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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    Plant responses to insect egg deposition
    Hilker, M. ; Fatouros, N.E. - \ 2015
    Annual Review of Entomology 60 (2015). - ISSN 0066-4170 - p. 493 - 515.
    sogatella-furcifera horvath - elm leaf beetle - parasitoid anagrus-nilaparvatae - medfly ceratitis-capitata - oryza-sativa l. - defense responses - pieris-brassicae - host location - phytophagous insects - ovicidal substance
    Plants can respond to insect egg deposition and thus resist attack by herbivorous insects from the beginning of the attack, egg deposition. We review ecological effects of plant responses to insect eggs and differentiate between egg-induced plant defenses that directly harm the eggs and indirect defenses that involve egg parasitoids. Furthermore, we discuss the ability of plants to take insect eggs as warning signals; the eggs indicate future larval feeding damage and trigger plant changes that either directly impair larval performance or attract enemies of the larvae. We address the questions of how egg-associated cues elicit plant defenses, how the information that eggs have been laid is transmitted within a plant, and which molecular and chemical plant responses are induced by egg deposition. Finally, we highlight evolutionary aspects of the interactions between plants and insect eggs and ask how the herbivorous insect copes with egg-induced plant defenses and may avoid them by counteradaptations.
    High-throughput phenotyping of plant resistance to aphids by automated video tracking
    Kloth, K.J. ; Broeke, C.J.M. ten; Thoen, H.P.M. ; Hanhart-van den Brink, M. ; Wiegers, G.L. ; Krips, O.E. ; Noldus, L.P.J.J. ; Dicke, M. ; Jongsma, M.A. - \ 2015
    Plant Methods 11 (2015). - ISSN 1746-4811 - 14 p.
    green peach aphid - nasonovia-ribisnigri - glucosinolate accumulation - signaling pathways - defense responses - feeding-behavior - myzus-persicae - lettuce aphid - arabidopsis - herbivores
    Background: Piercing-sucking insects are major vectors of plant viruses causing significant yield losses in crops.Functional genomics of plant resistance to these insects would greatly benefit from the availability of highthroughput, quantitative phenotyping methods. Results: We have developed an automated video tracking platform that quantifies aphid feeding behaviour on leaf discs to assess the level of plant resistance. Through the analysis of aphid movement, the start and duration of plant penetrations by aphids were estimated. As a case study, video tracking confirmed the near-complete resistance of lettuce cultivar ‘Corbana’ against Nasonovia ribisnigri (Mosely), biotype Nr:0, and revealed quantitative resistance in Arabidopsis accession Co-2 against Myzus persicae (Sulzer). The video tracking platform was benchmarked against Electrical Penetration Graph (EPG) recordings and aphid population development assays. The use of leaf discs instead of intact plants reduced the intensity of the resistance effect in video tracking, but sufficiently replicated experiments resulted in similar conclusions as EPG recordings and aphid population assays. One video tracking platform could screen 100 samples in parallel. Conclusions: Automated video tracking can be used to screen large plant populations for resistance to aphids and other piercing-sucking insects.
    A novel approach for multi-domain and multi-gene famliy identification provides insights into evolutionary dynamics of disease resistance genes in core eudicot plants
    Hofberger, J.A. ; Zhou, B. ; Tang, H. ; Jones, J. ; Schranz, M.E. - \ 2014
    BMC Genomics 15 (2014). - ISSN 1471-2164
    genome-wide analysis - nb-arc domain - arabidopsis-thaliana - whole-genome - draft genome - phylogenetic analysis - triggered immunity - mildew resistance - defense responses - encoding genes
    Background Recent advances in DNA sequencing techniques resulted in more than forty sequenced plant genomes representing a diverse set of taxa of agricultural, energy, medicinal and ecological importance. However, gene family curation is often only inferred from DNA sequence homology and lacks insights into evolutionary processes contributing to gene family dynamics. In a comparative genomics framework, we integrated multiple lines of evidence provided by gene synteny, sequence homology and protein-based Hidden Markov Modelling to extract homologous super-clusters composed of multi-domain resistance (R)-proteins of the NB-LRR type (for NUCLEOTIDE BINDING/LEUCINE-RICH REPEATS), that are involved in plant innate immunity. Results To assess the diversity of R-proteins within and between species, we screened twelve eudicot plant genomes including six major crops and found a total of 2,363 NB-LRR genes. Our curated R-proteins set shows a 50% average for tandem duplicates and a 22% fraction of gene copies retained from ancient polyploidy events (ohnologs). We provide evidence for strong positive selection acting on all identified genes and show significant differences in molecular evolution rates (Ka/Ks-ratio) among tandem- (mean = 1.59), ohnolog (mean = 1.36) and singleton (mean = 1.22) R-gene duplicates. To foster the process of gene-edited plant breeding, we report species-specific presence/absence of all 140 NB-LRR genes present in the model plant Arabidopsis and describe four distinct clusters of NB-LRR "gatekeeper" loci sharing syntenic orthologs across all analyzed genomes. Conclusion By curating a near-complete set of multi-domain R-protein clusters in an eudicot-wide scale, our analysis offers significant insight into evolutionary dynamics underlying diversification of the plant innate immune system. Furthermore, our methods provide a blueprint for future efforts to identify and more rapidly clone functional NB-LRR genes from any plant species.
    Phytohormone mediation of interactions between herbivores and plant pathogens
    Lazebnik, J. ; Frago, E. ; Dicke, M. ; Loon, J.J.A. van - \ 2014
    Journal of Chemical Ecology 40 (2014)7. - ISSN 0098-0331 - p. 730 - 741.
    systemic acquired-resistance - generalist insect herbivores - white-backed planthopper - rice blast fungus - defense responses - multitrophic interactions - necrotrophic pathogens - arabidopsis resistance - pseudomonas-syringae - aphid interactions
    Induced plant defenses against either pathogens or herbivore attackers are regulated by phytohormones. These phytohormones are increasingly recognized as important mediators of interactions between organisms associated with plants. In this review, we discuss the role of plant defense hormones in sequential tri-partite interactions among plants, pathogenic microbes, and herbivorous insects, based on the most recent literature. We discuss the importance of pathogen trophic strategy in the interaction with herbivores that exhibit different feeding modes. Plant resistance mechanisms also affect plant quality in future interactions with attackers. We discuss exemplary evidence for the hypotheses that (i) biotrophic pathogens can facilitate chewing herbivores, unless plants exhibit effector-triggered immunity, but (ii) facilitate or inhibit phloem feeders. (iii) Necrotrophic pathogens, on the other hand, can inhibit both phloem feeders and chewers. We also propose herbivore feeding mode as predictor of effects on pathogens of different trophic strategies, providing evidence for the hypotheses that (iv) phloem feeders inhibit pathogen attack by increasing SA induction, whereas (v) chewing herbivores tend not to affect necrotrophic pathogens, while they may either inhibit or facilitate biotrophic pathogens. Putting these hypotheses to the test will increase our understanding of phytohormonal regulation of plant defense to sequential attack by plant pathogens and insect herbivores. This will provide valuable insight into plant-mediated ecological interactions among members of the plant-associated community.
    Ecology of plant volatiles: taking a plant community perspective
    Pierik, R. ; Ballaré, C.L. ; Dicke, M. - \ 2014
    Plant, Cell & Environment 37 (2014)8. - ISSN 0140-7791 - p. 1845 - 1853.
    shade-avoidance - nicotiana-attenuata - neighbor detection - methyl jasmonate - associational resistance - arabidopsis-thaliana - defense responses - natural enemies - predatory mites - canopy light
    Although plants are sessile organisms, they can modulate their phenotype so as to cope with environmental stresses such as herbivore attack and competition with neighbouring plants. Plant-produced volatile compounds mediate various aspects of plant defence. The emission of volatiles has costs and benefits. Research on the role of plant volatiles in defence has focused primarily on the responses of individual plants. However, in nature, plants rarely occur as isolated individuals but are members of plant communities where they compete for resources and exchange information with other plants. In this review, we address the effects of neighbouring plants on plant volatile-mediated defences. We will outline the various roles of volatile compounds in the interactions between plants and other organisms, address the mechanisms of plant neighbour perception in plant communities, and discuss how neighbour detection and volatile signalling are interconnected. Finally, we will outline the most urgent questions to be addressed in the future.
    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.
    Dynamic hydrolase activities precede hypersensitive tissue collapse in tomato seedlings
    Sueldo, D. ; Ali, A. ; Misas-Villamil, J. ; Colby, T. ; Tameling, W.I.L. ; Joosten, M.H.A.J. ; Hoorn, R. van der - \ 2014
    New Phytologist 203 (2014)3. - ISSN 0028-646X - p. 913 - 925.
    programmed cell-death - vacuolar processing enzyme - pathogenesis-related proteins - disease resistance - cysteine proteases - defense responses - plant-pathogen - gene-expression - arabidopsis - activation
    Hydrolases such as subtilases, vacuolar processing enzymes (VPEs) and the proteasome play important roles during plant programmed cell death (PCD). We investigated hydrolase activities during PCD using activity-based protein profiling (ABPP), which displays the active proteome using probes that react covalently with the active site of proteins. We employed tomato (Solanum lycopersicum) seedlings undergoing synchronized hypersensitive cell death by co-expressing the avirulence protein Avr4 from Cladosporium fulvum and the tomato resistance protein Cf-4. Cell death is blocked in seedlings grown at high temperature and humidity, and is synchronously induced by decreasing temperature and humidity. ABPP revealed that VPEs and the proteasome are not differentially active, but that activities of papain-like cysteine proteases and serine hydrolases, including Hsr203 and P69B, increase before hypersensitive tissue collapse, whereas the activity of a carboxypeptidase-like enzyme is reduced. Similar dynamics were observed for these enzymes in the apoplast of tomato challenged with C. fulvum. Unexpectedly, these challenged plants also displayed novel isoforms of secreted putative VPEs. In the absence of tissue collapse at high humidity, the hydrolase activity profile is already altered completely, demonstrating that changes in hydrolase activities precede hypersensitive tissue collapse.
    Intra-specific variation in wild Brassica oleracea for aphid-induced plant responses and consequences for caterpillar-parasitoid interactions
    Li, Y. ; Dicke, M. ; Harvey, J.A. ; Gols, R. - \ 2014
    Oecologia 174 (2014)3. - ISSN 0029-8549 - p. 853 - 862.
    phloem-feeding insect - induced resistance - defense responses - interspecific interactions - multitrophic interactions - arabidopsis-thaliana - phytophagous insects - nicotiana-attenuata - jasmonic acid - host plants
    Herbivore-induced plant responses not only influence the initiating attackers, but also other herbivores feeding on the same host plant simultaneously or at a different time. Insects belonging to different feeding guilds are known to induce different responses in the host plant. Changes in a plant's phenotype not only affect its interactions with herbivores but also with organisms higher in the food chain. Previous work has shown that feeding by a phloem-feeding aphid on a cabbage cultivar facilitates the interaction with a chewing herbivore and its endoparasitoid. Here we study genetic variation in a plant's response to aphid feeding using plants originating from three wild Brassica oleracea populations that are known to differ in constitutive and inducible secondary chemistry. We compared the performance of two different chewing herbivore species, Plutella xylostella and M. brassicae, and their larval endoparasitoids Diadegma semiclausum and M. mediator, respectively, on plants that had been infested with aphids (Brevicoryne brassicae) for 1 week. Remarkably, early infestation with B. brassicae enhanced the performance of the specialist P. xylostella and its parasitoid D. semiclausum, but did not affect that of the generalist M. brassicae, nor its parasitoid M. mediator. Performance of the two herbivore-parasitoid interactions also varied among the cabbage populations and the effect of aphid infestation marginally differed among the three populations. Thus, the effect of aphid infestation on the performance of subsequent attackers is species specific, which may have concomitant consequences for the assembly of insect communities that are naturally associated with these plants.
    Modulation of flavonoid metabolites in Arabidopsis thaliana through overexpression of the MYB75 transcription factor: role of kaempferol-3,7-dirhamnoside in resistance to the specialist insect herbivore Pieris brassicae
    Onkokesung, N. ; Reichelt, M. ; Doorn, A. van; Schuurink, R.C. ; Loon, J.J.A. van; Dicke, M. - \ 2014
    Journal of Experimental Botany 65 (2014)8. - ISSN 0022-0957 - p. 2203 - 2217.
    plant-responses - anthocyanin accumulation - lepidopteran herbivores - coexpression analysis - biosynthetic-pathway - indole-glucosinolate - functional genomics - signaling pathways - defense responses - complex
    Anthocyanins and flavonols are secondary metabolites that can function in plant defence against herbivores. In Arabidopsis thaliana, anthocyanin and flavonol biosynthesis are regulated by MYB transcription factors. Overexpression of MYB75 (oxMYB75) in Arabidopsis results in increasing anthocyanin and flavonol levels which enhances plant resistance to generalist caterpillars. However, how these metabolites affect specialist herbivores has remained unknown. Performance of a specialist aphid (Brevicoryne brassicae) was unaffected after feeding on oxMYB75 plants, whereas a specialist caterpillar (Pieris brassicae) gained significantly higher body mass when feeding on this plant. An increase in anthocyanin and total flavonol glycoside levels correlated negatively with the body mass of caterpillars fed on oxMYB75 plants. However, a significant reduction of kaempferol-3,7-dirhamnoside (KRR) corresponded to an increased susceptibility of oxMYB75 plants to caterpillar feeding. Pieris brassicae caterpillars also grew less on an artificial diet containing KRR or on oxMYB75 plants that were exogenously treated with KRR, supporting KRR's function in direct defence against this specialist caterpillar. The results show that enhancing the activity of the anthocyanin pathway in oxMYB75 plants results in re-channelling of quercetin/kaempferol metabolites which has a negative effect on the accumulation of KRR, a novel defensive metabolite against a specialist caterpillar.
    Down-regulation of acetolactate synthase compromises OI-1- mediated resistance to powdery mildew in tomato
    Gao, D. ; Huibers, R.P. ; Loonen, A.E.H.M. ; Visser, R.G.F. ; Wolters, A.M.A. ; Bai, Y. - \ 2014
    BMC Plant Biology 14 (2014). - ISSN 1471-2229 - 11 p.
    glutamate-dehydrogenase gene - acetohydroxyacid synthase - monogenic-resistance - defense responses - nicotiana-tabacum - ol-genes - arabidopsis - plants - inhibition - biosynthesis
    Background - In a cDNA-AFLP analysis comparing transcript levels between powdery mildew (Oidium neolycopersici)-susceptible tomato cultivar Moneymaker (MM) and near isogenic lines (NILs) carrying resistance gene Ol-1 or Ol-4, a transcript-derived fragment (TDF) M11E69-195 was found to be present in NIL-Ol-1 but absent in MM and NIL-Ol-4. This TDF shows homology to acetolactate synthase (ALS). ALS is a key enzyme in the biosynthesis of branched-chain amino acids valine, leucine and isoleucine, and it is also a target of commercial herbicides. Results - Three ALS homologs ALS1, ALS2, ALS3 were identified in the tomato genome sequence. ALS1 and ALS2 show high similarity, whereas ALS3 is more divergent. Transient silencing of both ALS1 and ALS2 in NIL-Ol-1 by virus-induced gene silencing (VIGS) resulted in chlorotic leaf areas that showed increased susceptibility to O. neolycopersici (On). VIGS results were confirmed by stable transformation of NIL-Ol-1 using an RNAi construct targeting both ALS1 and ALS2. In contrast, silencing of the three ALS genes individually by RNAi constructs did not compromise the resistance of NIL-Ol-1. Application of the herbicide chlorsulfuron to NIL-Ol-1 mimicked the VIGS phenotype and caused loss of its resistance to On. Susceptible MM and On-resistant line NIL-Ol-4 carrying a nucleotide binding site and leucine rich repeat (NB-LRR) resistance gene were also treated with chlorsulfuron. Neither the susceptibility of MM nor the resistance of NIL-Ol-4 was affected. Conclusions - ALS is neither involved in basal defense, nor in resistance conferred by NB-LRR type resistance genes. Instead, it is specifically involved in Ol-1-mediated resistance to tomato powdery mildew, suggesting that ALS-induced change in amino acid homeostasis is important for resistance conferred by Ol-1.
    Two for all: receptor-associated kinases SOBIR1 and BAK1
    Liebrand, T.W.H. ; Burg, H.A. van den; Joosten, M.H.A.J. - \ 2014
    Trends in Plant Science 19 (2014)2. - ISSN 1360-1385 - p. 123 - 132.
    plant innate immunity - pattern-recognition receptors - ethylene-inducing xylanase - arabidopsis-thaliana - cladosporium-fulvum - defense responses - cell-death - signaling pathways - plasma-membrane - protein-kinase
    Leucine-rich repeat-receptor-like proteins (LRR-RLPs) are ubiquitous cell surface receptors lacking a cytoplasmic signalling domain. For most of these LRR-RLPs, it remained enigmatic how they activate cellular responses upon ligand perception. Recently, the LRR-receptor-like kinase (LRR-RLK) SUPPRESSOR OF BIR1-1 (SOBIR1) was shown to be essential for triggering defence responses by certain LRR-RLPs that act as immune receptors. In addition to SOBIR1, the regulatory LRR-RLK BRI1-ASSOCIATED KINASE-1 (BAK1) is also required for LRR-RLP function. Here, we compare the roles of SOBIR1 and BAK1 as regulatory LRR-RLKs in immunity and development. BAK1 has a general regulatory role in plasma membrane-associated receptor complexes comprising LRR-RLPs and/or LRR-RLKs. By contrast, SOBIR1 appears to be specifically required for the function of receptor complexes containing LRR-RLPs.
    Involvement of phospholipase D-related signal transduction in chemical-induced programmed cell death in tomato cell cultures
    Iakimova, E.T. ; Michaeli, R. ; Woltering, E.J. - \ 2013
    Protoplasma 250 (2013)5. - ISSN 0033-183X - p. 1169 - 1183.
    phosphatidic-acid accumulation - g-protein activation - suspension cells - plasma-membrane - nitric-oxide - chlamydomonas-reinhardtii - arabidopsis-thaliana - aerenchyma formation - disease resistance - defense responses
    Phospholipase D (PLD) and its product phosphatidic acid (PA) are incorporated in a complex metabolic network in which the individual PLD isoforms are suggested to regulate specific developmental and stress responses, including plant programmed cell death (PCD). Despite the accumulating knowledge, the mechanisms through which PLD/PA operate during PCD are still poorly understood. In this work, the role of PLD alpha 1 in PCD and the associated caspase-like proteolysis, ethylene and hydrogen peroxide (H2O2) synthesis in tomato suspension cells was studied. Wild-type (WT) and PLD alpha 1-silenced cell lines were exposed to the cell death-inducing chemicals camptothecin (CPT), fumonisin B1 (FB1) and CdSO4. A range of caspase inhibitors effectively suppressed CPT-induced PCD in WT cells, but failed to alleviate cell death in PLD alpha 1-deficient cells. Compared to WT, in CPT-treated PLD alpha 1 mutant cells, reduced cell death and decreased production of H2O2 were observed. Application of ethylene significantly enhanced CPT-induced cell death both in WT and PLD alpha 1 mutants. Treatments with the PA derivative lyso-phosphatidic acid and mastoparan (agonist of PLD/PLC signalling downstream of G proteins) caused severe cell death. Inhibitors, specific to PLD and PLC, remarkably decreased the chemical-induced cell death. Taken together with our previous findings, the results suggest that PLD alpha 1 contributes to caspase-like-dependent cell death possibly communicated through PA, reactive oxygen species and ethylene. The dead cells expressed morphological features of PCD such as protoplast shrinkage and nucleus compaction. The presented findings reveal novel elements of PLD/PA-mediated cell death response and suggest that PLD alpha 1 is an important factor in chemical-induced PCD signal transduction.
    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.
    Phenotypic plasticity of plant response to herbivore eggs: effects on resistance to caterpillars and plant development
    Pashalidou, F.G. ; Lucas-Barbosa, D. ; Loon, J.J.A. van; Dicke, M. ; Fatouros, N.E. - \ 2013
    Ecology 94 (2013)3. - ISSN 0012-9658 - p. 702 - 713.
    insect herbivores - pieris-brassicae - specialist herbivores - arabidopsis-thaliana - mamestra-brassicae - defense responses - bunias orientalis - chemical defense - pinus-sylvestris - getting ready
    Herbivory induces direct resistance responses in plants that negatively affect subsequently colonizing herbivores. Moreover, eggs of herbivorous insects can also activate plant resistance, which in some cases prevents hatching larvae from feeding. Until now, plant-mediated effects of eggs on subsequent herbivory, and the specificity of such responses, have remained poorly understood. We studied the specificity and effects of plant resistance induced by herbivore egg deposition against lepidopteran larvae of species with different dietary breadths, feeding on a wild annual plant, the crucifer Brassica nigra. We examined whether this plant-mediated response affects the growth of caterpillars of a specialist (Pieris brassicae) that feeds on B. nigra leaves and flowers, and a generalist (Mamestra brassicae) that rarely attacks this wild crucifer. We measured growth rates of neonate larvae to the end of their second instar after the larvae had hatched on plants exposed to eggs vs. plants without eggs, under laboratory and semi-field conditions. Moreover, we studied the effects of egg deposition by the two herbivore species on plant height and flowering rate before and after larval hatching. Larvae of both herbivore species that developed on plants previously infested with eggs of the specialist butterfly P. brassicae gained less mass compared with larvae that developed on egg-free plants. Plants exposed to butterfly eggs showed accelerated plant growth and flowering compared to egg-free plants. Egg deposition by the generalist moth M. brassicae, in contrast, had no effect on subsequent performance by either herbivore species, or on plant development. Our results demonstrate that B. nigra plants respond differently to eggs of two herbivore species in terms of plant development and induced resistance to caterpillar attack. For this annual crucifer, the retardation of caterpillar growth in response to deposition of eggs by P. brassicae in combination with enhanced growth and flowering likely result in reproductive assurance, after being exposed to eggs from an herbivore whose larvae rapidly reduce the plant's reproductive potential through florivory.
    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.
    Ve1-mediated resistance against Verticillium does not involve a hypersensitive response in Arabidopsis
    Zhang, Z. ; Esse, H.P. van; Damme, M. van; Fradin, E.F. ; Liu, Chun-Ming ; Thomma, B.P.H.J. - \ 2013
    Molecular Plant Pathology 14 (2013)7. - ISSN 1464-6722 - p. 719 - 727.
    ethylene-inducing xylanase - receptor-like proteins - gated ion-channel - disease resistance - rhynchosporium-secalis - functional-analysis - defense responses - gene family - tomato ve1 - cell-death
    The recognition of pathogen effectors by plant immune receptors leads to the activation of immune responses that often include a hypersensitive response (HR): rapid and localized host cell death surrounding the site of attempted pathogen ingress. We have demonstrated previously that the recognition of the Verticillium dahliae effector protein Ave1 by the tomato immune receptor Ve1 triggers an HR in tomato and tobacco. Furthermore, we have demonstrated that tomato Ve1 provides Verticillium resistance in Arabidopsis upon Ave1 recognition. In this study, we investigated whether the co-expression of Ve1 and Ave1 in Arabidopsis results in an HR, which could facilitate a forward genetics screen. Surprisingly, we found that the co-expression of Ve1 and Ave1 does not induce an HR in Arabidopsis. These results suggest that an HR may occur as a consequence of Ve1/Ave1-induced immune signalling in tomato and tobacco, but is not absolutely required for Verticillium resistance.
    Non-pathogenic rhizobacteria interfere with the attraction of parasitoids to aphid-induced plant volatiles via jasmonic acid signalling.
    Pineda, A. ; Soler Gamborena, R. ; Weldegergis, B.T. ; Shimwela, M.M. ; Loon, J.J.A. van; Dicke, M. - \ 2013
    Plant, Cell & Environment 36 (2013)2. - ISSN 0140-7791 - p. 393 - 404.
    brevicoryne-brassicae attack - herbivore-induced volatiles - phloem-feeding insects - arabidopsis-thaliana - mycorrhizal fungi - myzus-persicae - multitrophic interactions - mediated interactions - systemic resistance - defense responses
    Beneficial soil-borne microbes, such as mycorrhizal fungi or rhizobacteria, can affect the interactions of plants with aboveground insects at several trophic levels. While the mechanisms of interactions with herbivorous insects, that is, the second trophic level, are starting to be understood, it remains unknown how plants mediate the interactions between soil microbes and carnivorous insects, that is, the third trophic level. Using Arabidopsis thaliana Col-0 and the aphid Myzus persicae, we evaluate here the underlying mechanisms involved in the plant-mediated interaction between the non-pathogenic rhizobacterium Pseudomonas fluorescens and the parasitoid Diaeretiella rapae, by combining ecological, chemical and molecular approaches. Rhizobacterial colonization modifies the composition of the blend of herbivore-induced plant volatiles. The volatile blend from rhizobacteria-treated aphid-infested plants is less attractive to an aphid parasitoid, in terms of both olfactory preference behaviour and oviposition, than the volatile blend from aphid-infested plants without rhizobacteria. Importantly, the effect of rhizobacteria on both the emission of herbivore-induced volatiles and parasitoid response to aphid-infested plants is lost in an Arabidopsis mutant (aos/dde2-2) that is impaired in jasmonic acid production. By modifying the blend of herbivore-induced plant volatiles that depend on the jasmonic acid-signalling pathway, root-colonizing microbes interfere with the attraction of parasitoids of leaf herbivores.
    Seed and leaf treatments with natural compounds to induce resistance against Peronospora parasitica in Brassica oleracea
    Wolf, J.M. van der; Michta, A. ; Zouwen, P.S. van der; Boer, W.J. de; Davelaar, E. ; Stevens, L.H. - \ 2012
    Crop Protection 35 (2012). - ISSN 0261-2194 - p. 78 - 84.
    systemic acquired-resistance - induced disease resistance - defense responses - fusarium-wilt - downy mildew - damping-off - plants - protection - cucumber - growth
    Seed and leaf treatments with natural compounds having a low risk profile (LRP) were evaluated for their potential to induce resistance in cabbage plants (Brassica oleracea) against Peronospora parasitica, causal organism of downy mildew. The selection of 34 LRP compounds comprised micronutrients, organic compounds such as proline, riboflavin, oligogalacturonides, aminolignosulfonates, bacterial lipopolysaccharides, and bacterial and fungal extracts. Treatments with the synthetic chemical inducers 2,6-dichloroisonicotinic acid (INA), d,l-ß-aminobutyric acid, salicylic acid, benzothiadiazole and the fungicide Previcur™ were included as controls. After seed treatment a maximum reduction of 27% diseased leaf area was found with an extract of a Lysobacter strain, compared to a reduction of 99% for INA, the most effective synthetic inducer. Seed treatments with extracts of Pectobacterium carotovorum subsp. carotovorum, Bacillus macerans, Pseudomonas syringae, Streptomyces and Xanthomonas campestris strains also reduced downy mildew infection significantly. After leaf treatment, a maximum reduction of 85% was again found with the Lysobacter extract, compared to a reduction of 99% for INA, the most effective synthetic inducer. Leaf treatments with CuSO4 (=1 mM), MnCl2 (=10 mM), K2HPO4 (100 mM), and extracts of P. syringae, P. carotovorum subsp. carotovorum, Streptomyces, X. campestris and B. macerans strains also reduced the diseased leaf area, but CuSO4 was highly phytotoxic. For seed and leaf treatments with Lysobacter extract, proline, MnCl2 and INA the effect on the induction of chitinase and glucanase activity was tested, using two pathogenesis-related proteins as markers for induced resistance. For seed treatments only INA and for leaf treatments INA, proline and MnCl2 treatments resulted in increased activity of both enzymes. The rate of enzyme activity induced by INA was dependent on the time seeds were exposed to the compound. Highlights ¿ Seed treatments with isonicotinic acid protects Brassica seedlings from Peronospora infections. ¿ Treatments of seedlings with extracts of Lysobacter protects against Peronospora infections. ¿ Effect of seed treatments is dependent on the time of incubation with the elicitor
    Rhizobacteria modify plant–aphid interactions: a case of induced systemic susceptibility
    Pineda, A. ; Zheng, S.J. ; Loon, J.J.A. van; Dicke, M. - \ 2012
    Plant Biology 14 (2012)Suppl. s1. - ISSN 1435-8603 - p. 83 - 90.
    gene-expression - arabidopsis-thaliana - brevicoryne-brassicae - signaling pathways - induced resistance - insect herbivores - abscisic-acid - disease resistance - defense responses - myzus-persicae
    Beneficial microbes, such as plant growth-promoting rhizobacteria and mycorrhizal fungi, may have a plant-mediated effect on insects aboveground. The plant growth-promoting rhizobacterium Pseudomonas fluorescens can induce systemic resistance in Arabidopsis thaliana against several microbial pathogens and chewing insects. However, the plant-mediated effect of these beneficial microbes on phloem-feeding insects is not well understood. Using Arabidopsis as a model, we here report that P. fluorescens has a positive effect on the performance (weight gain and intrinsic rate of increase) of the generalist aphid Myzus persicae, while no effect was recorded on the crucifer specialist aphid Brevicoryne brassicae. Additionally, transcriptional analyses of selected marker genes revealed that in the plant–microbe interaction with M. persicae, rhizobacteria (i) prime the plant for enhanced expression of LOX2, a gene involved in the jasmonic acid (JA)-regulated defence pathway, and (ii) suppress the expression of ABA1, a gene involved in the abscisic acid (ABA) signalling pathway, at several time points. In contrast, almost no effect of the plant–microbe interaction with B. brassicae was found at the transcriptional level. This study presents the first data on rhizobacteria-induced systemic susceptibility to an herbivorous insect, supporting the pattern proposed for other belowground beneficial microbes and aboveground phloem feeders. Moreover, we provide further evidence that at the transcript level, soil-borne microbes modify plant–aphid interactions.
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