to soil environments. J Microbiol Methods 91: 246–251.
[43]  Bryant JP, Kuropat PJ, Cooper SM, Frisby K, Owensmith N (1989) Resource availability hypothesis of plant antiherbivore defense tested in a South-African Savanna ecosystem. Nature 340: 227–229.
[44]  Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230: 895–899.


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