J.M. Raaijmakers

Leiden University, Leyden, South Holland, Netherlands

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Publications (197)496.05 Total impact

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    ABSTRACT: The rhizosphere microbiome offers a range of ecosystem services to the plant, including nutrient acquisition and tolerance to (a)biotic stress. Here, analysing the data by Mendes et al. (2011), we show that short heat disturbances (50 or 80 °C, 1 h) of a soil suppressive to the root pathogenic fungus Rhizoctonia solani caused significant increase in alpha diversity of the rhizobacterial community and led to partial or complete loss of disease protection. A reassembly model is proposed where bacterial families that are heat tolerant and have high growth rates significantly increase in relative abundance after heat disturbance, while temperature-sensitive and slow-growing bacteria have a disadvantage. The results also pointed to a potential role of slow-growing, heat-tolerant bacterial families from Actinobacteria and Acidobacteria phyla in plant disease protection. In conclusion, short heat disturbance of soil results in rearrangement of rhizobacterial communities and this is correlated with changes in the ecosystem service disease suppression.
    No preview · Article · Feb 2016 · Ecology Letters
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    Yiying Liu · Christin Zachow · Jos Raaijmakers · Irene de Bruijn

    Preview · Article · Jan 2016 · International Journal of Molecular Sciences
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    ABSTRACT: Grasslands are an important source of biodiversity, providing a range of essential ecosystem services such as ensuring water quality and soil carbon storage. An increasing proportion of grasslands are used for pastoral agriculture, supporting production of domestic livestock. Pasture productivity is significantly affected by soil-borne microbial pathogens. Reducing the impact of soil-borne diseases in pastures is challenging given the complexity of interactions within the soil/rhizosphere microbiome and the diverse impacts of vegetation, land management, soil conditions and climate. Furthermore, there are fewer opportunities to control plant pathogens in pastures compared to arable cropping systems. The greater diversity of vegetation leads to the development of more diverse and less well characterized pathogen complexes, and the application of agrochemicals for control of soil-borne diseases is economically prohibitive and ecologically undesirable. Soil-borne plant pathogens can be suppressed through the general activity of the total soil microbiota acting in competition with the pathogenic microbiota, or by increases in the abundance and activity of specific microbes or microbial consortia that are antagonistic against selected pathogens. The development of strategies that enhance disease suppressiveness in pastures will depend not only on phylogenetic assessment of microbial communities, but also on a mechanistic understanding of the functional potential and properties (i.e. disease suppressive traits) of the soil microbiome. Collectively, this fundamental knowledge will be essential to identify the factors driving the emergence of desired disease suppressive microorganisms and traits. To understand and predict disease suppressive functionality, the spatial and temporal variability of the soil and plant-associated microbial populations and their activities must be taken into account. A systems-based approach is therefore required to identify the obstacles and opportunities related to controlling plant pathogens in pasture systems. Such an integrated approach should incorporate a “microbial” perspective to examine traits, drivers and activities of soil-borne microbes, while utilizing emerging tools in ecological genomics, as well as computational, statistical and modelling approaches that also accommodate the chemical and physical complexity of soil ecosystems.
    No preview · Article · Dec 2015 · Soil Biology and Biochemistry
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    ABSTRACT: Background Lysobacter species are Gram-negative bacteria widely distributed in soil, plant and freshwater habitats. Lysobacter owes its name to the lytic effects on other microorganisms. To better understand their ecology and interactions with other (micro)organisms, five Lysobacter strains representing the four species L. enzymogenes, L. capsici, L. gummosus and L. antibioticus were subjected to genomics and metabolomics analyses. Results Comparative genomics revealed a diverse genome content among the Lysobacter species with a core genome of 2,891 and a pangenome of 10,028 coding sequences. Genes encoding type I, II, III, IV, V secretion systems and type IV pili were highly conserved in all five genomes, whereas type VI secretion systems were only found in L. enzymogenes and L. gummosus. Genes encoding components of the flagellar apparatus were absent in the two sequenced L. antibioticus strains. The genomes contained a large number of genes encoding extracellular enzymes including chitinases, glucanases and peptidases. Various nonribosomal peptide synthase (NRPS) and polyketide synthase (PKS) gene clusters encoding putative bioactive metabolites were identified but only few of these clusters were shared between the different species. Metabolic profiling by imaging mass spectrometry complemented, in part, the in silico genome analyses and allowed visualisation of the spatial distribution patterns of several secondary metabolites produced by or induced in Lysobacter species during interactions with the soil-borne fungus Rhizoctonia solani. Conclusions Our work shows that mining the genomes of Lysobacter species in combination with metabolic profiling provides novel insights into the genomic and metabolic potential of this widely distributed but understudied and versatile bacterial genus. Electronic supplementary material The online version of this article (doi:10.1186/s12864-015-2191-z) contains supplementary material, which is available to authorized users.
    Full-text · Article · Dec 2015 · BMC Genomics
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    ABSTRACT: Lipopeptides (LP) are structurally diverse compounds with potent surfactant and broad-spectrum antibiotic activities. In Pseudomonas and other bacterial genera, LP biosynthesis is governed by large multimodular nonribosomal peptide synthetases (NRPS). To date, relatively little is known about the regulatory genetic network of LP biosynthesis. This study provides evidence that the chaperone ClpA, together with the serine protease ClpP, regulates the biosynthesis of the LP massetolide in Pseudomonas fluorescens SS101. Whole-genome transcriptome analyses of clpA and clpP mutants showed their involvement in the transcription of the NRPS genes massABC and the transcriptional regulator massAR. In addition, transcription of genes associated with cell wall and membrane biogenesis, energy production and conversion, amino acid transport and metabolism, and pilus assembly were altered by mutations in clpA and clpP. Proteome analysis allowed the identification of additional cellular changes associated to clpA and clpP mutations. The expression of proteins of the citrate cycle and the heat shock proteins DnaK and DnaJ were particularly affected. Combined with previous findings, these results suggest that the ClpAP complex regulates massetolide biosynthesis via the pathway-specific, LuxR-type regulator MassAR, the heat shock proteins DnaK and DnaJ, and proteins of the TCA cycle. Combining transcriptome and proteome analyses provided new insights into the regulation of LP biosynthesis in P. fluorescens and led to the identification of specific missing links in the regulatory pathways.
    Full-text · Article · Dec 2015 · BMC Microbiology
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    Ruth Gomez Exposito · Joeke Postma · Jos M. Raaijmakers · Irene De Bruijn
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    ABSTRACT: The genus Lysobacter includes several species that produce a range of extracellular enzymes and other metabolites with activity against bacteria, fungi, oomycetes, and nematodes. Lysobacter species were found to be more abundant in soil suppressive against the fungal root pathogen Rhizoctonia solani, but their actual role in disease suppression is still unclear. Here, the antifungal and plant growth-promoting activities of 18 Lysobacter strains, including 11 strains from Rhizoctonia-suppressive soils, were studied both in vitro and in vivo. Based on 16S rRNA sequencing, the Lysobacter strains from the Rhizoctonia-suppressive soil belonged to the four species Lysobacter antibioticus, Lysobacter capsici, Lysobacter enzymogenes, and Lysobacter gummosus. Most strains showed strong in vitro activity against R. solani and several other pathogens, including Pythium ultimum, Aspergillus niger, Fusarium oxysporum, and Xanthomonas campestris. When the Lysobacter strains were introduced into soil, however, no significant and consistent suppression of R. solani damping-off disease of sugar beet and cauliflower was observed. Subsequent bioassays further revealed that none of the Lysobacter strains was able to promote growth of sugar beet, cauliflower, onion, and Arabidopsis thaliana, either directly or via volatile compounds. The lack of in vivo activity is most likely attributed to poor colonization of the rhizosphere by the introduced Lysobacter strains. In conclusion, our results demonstrated that Lysobacter species have strong antagonistic activities against a range of pathogens, making them an important source for putative new enzymes and antimicrobial compounds. However, their potential role in R. solani disease suppressive soil could not be confirmed. In-depth omics'–based analyses will be needed to shed more light on the potential contribution of Lysobacter species to the collective activities of microbial consortia in disease suppressive soils.
    Preview · Article · Nov 2015 · Frontiers in Microbiology
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    ABSTRACT: In disease-suppressive soils, plants are protected from infections by specific root pathogens due to the antagonistic activities of soil and rhizosphere microorganisms. For most disease-suppressive soils, however, the microorganisms and mechanisms involved in pathogen control are largely unknown. Our recent studies identified Actinobacteria as the most dynamic phylum in a soil suppressive to the fungal root pathogen Rhizoctonia solani. Here we isolated and characterized 300 isolates of rhizospheric Actinobacteria from the Rhizoctonia-suppressive soil. Streptomyces species were the most abundant, representing approximately 70% of the isolates. Streptomyces are renowned for the production of an exceptionally large number of secondary metabolites, including volatile organic compounds (VOCs). VOC profiling of 12 representative Streptomyces isolates by SPME-GC-MS allowed a more refined phylogenetic delineation of the Streptomyces isolates than the sequencing of 16S rRNA and the house-keeping genes atpD and recA only. VOCs of several Streptomyces isolates inhibited hyphal growth of R. solani and significantly enhanced plant shoot and root biomass. Coupling of Streptomyces VOC profiles with their effects on fungal growth, pointed to VOCs potentially involved in antifungal activity. Subsequent assays with five synthetic analogues of the identified VOCs showed that methyl 2-methylpentanoate, 1,3,5-trichloro-2-methoxy benzene and the VOCs mixture have antifungal activity. In conclusion, our results point to a potential role of VOC-producing Streptomyces in disease suppressive soils and show that VOC profiling of rhizospheric Streptomyces can be used as a complementary identification tool to construct strain-specific metabolic signatures.
    Full-text · Article · Oct 2015 · Frontiers in Microbiology
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    ABSTRACT: Pseudomonads produce several lipopeptide biosurfactants that have antimicrobial properties, but also facilitate surface motility and influence biofilm formation. Detailed studies addressing the significance of lipopeptides for biofilm formation and architecture are rare. Hence the current study sets out to determine the specific role of the lipopeptide viscosin for Pseudomonas fluorescens SBW25 biofilm formation, architecture and dispersal, and to relate viscA gene expression with viscosin production and effect. Initially, we compared biofilm formation of SBW25 and the viscosin-deficient mutant strain SBW25ΔviscA in static microtiter assays. These experiments demonstrated that viscosin had little influence on the amount of biofilm formed by SBW25 during the early stages of biofilm development. Later, however, SBW25 formed significantly less biofilm than SBW25ΔviscA. The indication that viscosin is involved in biofilm dispersal was confirmed by chemical complementation of the mutant biofilm. Further, a fluorescent bioreporter showed that viscA expression was induced in biofilms 4 hours prior to dispersal. Subsequent detailed studies of biofilms formed in flow-cells for up to 5 days revealed that SBW25 and SBW25ΔviscA developed comparable biofilms dominated by well-defined mushroom-shaped structures. Carbon-starvation was required to obtain biofilm dispersal in this system. Dispersal of SBW25 biofilms was significantly larger than of SBW25ΔviscA biofilms after 3 hours, and importantly, carbon-starvation strongly induced viscA expression, in particular for cells that were apparently leaving the biofilm. Hence the current study points towards a role for viscosin-facilitated motility in dispersal of SBW25 biofilms.
    No preview · Article · Sep 2015 · Microbiology
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    ABSTRACT: Emerging fungal and oomycete pathogens are increasingly threatening animals and plants globally. Amongst oomycetes, Saprolegnia species adversely affect wild and cultivated populations of amphibians and fish, leading to substantial reductions in biodiversity and food productivity. With the ban of several chemical control measures, new sustainable methods are needed to mitigate Saprolegnia infections in aquaculture. Here, PhyloChip-based community analyses showed that the Pseudomonadales, particularly Pseudomonas species, represent one of the largest bacterial orders associated with salmon eggs from a commercial hatchery. Among the Pseudomonas species isolated from salmon eggs, significantly more biosurfactant producers were retrieved from healthy salmon eggs than from Saprolegnia-infected eggs. Subsequent in vivo activity bioassays showed that Pseudomonas isolate H6 significantly reduced salmon egg mortality caused by Saprolegnia diclina. Live colony mass spectrometry showed that strain H6 produces a viscosin-like lipopeptide surfactant. This biosurfactant inhibited growth of Saprolegnia in vitro, but no significant protection of salmon eggs against Saprolegniosis was observed. These results indicate that live inocula of aquatic Pseudomonas strains, instead of their bioactive compound, can provide new (micro)biological and sustainable means to mitigate oomycete diseases in aquaculture.
    Full-text · Article · Aug 2015 · PLoS ONE
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    ABSTRACT: A wide variety of enzymatic pathways that produce specialized metabolites in bacteria, fungi and plants are known to be encoded in biosynthetic gene clusters. Information about these clusters, pathways and metabolites is currently dispersed throughout the literature, making it difficult to exploit. To facilitate consistent and systematic deposition and retrieval of data on biosynthetic gene clusters, we propose the Minimum Information about a Biosynthetic Gene cluster (MIBiG) data standard.
    Full-text · Article · Aug 2015 · Nature Chemical Biology
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    ABSTRACT: Protozoan predation of bacteria can significantly affect soil microbial community composition and ecosystem functioning. Bacteria possess diverse defense strategies to resist or evade protozoan predation. For soil-dwelling Pseudomonas species, several secondary metabolites were proposed to provide protection against different protozoan genera. By combining whole-genome transcriptome analyses with (live) imaging mass spectrometry (IMS), we observed multiple changes in the molecular and chemical dialogues between Pseudomonas fluorescens and the protist Naegleria americana. Lipopeptide (LP) biosynthesis was induced in Pseudomonas upon protozoan grazing and LP accumulation transitioned from homogeneous distributions across bacterial colonies to site-specific accumulation at the bacteria-protist interface. Also putrescine biosynthesis was upregulated in P. fluorescens upon predation. We demonstrated that putrescine induces protozoan trophozoite encystment and adversely affects cyst viability. This multifaceted study provides new insights in common and strain-specific responses in bacteria-protozoa interactions, including responses that contribute to bacterial survival in highly competitive soil and rhizosphere environments.
    Full-text · Article · Aug 2015 · Scientific Reports
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    ABSTRACT: The plant microbiome represents an enormous untapped resource for discovering novel genes and bioactive compounds. Previously, we isolated Pseudomonas sp. SH-C52 from the rhizosphere of sugar beet plants grown in a soil suppressive to the fungal pathogen Rhizoctonia solani and showed that its antifungal activity is, in part, attributed to the production of the chlorinated 9-amino-acid lipopeptide thanamycin (Mendes et al., 2011). To get more insight into its biosynthetic repertoire, the genome of Pseudomonas sp. SH-C52 was sequenced and subjected to in silico, mutational and functional analyses. The sequencing revealed a genome size of 6.3 Mb and 5579 predicted ORFs. Phylogenetic analysis placed strain SH-C52 within the Pseudomonas corrugata clade. In silico analysis for secondary metabolites revealed a total of six non-ribosomal peptide synthetase (NRPS) gene clusters, including the two previously described NRPS clusters for thanamycin and the 2-amino acid antibacterial lipopeptide brabantamide. Here we show that thanamycin also has activity against an array of other fungi and that brabantamide A exhibits anti-oomycete activity and affects phospholipases of the late blight pathogen Phytophthora infestans. Most notably, mass spectrometry led to the discovery of a third lipopeptide, designated thanapeptin, with a 22-amino-acid peptide moiety. Seven structural variants of thanapeptin were found with varying degrees of activity against P. infestans. Of the remaining four NRPS clusters, one was predicted to encode for yet another and unknown lipopeptide with a predicted peptide moiety of 8-amino acids. Collectively, these results show an enormous metabolic potential for Pseudomonas sp. SH-C52, with at least three structurally diverse lipopeptides, each with a different antimicrobial activity spectrum.
    Preview · Article · Jul 2015 · Frontiers in Microbiology
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    Juan E Pérez-Jaramillo · Rodrigo Mendes · Jos M Raaijmakers
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    ABSTRACT: The rhizosphere microbiome is pivotal for plant health and growth, providing defence against pests and diseases, facilitating nutrient acquisition and helping plants to withstand abiotic stresses. Plants can actively recruit members of the soil microbial community for positive feedbacks, but the underlying mechanisms and plant traits that drive microbiome assembly and functions are largely unknown. Domestication of plant species has substantially contributed to human civilization, but also caused a strong decrease in the genetic diversity of modern crop cultivars that may have affected the ability of plants to establish beneficial associations with rhizosphere microbes. Here, we review how plants shape the rhizosphere microbiome and how domestication may have impacted rhizosphere microbiome assembly and functions via habitat expansion and via changes in crop management practices, root exudation, root architecture, and plant litter quality. We also propose a "back to the roots" framework that comprises the exploration of the microbiome of indigenous plants and their native habitats for the identification of plant and microbial traits with the ultimate goal to reinstate beneficial associations that may have been undermined during plant domestication.
    Full-text · Article · Jun 2015 · Plant Molecular Biology
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    ABSTRACT: Pseudomonas spp. are prolific producers of natural products from many structural classes. Here we show that the soil bacterium Pseudomonas protegens Pf-5 is capable of producing trace levels of the triazine natural product toxoflavin (1) under microaerobic conditions. We evaluated toxoflavin production by derivatives of Pf-5 having deletions in specific biosynthesis genes, which led us to propose a new biosynthetic pathway for toxoflavin that shares the first two steps with riboflavin biosynthesis. We also report that toxM, which is not present in the well-characterized cluster of Burkholderia glumae, encodes a monooxygenase that degrades toxoflavin. The toxoflavin degradation product of ToxM is identical to that of TflA, the toxoflavin lyase from Paenibacillus polymyxa. Toxoflavin production by P. protegens causes inhibition of several plant-pathogenic bacteria, and introduction of toxM into the toxoflavin-sensitive strain P. syringae DC3000 results in resistance to toxoflavin. © 2015 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim.
    No preview · Article · Jun 2015 · ChemBioChem
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    Emilie Chapelle · Rodrigo Mendes · Peter A Hm Bakker · Jos M Raaijmakers
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    ABSTRACT: The rhizosphere is the infection court where soil-borne pathogens establish a parasitic relationship with the plant. To infect root tissue, pathogens have to compete with members of the rhizosphere microbiome for available nutrients and microsites. In disease-suppressive soils, pathogens are strongly restricted in growth by the activities of specific rhizosphere microorganisms. Here, we sequenced metagenomic DNA and RNA of the rhizosphere microbiome of sugar beet seedlings grown in a soil suppressive to the fungal pathogen Rhizoctonia solani. rRNA-based analyses showed that Oxalobacteraceae, Burkholderiaceae, Sphingobacteriaceae and Sphingomonadaceae were significantly more abundant in the rhizosphere upon fungal invasion. Metatranscriptomics revealed that stress-related genes (ppGpp metabolism and oxidative stress) were upregulated in these bacterial families. We postulate that the invading pathogenic fungus induces, directly or via the plant, stress responses in the rhizobacterial community that lead to shifts in microbiome composition and to activation of antagonistic traits that restrict pathogen infection.The ISME Journal advance online publication, 29 May 2015; doi:10.1038/ismej.2015.82.
    Full-text · Article · May 2015 · The ISME Journal
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    ABSTRACT: Microorganisms are important factors in shaping our environment. One key characteristic that has been neglected for a long time is the ability of microorganisms to release chemically diverse volatile compounds. At present, it is clear that the blend of volatiles released by microorganisms can be very complex and often includes many unknown compounds for which the chemical structures remain to be elucidated. The biggest challenge now is to unravel the biological and ecological functions of these microbial volatiles. There is increasing evidence that microbial volatiles can act as infochemicals in interactions among microbes and between microbes and their eukaryotic hosts. Here, we review and discuss recent advances in understanding the natural roles of volatiles in microbe-microbe interactions. Specific emphasis will be given to the antimicrobial activities of microbial volatiles and their effects on bacterial quorum sensing, motility, gene expression and antibiotic resistance.The ISME Journal advance online publication, 29 May 2015; doi:10.1038/ismej.2015.42.
    Full-text · Article · May 2015 · The ISME Journal
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    Yong-Soon Park · Swarnalee Dutta · Mina Ann · Jos M. Raaijmakers · Kyungseok Park
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    ABSTRACT: Volatile organic compounds (VOCs) from plant growth-promoting rhizobacteria (PGPR) play key roles in modulating plant growth and induced systemic resistance (ISR) to pathogens. Despite their significance, the physiological functions of the specific VOCs produced by Pseudomonas fluorescens SS101 (Pf.SS101) have not been precisely elucidated. The effects of Pf.SS101 and its VOCs on augmentation of plant growth promotion were investigated in vitro and in planta. Significant growth promotion was observed in plants exposed Pf.SS101 under both conditions, suggesting its VOCs play a key role in promoting plant growth. Solid-phase micro-extraction (SPME) and a gas chromatography-mass spectrophotometer (GC-MS) system were used to characterize the VOCs emitted by Pf.SS101 and 11 different compounds were detected in samples inoculated this bacterium, including 13-Tetradecadien-1-ol, 2-butanone and 2-Methyl-n-1-tridecene. Application of these compounds resulted in enhanced plant growth. This study suggests that Pf.SS101 promotes the growth of plants via the release of VOCs including 13-Tetradecadien-1-ol, 2-butanone and 2-Methyl-n-1-tridecene, thus increasing understanding of the role of VOCs in plant-bacterial inter-communication. Copyright © 2015. Published by Elsevier Inc.
    Full-text · Article · Apr 2015 · Biochemical and Biophysical Research Communications
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    ABSTRACT: Endophytic Pseudomonas poae strain RE*1-1-14 was originally isolated from internal root tissue of sugar beet plants and shown to suppress growth of the fungal pathogen Rhizoctonia solani both in vitro and in the field. To identify genes involved in its biocontrol activity, RE*1-1-14 random mutagenesis and sequencing led to the identification of a nonribosomal peptide synthetase (NRPS) gene cluster predicted to encode a lipopeptide (LP) with a 10-amino acid peptide moiety. The two unlinked gene clusters consisted of three NRPS genes, designated poaA (cluster 1), and poaB and poaC (cluster 2), spanning approximately 33.7 kb. In silico analysis followed by chemical analyses revealed that the encoded LP designated poaeamide, is a structurally new member of the orfamide family. Poaeamide inhibited mycelial growth of R. solani and different oomycetes including Phytophthora capsici, Ph. infestans, and Pythium ultimum. The novel LP was shown to be essential for swarming motility of strain RE*1-1-14 and had an impact on root colonization of sugar beet seedlings The poaeamide-deficient mutant colonized the rhizosphere and upper plant cortex at higher densities and with more scattered colonization patterns than the wildtype. Collectively these results indicate that P. poae RE*1-1-14 produces a structurally new LP that is relevant for its antagonistic activity against soil-borne plant pathogens and for colonization of sugar beet roots.
    Full-text · Article · Mar 2015 · Molecular Plant-Microbe Interactions
  • Rodrigo Mendes · Jos M Raaijmakers
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    ABSTRACT: The ISME Journal: Multidisciplinary Journal of Microbial Ecology is the official Journal of the International Society for Microbial Ecology, publishing high-quality, original research papers, short communications, commentary articles and reviews in the rapidly expanding and diverse discipline of microbial ecology.
    No preview · Article · Feb 2015 · The ISME Journal
  • Jos M. Raaijmakers
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    ABSTRACT: The rhizosphere provides a home to numerous (micro)organisms that in turn may affect plant growth, development, and tolerance to abiotic and biotic stresses. How plants shape the rhizosphere microbiome has been subject of many past and present studies with the ultimate goal to identify plant genetic traits that select and support beneficial microorganisms. Novel ‘omics technologies have provided more in-depth knowledge of the diversity and functioning of the rhizosphere microbiome and significant advances are being made to uncover mechanisms, genes and metabolites involved in the multitrophic interactions in the rhizosphere. To better understand this intriguing complexity, both reductionists’ and systems ecology approaches are needed to identify the biotic and abiotic factors involved in microbiome assembly. Here, different strategies are discussed to re-shape the rhizosphere microbiome in favour of microbial consortia that promote root development and plant growth, and that prevent the proliferation of pests and diseases.
    No preview · Chapter · Jan 2015

Publication Stats

7k Citations
496.05 Total Impact Points

Institutions

  • 2015
    • Leiden University
      • Institute of Biology Leiden
      Leyden, South Holland, Netherlands
  • 2014-2015
    • Netherlands Institute of Ecology (NIOO-KNAW)
      Wageningen, Gelderland, Netherlands
  • 2000-2015
    • Wageningen University
      • Department of Phytopathology
      Wageningen, Gelderland, Netherlands
  • 2009
    • Sonoma State University
      • Department of Biology
      Ронърт Парк, California, United States
  • 2007
    • University of São Paulo
      • Departamento de Genética (LGN) (ESALQ)
      San Paulo, São Paulo, Brazil
  • 2003
    • University of Burgundy
      Dijon, Bourgogne, France
  • 1997-2002
    • Washington State University
      • Department of Plant Pathology
      پولمن، واشینگتن, Washington, United States
  • 1994-1995
    • Utrecht University
      Utrecht, Utrecht, Netherlands