Staff Publications

Staff Publications

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    'Staff publications' is the digital repository of Wageningen University & Research

    'Staff publications' contains references to publications authored by Wageningen University staff from 1976 onward.

    Publications authored by the staff of the Research Institutes are available from 1995 onwards.

    Full text documents are added when available. The database is updated daily and currently holds about 240,000 items, of which 72,000 in open access.

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    The diversion of 2-C-methyl-D-erythritol-2,4-cyclodiphosphate from the 2-C-methyl-D-erythritol 4-phosphate pathway to hemiterpene glycosides mediates stress responses in Arabidopsis thaliana
    Gonzalez-Cabanelas, D. ; Wright, L.P. ; Paetz, C. ; Onkokesung, N. ; Gershenzon, J. ; Rodriguez-Concepcion, M. ; Phillips, M.A. - \ 2015
    The Plant Journal 82 (2015)1. - ISSN 0960-7412 - p. 122 - 137.
    plant defensin gene - isoprenoid biosynthesis - salicylic-acid - gas-chromatography - mass-spectrometry - mep pathway - synthase - resistance - jasmonate - reveals
    2-C-Methyl-D-erythritol-2,4-cyclodiphosphate (MEcDP) is an intermediate of the plastid-localized 2-C-methyl-D-erythritol-4-phosphate (MEP) pathway which supplies isoprenoid precursors for photosynthetic pigments, redox co-factor side chains, plant volatiles, and phytohormones. The Arabidopsis hds-3 mutant, defective in the 1-hydroxy-2-methyl-2-(E)-butenyl-4-diphosphate synthase step of the MEP pathway, accumulates its substrate MEcDP as well as the free tetraol 2-C-methyl-D-erythritol (ME) and glucosylated ME metabolites, a metabolic diversion also occurring in wild type plants. MEcDP dephosphorylation to the free tetraol precedes glucosylation, a process which likely takes place in the cytosol. Other MEP pathway intermediates were not affected in hds-3. Isotopic labeling, dark treatment, and inhibitor studies indicate that a second pool of MEcDP metabolically isolated from the main pathway is the source of a signal which activates salicylic acid induced defense responses before its conversion to hemiterpene glycosides. The hds-3 mutant also showed enhanced resistance to the phloem-feeding aphid Brevicoryne brassicae due to its constitutively activated defense response. However, this MEcDP-mediated defense response is developmentally dependent and is repressed in emerging seedlings. MEcDP and ME exogenously applied to adult leaves mimics many of the gene induction effects seen in the hds-3 mutant. In conclusion, we have identified a metabolic shunt from the central MEP pathway that diverts MEcDP to hemiterpene glycosides via ME, a process linked to balancing plant responses to biotic stress.
    Natural loss-of-function mutation of EDR1 conferring resistance to tomato powdery mildew in Arabidopsis thaliana accession C24
    Gao, D. ; Appiano, M. ; Huibers, R.P. ; Loonen, A.E.H.M. ; Visser, R.G.F. ; Wolters, A.M.A. ; Bai, Y. - \ 2015
    Molecular Plant Pathology 16 (2015)1. - ISSN 1464-6722 - p. 71 - 82.
    salicylic-acid - downy mildew - gene - defense - plants - microsatellites - mechanism - evolution - cloning - kinase
    To screen for potentially novel types of resistance to tomato powdery mildew Oidium neolycopersici, a disease assay was performed on 123 Arabidopsis thaliana accessions. Forty accessions were fully resistant, and one, C24, was analysed in detail. By quantitative trait locus (QTL) analysis of an F2 population derived from C24 × Sha (susceptible accession), two QTLs associated with resistance were identified in C24. Fine mapping of QTL-1 on chromosome 1 delimited the region to an interval of 58¿kb encompassing 15 candidate genes. One of these was Enhanced Disease Resistance 1 (EDR1). Evaluation of the previously obtained edr1 mutant of Arabidopsis accession Col-0, which was identified because of its resistance to powdery mildew Golovinomyces cichoracearum, showed that it also displayed resistance to O.¿neolycopersici. Sequencing of EDR1 in our C24 germplasm (referred to as C24-W) revealed two missing nucleotides in the second exon of EDR1 resulting in a premature stop codon. Remarkably, C24 obtained from other laboratories does not contain the EDR1 mutation. To verify the identity of C24-W, a DNA region containing a single nucleotide polymorphism (SNP) unique to C24 was sequenced showing that C24-W contains the C24-specific nucleotide. C24-W showed enhanced resistance to O.¿neolycopersici compared with C24 not containing the edr1 mutation. Furthermore, C24-W displayed a dwarf phenotype, which was not associated with the mutation in EDR1 and was not caused by the differential accumulation of pathogenesis-related genes. In conclusion, we identified a natural edr1 mutant in the background of C24.
    Enhancing crop resilience to combined abiotic and biotic stress through the dissection of physiological and molecular crosstalk
    Kissoudis, C. ; Wiel, C.C.M. van de; Visser, R.G.F. ; Linden, C.G. van der - \ 2014
    Frontiers in Plant Science 5 (2014). - ISSN 1664-462X - 20 p.
    systemic acquired-resistance - activated protein-kinase - programmed cell-death - regulated gene-expression - plant immune-responses - abscisic-acid - salicylic-acid - disease resistance - arabidopsis-thaliana - transcription factor
    Plants growing in their natural habitats are often challenged simultaneously by multiple stress factors, both abiotic and biotic. Research has so far been limited to responses to individual stresses, and understanding of adaptation to combinatorial stress is limited, but indicative of non-additive interactions. Omics data analysis and functional characterization of individual genes has revealed a convergence of signaling pathways for abiotic and biotic stress adaptation. Taking into account that most data originate from imposition of individual stress factors, this review summarizes these findings in a physiological context, following the pathogenesis timeline and highlighting potential differential interactions occurring between abiotic and biotic stress signaling across the different cellular compartments and at the whole plant level. Potential effects of abiotic stress on resistance components such as extracellular receptor proteins, R-genes and systemic acquired resistance will be elaborated, as well as crosstalk at the levels of hormone, reactive oxygen species, and redox signaling. Breeding targets and strategies are proposed focusing on either manipulation and deployment of individual common regulators such as transcription factors or pyramiding of non- (negatively) interacting components such as R-genes with abiotic stress resistance genes. We propose that dissection of broad spectrum stress tolerance conferred by priming chemicals may provide an insight on stress cross regulation and additional candidate genes for improving crop performance under combined stress. Validation of the proposed strategies in lab and field experiments is a first step toward the goal of achieving tolerance to combinatorial stress in crops.
    Activation tagging of ATHB13 in Arabidopsis thaliana confers broad-spectrum disease resistance
    Gao, D. ; Huibers, R.P. ; Chen, X. ; Loonen, A.E.H.M. ; Visser, R.G.F. ; Wolters, A.M.A. ; Bai, Y. - \ 2014
    Plant Molecular Biology 86 (2014)6. - ISSN 0167-4412 - p. 641 - 653.
    vegetative storage protein - powdery mildew resistance - transcription factors hahb1 - nudix hydrolase - salicylic-acid - plant defense - cell-death - hd-zip - oidium-neolycopersici - expression patterns
    Powdery mildew species Oidium neolycopersici (On) can cause serious yield losses in tomato production worldwide. Besides on tomato, On is able to grow and reproduce on Arabidopsis. In this study we screened a collection of activation-tagged Arabidopsis mutants and identified one mutant, 3221, which displayed resistance to On, and in addition showed a reduced stature and serrated leaves. Additional disease tests demonstrated that the 3221 mutant exhibited resistance to downy mildew (Hyaloperonospora arabidopsidis) and green peach aphid (Myzus persicae), but retained susceptibility to bacterial pathogen Pseudomonas syringae pv tomato DC3000. The resistance trait and morphological alteration were mutually linked in 3221. Identification of the activation tag insertion site and microarray analysis revealed that ATHB13, a homeodomain-leucine zipper (HD-Zip) transcription factor, was constitutively overexpressed in 3221. Silencing of ATHB13 in 3221 resulted in the loss of both the morphological alteration and resistance, whereas overexpression of the cloned ATHB13 in Col-0 and Col-eds1-2 backgrounds resulted in morphological alteration and resistance. Microarray analysis further revealed that overexpression of ATHB13 influenced the expression of a large number of genes. Previously, it was reported that ATHB13-overexpressing lines conferred tolerance to abiotic stress. Together with our results, it appears that ATHB13 is involved in the crosstalk between abiotic and biotic stress resistance pathways.
    Phenotypic analyses of Arabidopsis T-DNA insertion lines and expression profiling reveal that multiple L-type lectin receptor kinases are involved in plant immunity
    Wang, Y. ; Bouwmeester, K. ; Beseh, P. ; Shan, W. ; Govers, F. - \ 2014
    Molecular Plant-Microbe Interactions 27 (2014)12. - ISSN 0894-0282 - p. 1390 - 1402.
    pattern-triggered immunity - phytophthora-infestans - salicylic-acid - defense responses - innate immunity - thaliana - gene - resistance - biology - roles
    L-type lectin receptor kinases (LecRKs) are membrane-spanning receptor-like kinases with putative roles in biotic and abiotic stress responses and in plant development. In Arabidopsis, 45 LecRKs were identified but their functions are largely unknown. Here, a systematic functional analysis was carried out by evaluating phenotypic changes of Arabidopsis LecRK T-DNA insertion lines in plant development and upon exposure to various external stimuli. None of the LecRK T-DNA insertion lines showed clear developmental changes, neither under normal conditions nor upon abiotic stress treatment. However, many of the T-DNA insertion lines showed altered resistance to Phytophthora brassicae, Phytophthora capsici, Pseudomonas syringae or Alternaria brassicicola. One mutant defective in LecRK-V.5 expression, was compromised in resistance to two Phytophthora spp. but showed enhanced resistance to P. syringae. LecRK-V.5 overexpression confirmed its dual role in resistance and susceptibility depending on the pathogen. Combined analysis of these phenotypic data and LecRK expression profiles retrieved from public datasets revealed that LecRKs which are hardly induced upon infection or even suppressed are also involved in pathogen resistance. Computed co-expression analysis revealed that LecRKs with similar function displayed diverse expression patterns. Since LecRKs are widespread in plants, the results presented here provide invaluable information for exploring the potential of LecRKs as novel sources of resistance in crops.
    Plant interactions with multiple insect herbivores: from community to genes
    Stam, J.M. ; Kroes, A. ; Li, Y. ; Gols, R. ; Loon, J.J.A. van; Poelman, E.H. ; Dicke, M. - \ 2014
    Annual Review of Plant Biology 65 (2014). - ISSN 1543-5008 - p. 689 - 713.
    milkweed asclepias-syriaca - primrose oenothera-biennis - indirect interaction webs - top-down forces - salicylic-acid - jasmonic acid - brassica-oleracea - bottom-up - arabidopsis-thaliana - phytophagous insects
    Every plant is a member of a complex insect community that consists of tens to hundreds of species that belong to different trophic levels. The dynamics of this community are critically influenced by the plant, which mediates interactions between community members that can occur on the plant simultaneously or at different times. Herbivory results in changes in the plant's morphological or chemical phenotype that affect interactions with subsequently arriving herbivores. Changes in the plant's phenotype are mediated by molecular processes such as phytohormonal signaling networks and transcriptomic rearrangements that are initiated by oral secretions of the herbivore. Processes at different levels of biological complexity occur at timescales ranging from minutes to years. In this review, we address plant-mediated interactions with multiple species of the associated insect community and their effects on community dynamics, and link these to the mechanistic effects that multiple attacks have on plant phenotypes.
    Genetics and molecular mechanisms of resistance to powdery mildews in tomato (Solanum lycopersicum) and its wild relatives
    Seifi Abdolabad, A.R. ; Dongli Gao, Dongli ; Zheng, Z. ; Pavan, S.N.C. ; Faino, L. ; Visser, R.G.F. ; Wolters, A.M.A. ; Bai, Y. - \ 2014
    European Journal of Plant Pathology 138 (2014)3. - ISSN 0929-1873 - p. 641 - 665.
    plant-pathogen interactions - hypersensitive cell-death - rna silencing suppressors - multiple fungal pathogens - race-specific resistance - leucine-rich repeat - oidium-neolycopersici - disease resistance - abscisic-acid - salicylic-acid
    Powdery mildews (PMs) cause disease in a wide range of plant species including important crops. Taking tomato as an example, here we review findings on the genetic basis and mechanisms of plant resistance to PMs. First, we present a summary of our research on tomato resistance to two PM species, with the focus on Oidium neolycopersici. We discuss the genetics of resistance to this pathogen in tomato. Then, we compare different forms of resistance mediated by different resistance genes based on molecular and cytological data. Also, we provide a comparison between these resistance genes in tomato with those in barley, Arabidopsis and wheat, in order to present a model for the genetic basis of resistance to PMs in plants. We try to accommodate these resistance mechanisms in the current model of plant innate immunity. At the end we discuss possibilities to translate these findings to practical approaches in breeding for resistance to PMs in crops.
    Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs
    Denance, N. ; Sanchez Vallet, A. ; Goffner, D. ; Molina, A. - \ 2013
    Frontiers in Plant Science 4 (2013). - ISSN 1664-462X
    systemic acquired-resistance - pattern-recognition receptors - mediated defense responses - syringae pv. tomato - abscisic-acid - pseudomonas-syringae - salicylic-acid - arabidopsis-thaliana - botrytis-cinerea - ustilago-maydis
    Plant growth and response to environmental cues are largely governed by phytohormones. The plant hormones ethylene, jasmonic acid, and salicylic acid (SA) play a central role in the regulation of plant immune responses. In addition, other plant hormones, such as auxins, abscisic acid (ABA), cytokinins, gibberellins, and brassinosteroids, that have been thoroughly described to regulate plant development and growth, have recently emerged as key regulators of plant immunity. Plant hormones interact in complex networks to balance the response to developmental and environmental cues and thus limiting defense-associated fitness costs. The molecular mechanisms that govern these hormonal networks are largely unknown. Moreover, hormone signaling pathways are targeted by pathogens to disturb and evade plant defense responses. In this review, we address novel insights on the regulatory roles of the ABA, SA, and auxin in plant resistance to pathogens and we describe the complex interactions among their signal transduction pathways. The strategies developed by pathogens to evade hormone-mediated defensive responses are also described. Based on these data we discuss how hormone signaling could be manipulated to improve the resistance of crops to pathogens.
    Morphological and biochemical characterization of Erwinia amylovora-induced hypersensitive cell death in apple leaves
    Iakimova, E.T. ; Sobiczewski, P. ; Michalczuk, L. ; Wegrzynowicz-Lesiak, E. ; Mikicinski, A. ; Woltering, E.J. - \ 2013
    Plant Physiology and Biochemistry 63 (2013). - ISSN 0981-9428 - p. 292 - 305.
    vacuolar-processing-enzyme - 1-aminocyclopropane-1-carboxylic acid synthase - mitochondrial permeability transition - arabidopsis-thaliana - fire blight - oxidative stress - defense responses - salicylic-acid - host plants - disease resistance
    In attached apple leaves, spot-inoculated with Erwinia amylovora, the phenotypic appearance of the hypersensitive response (HR) and the participation of ethylene, reactive oxygen species (ROS) and of vacuolar processing enzyme (VPE) (a plant caspase-1-like protease) were analysed. The HR in both the resistant and susceptible genotypes expressed a similar pattern of distinguishable micro HR lesions that progressed into confined macro HR lesions. The HR symptoms in apple were compared to those in non-host tobacco. The morphology of dead cells (protoplast shrinkage and retraction from cell wall) in apple leaves resembled necrotic programmed cell death (PCD). Lesion formation in both cv. Free Redstar (resistant) and cv. Idared (highly susceptible) was preceded by ROS accumulation and elevation of ethylene levels. Treatment of infected leaves with an inhibitor of ethylene synthesis led to a decrease of ethylene emission and suppression of lesion development in both cultivars. In the resistant but not in the susceptible apple cultivar an early and late increase in VPE gene expression was detected. This suggests that VPE might be an underlying component of the response to E. amylovora in resistant apple cultivars. The findings show that in the studied pathosystem the cell death during the HR proceeds through a signal transduction cascade in which ROS, ethylene and VPE pathways play a role.
    Two-way plant mediated interactions between root-associated microbes and insects: from ecology to mechanisms
    Pangesti, N.P.D. ; Pineda Gomez, A.M. ; Pieterse, C.M.J. ; Dicke, M. ; Loon, J.J.A. van - \ 2013
    Frontiers in Plant Science 4 (2013). - ISSN 1664-462X - 11 p.
    induced systemic resistance - arbuscular mycorrhizal fungi - below-ground interactions - arabidopsis-thaliana - rhizosphere microbiome - defense responses - salicylic-acid - bacterial communities - jasmonic acid - pathogenic microorganisms
    Plants are members of complex communities and function as a link between above- and below-ground organisms. Associations between plants and soil-borne microbes commonly occur and have often been found beneficial for plant fitness. Root-associated microbes may trigger physiological changes in the host plant that influence interactions between plants and aboveground insects at several trophic levels. Aboveground, plants are under continuous attack by insect herbivores and mount multiple responses that also have systemic effects on belowground microbes. Until recently, both ecological and mechanistic studies have mostly focused on exploring these below- and above-ground interactions using simplified systems involving both single microbe and herbivore species, which is far from the naturally occurring interactions. Increasing the complexity of the systems studied is required to increase our understanding of microbe-plant-insect interactions and to gain more benefit from the use of non-pathogenic microbes in agriculture. In this review, we explore how colonization by either single non-pathogenic microbe species or a community of such microbes belowground affects plant growth and defense and how this affects the interactions of plants with aboveground insects at different trophic levels. Moreover, we review how plant responses to foliar herbivory by insects belonging to different feeding guilds affect interactions of plants with non-pathogenic soil-borne microbes. The role of phytohormones in coordinating plant growth, plant defenses against foliar herbivores while simultaneously establishing associations with non-pathogenic soil microbes is discussed.
    Canopy light cues affect emission of constitutive and methyl jasmonate-induced volatile organic compounds in Arabidopsis thaliana
    Kegge, W. ; Weldegergis, B.T. ; Soler, R. ; Vergeer-van Eijk, M.H. ; Dicke, M. ; Voesenek, L.A.C.J. ; Pierik, R. - \ 2013
    New Phytologist 200 (2013)3. - ISSN 0028-646X - p. 861 - 874.
    salicylic-acid - host-plant - induced resistance - insect herbivores - indirect defenses - chemical ecology - shade avoidance - abiotic factors - bean-plants - ethylene
    The effects of plant competition for light on the emission of plant volatile organic compounds (VOCs) were studied by investigating how different light qualities that occur in dense vegetation affect the emission of constitutive and methyl-jasmonate-induced VOCs. Arabidopsis thaliana Columbia (Col-0) plants and Pieris brassicae caterpillars were used as a biological system to study the effects of light quality manipulations on VOC emissions and attraction of herbivores. VOCs were analysed using gas chromatography-mass spectrometry and the effects of light quality, notably the red : far red light ratio (R : FR), on expression of genes associated with VOC production were studied using reverse transcriptase-quantitative PCR. The emissions of both constitutive and methyl-jasmonate-induced green leaf volatiles and terpenoids were partially suppressed under low R : FR and severe shading conditions. Accordingly, the VOC-based preference of neonates of the specialist lepidopteran herbivore P. brassicae was significantly affected by the R : FR ratio. We conclude that VOC-mediated interactions among plants and between plants and organisms at higher trophic levels probably depend on light alterations caused by nearby vegetation. Studies on plant-plant and plant-insect interactions through VOCs should take into account the light quality within dense stands when extrapolating to natural and agricultural field conditions.
    Ecological and phytohormonal aspects of plant volatile emission in response to single and dual infestations with herbivores and phytopathogens
    Ponzio, C. ; Gols, R. ; Pieterse, C.M.J. ; Dicke, M. - \ 2013
    Functional Ecology 27 (2013)3. - ISSN 0269-8463 - p. 587 - 598.
    tritrophic interaction webs - attract insect vectors - host-plant - pseudomonas-syringae - fungal-infection - egg parasitoids - salicylic-acid - damaged plants - beet armyworm - cross-talk
    In their natural environment, plants are faced with a multitude of attackers, of which insect herbivores and plant pathogens are an important component. In response to these attacks, plants release volatile organic compounds (VOCs), which play an important role in the communication between plants and the associated community members, such as other herbivores, phytopathogens and the natural enemies of herbivores. While numerous studies have focused on either plantpathogen or plantinsect interactions, less is known when these two sets of interactions co-occur. Depending on the mode of attack of the pathogen (necrotroph vs. biotroph) or herbivore (chewing vs. piercing-sucking) they will activate different defence pathways in the plant in which the phytohormones salicylic acid (SA), jasmonic acid (JA) and ethylene (ET) play key roles. As these pathways can crosstalk, a pathogen infection can interfere in a plant's defence response to herbivory, and vice versa. Infestation of a plant with organisms inducing SA signalling prior to or simultaneously with attack by organisms that induce the JA pathway often suppresses JA signalling. However, the impact of this signalling pathway crosstalk on VOC induction is not clear cut, as there is high variability in the effects on volatile emissions, ranging from suppression to enhanced emission. The effects of the modified volatile blends on the foraging success of carnivorous natural enemies of herbivorous insects have started to be investigated. Foraging success of natural enemies generally withstands this modification of the host-induced VOC blend, but the presence or absence of key compounds is an important determinant of the response of certain carnivores. Further studies incorporating plantinsect and plantpathogen interactions at different levels of biological integration will provide valuable insight in how plants integrate signals from different suites of attacking organisms into an adaptive defence response.
    Beneficial microbes in a changing environment: are they always helping plants to deal with insects?
    Pineda, A. ; Dicke, M. ; Pieterse, C.M.J. ; Pozo, M.J. - \ 2013
    Functional Ecology 27 (2013)3. - ISSN 0269-8463 - p. 574 - 586.
    arbuscular mycorrhizal symbiosis - ultraviolet-b radiation - abscisic-acid - climate-change - induced resistance - defense responses - water-stress - signaling pathways - fungal endophyte - salicylic-acid
    Plants have a complex immune system that defends them against attackers (e.g. herbivores and microbial pathogens) but that also regulates the interactions with mutualistic organisms (e.g. mycorrhizal fungi and plant growth-promoting rhizobacteria). Plants have to respond to multiple environmental challenges, so they need to integrate both signals associated with biotic and abiotic stresses in the most appropriate response to survive. Beneficial microbes such as rhizobacteria and mycorrhizal fungi can help plants to deal' with pathogens and herbivorous insects as well as to tolerate abiotic stress. Therefore, beneficial microbes may play an important role in a changing environment, where abiotic and biotic stresses on plants are expected to increase. The effects of beneficial microbes on herbivores are highly context-dependent, but little is known on what is driving such dependency. Recent evidence shows that abiotic stresses such as changes in soil nutrients, drought and salt stress, as well as ozone can modify the outcome of plantmicrobeinsect interactions. Here, we review how abiotic stress can affect plantmicrobe, plantinsect and plantmicrobeinsect interactions, and the role of the network of plant signal-transduction pathways in regulating such interactions. Most of the studies on the effects of abiotic stress on plantmicrobeinsect interactions show that the effects of microbes on herbivores (positive or negative) are strengthened under stressful conditions. We propose that, at least in part, this is due to the crosstalk of the different plant signalling pathways triggered by each stress individually. By understanding the cross-regulation mechanisms we may be able to predict the possible outcomes of plant-microbeinsect interactions under particular abiotic stress conditions. We also propose that microbes can help plants to deal with insects mainly under conditions that compromise efficient activation of plant defences. In the context of global change, it is crucial to understand how abiotic stresses will affect species interactions, especially those interactions that are beneficial for plants. The final aim of this review is to stimulate studies unravelling when these beneficial' microbes really benefit a plant.
    The rhizosphere microbiome: significance of plant beneficial, plant pathogenic and human pathogenic microorganisms
    Mendes, R. ; Garbeva, P. ; Raaijmakers, J.M. - \ 2013
    FEMS Microbiology Reviews 37 (2013)5. - ISSN 0168-6445 - p. 634 - 663.
    growth-promoting rhizobacteria - pseudomonas-aeruginosa 7nsk2 - bacterial community structure - disease-suppressive bacteria - induced systemic resistance - tobacco necrosis virus - barley hordeum-vulgare - max l merr - arabidopsis-thaliana - salicylic-acid
    Microbial communities play a pivotal role in the functioning of plants by influencing their physiology and development. While many members of the rhizosphere microbiome are beneficial to plant growth, also plant pathogenic microorganisms colonize the rhizosphere striving to break through the protective microbial shield and to overcome the innate plant defense mechanisms in order to cause disease. A third group of microorganisms that can be found in the rhizosphere are the true and opportunistic human pathogenic bacteria, which can be carried on or in plant tissue and may cause disease when introduced into debilitated humans. Although the importance of the rhizosphere microbiome for plant growth has been widely recognized, for the vast majority of rhizosphere microorganisms no knowledge exists. To enhance plant growth and health, it is essential to know which microorganism is present in the rhizosphere microbiome and what they are doing. Here, we review the main functions of rhizosphere microorganisms and how they impact on health and disease. We discuss the mechanisms involved in the multitrophic interactions and chemical dialogues that occur in the rhizosphere. Finally, we highlight several strategies to redirect or reshape the rhizosphere microbiome in favor of microorganisms that are beneficial to plant growth and health.
    NON-SMOKY GLYCOSYLTRANSFERASE1 Prevents the Release of Smoky Aroma from Tomato Fruit
    Tikunov, Y.M. ; Molthoff, J.W. ; Vos, R.C.H. de; Beekwilder, M.J. ; Houwelingen, A.M.M.L. van; Hooft, J.J.J. van der; Nijenhuis-de Vries, M.A. ; Labrie, C.W. ; Verkerke, W. ; Geest, H.C. van de; Víquez Zamora, A.M. ; Presa, S. ; Rambla Nebot, J.L. ; Granell, A. ; Hall, R.D. ; Bovy, A.G. - \ 2013
    The Plant Cell 25 (2013)8. - ISSN 1040-4651 - p. 3067 - 3078.
    mass spectrometry - small molecules - salicylic-acid - key enzyme - flavor - volatiles - biosynthesis - components - odor - gene
    Phenylpropanoid volatiles are responsible for the key tomato fruit (Solanum lycopersicum) aroma attribute termed “smoky.” Release of these volatiles from their glycosylated precursors, rather than their biosynthesis, is the major determinant of smoky aroma in cultivated tomato. Using a combinatorial omics approach, we identified the NON-SMOKY GLYCOSYLTRANSFERASE1 (NSGT1) gene. Expression of NSGT1 is induced during fruit ripening, and the encoded enzyme converts the cleavable diglycosides of the smoky-related phenylpropanoid volatiles into noncleavable triglycosides, thereby preventing their deglycosylation and release from tomato fruit upon tissue disruption. In an nsgt1/nsgt1 background, further glycosylation of phenylpropanoid volatile diglycosides does not occur, thereby enabling their cleavage and the release of corresponding volatiles. Using reverse genetics approaches, the NSGT1-mediated glycosylation was shown to be the molecular mechanism underlying the major quantitative trait locus for smoky aroma. Sensory trials with transgenic fruits, in which the inactive nsgt1 was complemented with the functional NSGT1, showed a significant and perceivable reduction in smoky aroma. NSGT1 may be used in a precision breeding strategy toward development of tomato fruits with distinct flavor phenotypes.
    Botrytis cinerea mutants deficient in D-galacturonic acid catabolism have a perturbed virulence on Nicotiana benthamiana and Arabidopsis, but not on tomato
    Zhang, L. ; Kan, J.A.L. van - \ 2013
    Molecular Plant Pathology 14 (2013)1. - ISSN 1464-6722 - p. 19 - 29.
    cell-wall polysaccharides - plant defensin gene - salicylic-acid - filamentous fungi - thaliana - pathogen - resistance - pathway - camalexin - biosynthesis
    d-Galacturonic acid is the most abundant monosaccharide component of pectic polysaccharides that comprise a significant part of most plant cell walls. Therefore, it is potentially an important nutritional factor for Botrytis cinerea when it grows in and t
    Friend or foe: genetic and functional characterization of plant endophytic Pseudomonas aeruginosa
    Kumar, A. ; Munder, A. ; Aravind, R. ; Eapen, S.J. ; Tümmler, B. ; Raaijmakers, J.M. - \ 2013
    Environmental Microbiology 15 (2013)3. - ISSN 1462-2912 - p. 764 - 779.
    iii secretion system - fluorescent pseudomonas - population-structure - opportunistic pathogen - biological-control - swarming motility - botrytis-cinerea - salicylic-acid - lung infection - diversity
    Endophytic Pseudomonas aeruginosa strain BP35 was originally isolated from black pepper grown in the rain forest in Kerala, India. Strain PaBP35 was shown to provide significant protection to black pepper against infections by Phytophthora capsici and Radopholus similis. For registration and implementation in disease management programmes, several traits of PaBP35 were investigated including its endophytic behaviour, biocontrol activity, phylogeny and toxicity to mammals. The results showed that PaBP35 efficiently colonized black pepper shoots and displayed a typical spatiotemporal pattern in its endophytic movement with concomitant suppression of Phytophthora rot. Confocal laser scanning microscopy revealed high populations of PaBP35::gfp2 inside tomato plantlets, supporting its endophytic behaviour in other plant species. Polyphasic approaches to genotype PaBP35, including BOX-PCR, recN sequence analysis, multilocus sequence typing and comparative genome hybridization analysis, revealed its uniqueness among P.¿aeruginosa strains representing clinical habitats. However, like other P.¿aeruginosa strains, PaBP35 exhibited resistance to antibiotics, grew at 25–41°C and produced rhamnolipids and phenazines. PaBP35 displayed strong type II secretion effectors-mediated cytotoxicity on mammalian A549 cells. Coupled with pathogenicity in a murine airway infection model, we conclude that this plant endophytic strain is as virulent as clinical P.¿aeruginosa strains. Safety issues related to the selection of plant endophytic bacteria for crop protection are discussed.
    Jasmonate and ethylene signaling mediate whitefly-induced interference with indirect plant defense in Arabidopsis thaliana
    Zhang, P.J. ; Broekgaarden, C. ; Zheng, S.J. ; Snoeren, T.A.L. ; Loon, J.J.A. van; Gols, R. ; Dicke, M. - \ 2013
    New Phytologist 197 (2013)4. - ISSN 0028-646X - p. 1291 - 1299.
    salicylic-acid - transcriptome changes - feeding guilds - tomato plants - herbivores - volatiles - insect - responses - gene - involvement
    Upon herbivore attack, plants activate an indirect defense, that is, the release of a complex mixture of volatiles that attract natural enemies of the herbivore. When plants are simultaneously exposed to two herbivore species belonging to different feeding guilds, one herbivore may interfere with the indirect plant defense induced by the other herbivore. However, little is understood about the mechanisms underlying such interference. Here, we address the effect of herbivory by the phloem-feeding whitefly Bemisia tabaci on the induced indirect defense of Arabidopsis thaliana plants to Plutella xylostella caterpillars, that is, the attraction of the parasitoid wasp Diadegma semiclausum. Assays with various Arabidopsis mutants reveal that B. tabaci infestation interferes with indirect plant defense induced by P. xylostella, and that intact jasmonic acid and ethylene signaling are required for such interference caused by B. tabaci. Chemical analysis of plant volatiles showed that the composition of the blend emitted in response to the caterpillars was significantly altered by co-infestation with whiteflies. Moreover, whitefly infestation also had a considerable effect on the transcriptomic response of the plant to the caterpillars. Understanding the mechanisms underlying a plant’s responses to multiple attackers will be important for the development of crop protection strategies in a multi-attacker context.
    Neonates know better than their mothers when selecting a host plant
    Soler, R. ; Pineda, A. ; Li, Y. ; Ponzio, C.A.M. ; Loon, J.J.A. van; Weldegergis, B.T. ; Dicke, M. - \ 2012
    Oikos 121 (2012). - ISSN 0030-1299 - p. 1923 - 1934.
    phytophagous insects - oviposition behavior - salicylic-acid - jasmonic acid - pierid butterflies - battus-philenor - geometrid moth - egg load - preference - performance
    Evolutionary ecological theory predicts that among insect herbivores ‘mothers know best’ when selecting a plant to deposit their eggs. Host-plant selection is usually studied for the adult stage exclusively, although mothers have not always been reported to know best. Here, we investigate the host-plant selection behaviour of caterpillars, which are considered to be completely dependent on their mothers’ choices. We use a system that offers a biologically relevant framework to compare the degree of participation of adults and juveniles in host-plant selection. Our results show that neonate Pieris brassicae caterpillars can actively discriminate between conspecific Brassica oleracea plants with or without aphid (Brevicoryne brassicae) infestation. The caterpillars prefer aphid-infested plants on which their performance is significantly better, while their mothers, the female butterflies, did not discriminate. We compared caterpillar preferences of individuals released individually or in groups, because P. brassicae is a gregarious species. We found that the strength of the preference for aphid-infested plants was not affected by the degree of grouping. Caterpillar choices were made before contact with the plants, indicating that plant odours were used for orientation. However, the composition of the volatile blends emitted by plants with and without aphids did not show strong differences. Similarly, like with aphid-infested plants, plants treated with salicylic acid (SA) were also preferred by neonates over untreated control, indicating that the infestation by aphids may have rendered the plants more attractive to the neonates via changes related to interference with JA-signaling. The main parasitoid of the caterpillars did not discriminate between plants with hosts in the presence or absence of aphids, showing that top–down forces do not influence the relative suitability of the different food sources for the caterpillars. These data are discussed in the context of mothers and offspring having both important, but different roles in the process of host-plant selection. Butterflies may select the plant species patch, while their offspring adjust and/or update the choices of their mothers at the local scale, within the micro-habitat selected by the adult.
    Metabolic and transcriptomic changes induced in Arabidopsis by the rhizobacterium Pseudomonas fluorescens SS101
    Mortel, J.E. van de; Vos, R.C.H. de; Dekkers, E. ; Pineda, A. ; Guillod, L. ; Bouwmeester, K. ; Loon, J.J.A. van; Dicke, M. ; Raaijmakers, J.M. - \ 2012
    Plant Physiology 160 (2012)4. - ISSN 0032-0889 - p. 2173 - 2188.
    induced systemic resistance - growth-promoting rhizobacteria - tobacco necrosis virus - syringae pv. tomato - salicylic-acid - acquired-resistance - aeruginosa 7nsk2 - gene-expression - beneficial microbes - disease resistance
    Systemic resistance induced in plants by nonpathogenic rhizobacteria is typically effective against multiple pathogens. Here, we show that root-colonizing Pseudomonas fluorescens strain SS101 (Pf.SS101) enhanced resistance in Arabidopsis (Arabidopsis thaliana) against several bacterial pathogens, including Pseudomonas syringae pv tomato (Pst) and the insect pest Spodoptera exigua. Transcriptomic analysis and bioassays with specific Arabidopsis mutants revealed that, unlike many other rhizobacteria, the Pf.SS101-induced resistance response to Pst is dependent on salicylic acid signaling and not on jasmonic acid and ethylene signaling. Genome-wide transcriptomic and untargeted metabolomic analyses showed that in roots and leaves of Arabidopsis plants treated with Pf.SS101, approximately 1,910 genes and 50 metabolites were differentially regulated relative to untreated plants. Integration of both sets of “omics” data pointed to a prominent role of camalexin and glucosinolates in the Pf.SS101-induced resistance response. Subsequent bioassays with seven Arabidopsis mutants (myb51, cyp79B2cyp79B3, cyp81F2, pen2, cyp71A12, cyp71A13, and myb28myb29) disrupted in the biosynthesis pathways for these plant secondary metabolites showed that camalexin and glucosinolates are indeed required for the induction of Pst resistance by Pf.SS101. Also for the insect S. exigua, the indolic glucosinolates appeared to play a role in the Pf.SS101-induced resistance response. This study provides, to our knowledge for the first time, insight into the substantial biochemical and temporal transcriptional changes in Arabidopsis associated with the salicylic acid-dependent resistance response induced by specific rhizobacteria.
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