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The positively-selected effector MiL648 of the root-knot nematode Meloidogyne incognita plays a role in tomato infections
Verhoeven, Ava ; Put, Sanne ; Slootweg, E.J. ; Raaij, D.R. van; Overmars, H.A. ; Goverse, A. ; Smant, G. - \ 2018
Insight in the molecular basis of virulence can help us to identify new and more durable sources of resistance to the root-knot nematode Meloidogyne incognita in tomato. Recently, we identified the effector MiL648 by applying a genome-wide scan for positively selected secreted proteins. To acquire a better understanding of the function of MiL648, we are currently functionally characterising the protein in plants using host-induced gene silencing. Several in planta targets of the putative effector have now been found by a yeast-two-hybrid screening and interactions were checked using Co-IPs. To identify the role of the host targets in the infection process, homologs of the host targets were knocked out in Arabidopsis.
The effect of storage time and temperature on the population dynamics and vitality of Meloidogyne chitwoodi in potato tubers
Teklu, Misghina G. ; Schomaker, Corrie H. ; Been, Thomas H. - \ 2018
Nematology 20 (2018)4. - ISSN 1388-5545 - p. 373 - 385.
Hatching curves - infectivity - quarantine pest - root-knot nematode - tuber peel - tuber storage - viability
The population densities of Meloidogyne chitwoodi in potato tubers stored at 4, 8 and 12°C after 0, 60, 120, 180 and 240 days of storage were assessed. Compared to day 0, storage temperatures of 4 and 8°C reduced population densities to 9 and 35%, respectively, after 240 days of storage, while nematode numbers in tubers stored at 12°C increased 2.5 times. The maximum hatching rate of nematodes from tubers stored at 8 and 12°C increased linearly with storage time. At 4°C it remained constant. The time required for the hatching process to reach the maximum number of second-stage juveniles (J2) decreased with increasing storage temperature. Recovered juveniles of M. chitwoodi from tubers after 180 and 240 days of storage at all three temperatures were still infective and able to multiply on 'Desiree' with estimates of the maximum multiplication rate (a) and the maximum population density (M) of 63.6 and 70.8 J2 (g dry soil)-1, respectively.
The role of PLETHORA during gall formation of the root-knot nematode Meloidogyne incognita in Arabidopsis thaliana
Oosterbeek, Matthijs ; Overmars, H.A. ; Scheres, B.J.G. ; Bakker, J. ; Goverse, A. - \ 2018
Functional characterisation of the positively-selected effector MiL648 of the root-knot nematode Meloidogyne incognita
Verhoeven, Ava ; Prins, J.C.P. ; Finkers-Tomczak, A.M. ; Slootweg, E.J. ; Varossieau, K. ; Raaij, D.R. van; Goverse, A. ; Smant, G. - \ 2018
Genome-wide association mapping of the architecture of susceptibility to the root-knot nematode Meloidogyne incognita in Arabidopsis thaliana
Warmerdam, S. ; Sterken, M.G. ; Schaik, C.C. van; Oortwijn, M.E.P. ; Sukarta, O.C.A. ; Lozano Torres, J.L. ; Dicke, M. ; Helder, J. ; Kammenga, J.E. ; Goverse, A. ; Bakker, J. ; Smant, G. - \ 2018
Functional characterization of the positively-selected effector MiL648 of the root-knot nematode Meloidogyne incognita
Verhoeven, Ava - \ 2018
Genome-wide association mapping of the architecture of susceptibility to the root-knot nematode Meloidogyne incognita in Arabidopsis thaliana
Warmerdam, Sonja ; Sterken, Mark G. ; Schaik, Casper van; Oortwijn, Marian E.P. ; Sukarta, Octavina C.A. ; Lozano-Torres, Jose L. ; Dicke, Marcel ; Helder, Johannes ; Kammenga, Jan E. ; Goverse, Aska ; Bakker, Jaap ; Smant, Geert - \ 2018
New Phytologist 218 (2018)2. - ISSN 0028-646X - p. 724 - 737.
Susceptibility to the root-knot nematode Meloidogyne incognita in plants is thought to be a complex trait based on multiple genes involved in cell differentiation, growth and defence. Previous genetic analyses of susceptibility to M. incognita have mainly focused on segregating dominant resistance genes in crops. It is not known if plants harbour significant genetic variation in susceptibility to M. incognita independent of dominant resistance. To study the genetic architecture of susceptibility to M. incognita, we analysed nematode reproduction on a highly diverse set of 340 natural inbred lines of Arabidopsis thaliana with genome-wide association mapping. We observed a surprisingly large variation in nematode reproduction among these lines. Genome-wide association mapping revealed four quantitative trait loci (QTLs) located on chromosomes 1 and 5 of A. thaliana significantly associated with reproductive success of M. incognita, none of which harbours typical resistance gene homologues. Mutant analysis of three genes located in two QTLs showed that the transcription factor BRASSINAZOLE RESISTANT1 and an F-box family protein may function as (co-)regulators of susceptibility to M. incognita in Arabidopsis.
Our data suggest that breeding for loss-of-susceptibility, based on allelic variants critically involved in nematode feeding, could be used to make crops more resilient to root-knot nematodes.
A new reference genome sequence for genotyping virulence in continental European field populations of Globodera pallida
Holterman, M.H.M. ; Blokhina, T. ; Elsen, S.J.J. van den; Lozano Torres, J.L. ; Smant, G. ; Helder, J. - \ 2017
Plant-parasitic nematodes form an increasingly important problem in agriculture, causing significant crop losses worldwide. The majority of these losses are caused by a small number of species, such as cyst nematodes (e.g., Globodera rostochiensis and G. pallida), root-knot nematodes (Meloidogyne spp.) and stem nematodes (Ditylenchus spp.). With a regulatory ban on most nematicidal agrochemicals, the main method of control at the moment is the use of resistant crop cultivars. However, the current spectrum of nematode resistance genes used in major crops is extremely narrow. Prolonged exposure of field populations to a narrow range of resistance genes can result in the appearance of nematode genotypes with modified virulence characteristics.
To better understand the genetic mechanisms underlying selection for virulence in the potato cyst nematode G. pallida in the Netherlands, we needed to generate a new reference genome. For this, we deliberately chose an old isolate; a population that had not been exposed to potato cultivars harbouring the resistance genes that were most widely used over the past thirty years. We generated a new genome sequence of this G. pallida isolate with PacBio sequencing technology. This resulted in a new genome sequence which consists of significantly fewer and longer contigs than the publicly available genome sequence of this species. An automated procedure was used to create an initial annotation. After a further manual refinement of the annotation with a particular focus on effector families, this genome sequence will serve as a reference for the elucidation of virulence characteristics in G. pallida populations from The Netherlands and surrounding countries.
Genome wide association mapping reveals natural variation in susceptibility in Arabidopsis thaliana to the root-knot nematode Meloidogyne incognita.
Warmerdam, Sonja - \ 2017
Damage-associated responses of the host contribute to defence against cyst nematodes but not root-knot nematodes
Shah, Syed Jehangir ; Anjam, Muhammad Shahzad ; Mendy, Badou ; Anwer, Muhammad Arslan ; Habash, Samer S. ; Lozano-Torres, Jose L. ; Grundler, Florian M.W. ; Siddique, Shahid - \ 2017
Journal of Experimental Botany 68 (2017)21-22. - ISSN 0022-0957 - p. 5949 - 5960.
When nematodes invade and subsequently migrate within plant roots, they generate cell wall fragments (in the form of oligogalacturonides; OGs) that can act as damage-associated molecular patterns and activate host defence responses. However, the molecular mechanisms mediating damage responses in plant–nematode interactions remain unexplored. Here, we characterized the role of a group of cell wall receptor proteins in Arabidopsis, designated as polygalacturonase-inhibiting proteins (PGIPs), during infection with the cyst nematode Heterodera schachtii and the root-knot nematode Meloidogyne incognita. PGIPs are encoded by a family of two genes in Arabidopsis, and are involved in the formation of active OG elicitors. Our results show that PGIP gene expression is strongly induced in response to cyst nematode invasion of roots. Analyses of loss-of-function mutants and overexpression lines revealed that PGIP1 expression attenuates infection of host roots by cyst nematodes, but not root-knot nematodes. The PGIP1-mediated attenuation of cyst nematode infection involves the activation of plant camalexin and indole-glucosinolate pathways. These combined results provide new insights into the molecular mechanisms underlying plant damage perception and response pathways during infection by cyst and root-knot nematodes, and establishes the function of PGIP in plant resistance to cyst nematodes.
Apoplastic venom allergen-like proteins of plant parasitic nematodes modulate the activation of plant innate immunity by cell surface receptors
Wilbers, Ruud - \ 2017
Despite causing considerable damage to host tissue during the onset of parasitism, nematodes establish remarkably persistent infections in both animals and plants. It is thought that an elaborate repertoire of effector proteins in nematode secretions suppresses damage-triggered immune responses of the host. However, the nature and mode of action of most immunomodulatory compounds in nematode secretions are not well understood. Here, we show that venom allergen-like proteins of plant-parasitic nematodes selectively suppress host immunity mediated by surface-localized immune receptors. Venom allergen-like proteins are uniquely conserved in secretions of all animal- and plant-parasitic nematodes studied to date, but their role during the onset of parasitism has thus far remained elusive. Knocking-down the expression of the venom allergen-like protein Gr-VAP1 severely hampered the infectivity of the potato cyst nematode Globodera rostochiensis. By contrast, heterologous expression of Gr-VAP1 and two other venom allergen-like proteins from the beet cyst nematode Heterodera schachtii in plants resulted in the loss of basal immunity to multiple unrelated pathogens. The modulation of basal immunity by ectopic venom allergen-like proteins in Arabidopsis thaliana involved extracellular protease-based host defenses and non-photochemical quenching in chloroplasts. Non-photochemical quenching regulates the initiation of the defense-related programmed cell death, the onset of which was commonly suppressed by venom allergen-like proteins from G. rostochiensis, H. schachtii, and the root-knot nematode Meloidogyne incognita. Surprisingly, these venom allergen-like proteins only affected the programmed cell death mediated by surface-localized immune receptors. Furthermore, the delivery of venom allergen-like proteins into host tissue coincides with the enzymatic breakdown of plant cell walls by migratory nematodes. We therefore conclude that parasitic nematodes most likely utilize venom allergen-like proteins to suppress the activation of defenses by immunogenic breakdown products in damaged host tissue.
Classification of European beech forests : a Gordian Knot?
Willner, Wolfgang ; Jiménez-Alfaro, Borja ; Agrillo, Emiliano ; Biurrun, Idoia ; Campos, Juan Antonio ; Čarni, Andraž ; Casella, Laura ; Csiky, János ; Ćušterevska, Renata ; Didukh, Yakiv P. ; Ewald, Jörg ; Jandt, Ute ; Jansen, Florian ; Kącki, Zygmunt ; Kavgacı, Ali ; Lenoir, Jonathan ; Marinšek, Aleksander ; Onyshchenko, Viktor ; Rodwell, John S. ; Schaminée, Joop H.J. ; Šibík, Jozef ; Škvorc, Željko ; Svenning, Jens Christian ; Tsiripidis, Ioannis ; Turtureanu, Pavel Dan ; Tzonev, Rossen ; Vassilev, Kiril ; Venanzoni, Roberto ; Wohlgemuth, Thomas ; Chytrý, Milan - \ 2017
Applied Vegetation Science 20 (2017)3. - ISSN 1402-2001 - p. 494 - 512.
Beech forest - Europe - Fagetalia sylvaticae - Fagion sylvaticae - Fagus sylvatica - Luzulo-Fagion sylvaticae - Syntaxonomy - TWINSPAN - Vegetation plot database

Questions: What are the main floristic patterns in European beech forests? Which classification at the alliance and suballiance level is the most convincing?. Location: Europe and Asia Minor. Methods: We applied a TWINSPAN classification to a data set of 24 605 relevés covering the whole range of Fagus sylvatica forests and the western part of Fagus orientalis forests. We identified 24 ‘operational phytosociological units’ (OPUs), which were used for further analysis. The position of each OPU along the soil pH and temperature gradient was evaluated using Ellenberg Indicator Values. Fidelity of species to OPUs was calculated using the phi coefficient and constancy ratio. We compared alternative alliance concepts, corresponding to groups of OPUs, in terms of number and frequency of diagnostic species. We also established formal definitions for the various alliance concepts based on comparison of the total cover of the diagnostic species groups, and evaluated alternative geographical subdivisions of beech forests. Results: The first and second division levels of TWINSPAN followed the temperature and soil pH gradients, while lower divisions were mainly geographical. We grouped the 22 OPUs of Fagus sylvatica forests into acidophytic, meso-basiphytic and thermo-basiphytic beech forests, and separated two OPUs of F. orientalis forests. However, a solution with only two ecologically defined alliances of F. sylvatica forests (acidophytic vs basiphytic) was clearly superior with regard to number and frequency of diagnostic species. In contrast, when comparing groupings with three to six geographical alliances of basiphytic beech forests, respectively, we did not find a strongly superior solution. Conclusions: We propose to classify F. sylvatica forests into 15 suballiances – three acidophytic and 12 basiphytic ones. Separating these two groups at alliance or order level was clearly supported by our results. Concerning the grouping of the 12 basiphytic suballiances into ecological or geographical alliances, as advocated by many authors, we failed to find an optimal solution. Therefore, we propose a multi-dimensional classification of basiphytic beech forests, including both ecological and geographical groups as equally valid concepts which may be used alternatively depending on the purpose and context of the classification.

Functional characterization of the positively-selected effector MiL648 of the root-knot nematode Meloidogyne incognita
Verhoeven, Ava ; Prins, J.C.P. ; Finkers-Tomczak, A.M. ; Slootweg, E.J. ; Varossieau, K. ; Raaij, D.R. van; Pomp, H. ; Goverse, A. ; Smant, G. - \ 2017
Genome-wide association mapping reveals natural variation in susceptibility in Arabidopsis thaliana to the root-knot nematode Meloidogyne incognita
Warmerdam, Sonja - \ 2016
Fungal root endophytes of tomato from Kenya and their nematode biocontrol potential
Bogner, C.W. ; Kariuki, George M. ; Elashry, A. ; Sichtermann, Gisela ; Buch, Ann-Katrin ; Mishra, Bagdevi ; Thines, M. ; Grundler, F.M.W. ; Schouten, A. - \ 2016
Mycological Progress 15 (2016). - ISSN 1617-416X
The significance of fungal endophytes in African agriculture, particularly Kenya, has not been well investigated. Therefore, the objective of the present work was isolation, multi-gene phylogenetic characterization and biocontrol assessment of endophytic fungi harbored in tomato roots for nematode infection management. A survey was conducted in five different counties along the central and coastal regions of Kenya to determine the culturable endophytic mycobiota. A total of 76 fungal isolates were obtained and characterized into 40 operational taxonomic units based on the analysis of ITS, β-tubulin and tef1α gene sequence data. Among the fungal isolates recovered, the most prevalent species associated with tomato roots were members of the Fusarium oxysporum and F. solani species complexes. Of the three genes utilized for endophyte characterization, tef1α provided the best resolution. A combination of ITS, β-tubulin and tef1α resulted in a better resolution as compared to single gene analysis. Biotests demonstrated the ability of selected non-pathogenic fungal isolates to successfully reduce nematode penetration and subsequent galling as well as reproduction of the root-knot nematode Meloidogyne incognita. Most Trichoderma asperellum and F. oxysporum species complex isolates reduced root-knot nematode egg densities by 35–46 % as compared to the non-fungal control and other isolates. This study provides first insights into the culturable endophytic mycobiota of tomato roots in Kenya and the potential of some isolates for use against the root-knot nematode M. incognita. The data can serve as a framework for fingerprinting potential beneficial endophytic fungal isolates which are optimized for abiotic and biotic environments and are useful in biocontrol strategies against nematode pests in Kenyan tomato cultivars. This information would therefore provide an alternative or complementary crop protection component.
Targeted vaccination against the bevacizumab binding site on VEGF using 3D-structured peptides elicits efficient antitumor activity
Wentink, Madelon Q. ; Hackeng, Tilman M. ; Tabruyn, Sebastien P. ; Puijk, Wouter C. ; Schwamborn, Klaus ; Altschuh, Daniele ; Meloen, Rob H. ; Schuurman, Teun ; Griffioen, Arjan W. ; Timmerman, Peter - \ 2016
Proceedings of the National Academy of Sciences of the United States of America 113 (2016)44. - ISSN 0027-8424 - p. 12532 - 12537.
Angiogenesis - Immunization - Peptide vaccines - Protein mimicry - VEGF

Therapeutic targeting of the VEGF signaling axis by the VEGFneutralizing monoclonal antibody bevacizumab has clearly demonstrated clinical benefit in cancer patients. To improve this strategy using a polyclonal approach, we developed a vaccine targeting VEGF using 3D-structured peptides that mimic the bevacizumab binding site. An in-depth study on peptide optimization showed that the antigen's 3D structure is essential to achieve neutralizing antibody responses. Peptide 1 adopts a clear secondary, native-like structure, including the typical cysteine-knot fold, as evidenced by CD spectroscopy. Binding and competition studies with bevacizumab in ELISA and surface plasmon resonance analysis revealed that peptide 1 represents the complete bevacizumab binding site, including the hairpin loop (β5-turn-β6) and the structure-supporting β2-α2-β3 loop. Vaccination with peptide 1 elicited high titers of cross-reactive antibodies to VEGF, with potent neutralizing activity. Moreover, vaccination-induced antisera displayed strong angiostatic and tumor-growth-inhibiting properties in a preclinical mouse model for colorectal carcinoma, whereas antibodies raised with peptides exclusively encompassing the β5-turn-β6 loop (peptides 15 and 20) did not. Immunization with peptide 1 or 7 (murine analog of 1) in combinationwith the potent adjuvant raffinose fatty acid sulfate ester (RFASE) showed significant inhibition of tumor growth in the B16F10 murine melanoma model. Based on these data, we conclude that this vaccination technology,which is currently being investigated in a phase I clinical trial (NCT02237638), can potentially outperform currently applied anti-VEGF therapeutics.

Exploiting natural variation in susceptibility of Arabidopsis thaliana to Meloidogyne incognita to breed broad-spectrum resistance to root-knot nematodes
Warmerdam, S. ; Schaik, C.C. van; Lozano Torres, J.L. ; Finkers-Tomczak, A.M. ; Sterken, M.G. ; Bakker, J. ; Goverse, A. ; Smant, G. - \ 2016
Arabidopsis thaliana HAPMAP population, genome wide association mapping, parasitic nematode, plant-nematode interaction, susceptibility factors.
The root knot nematode Meloidogyne incognita is able to parasitize hundreds of plant species and is a major threat in nearly all vegetable-growing regions in the world. Current resistance is based on major dominant resistance (R) genes, which are frequently overcome by the occurrence of resistance-breaking races of M. incognita. Allelic variation in genetic loci associated with susceptibility to plant-parasitic nematodes within a single plant species has thus far not been used to breed durable broad-spectrum resistance in crops. We investigated the susceptibility of 350 different ecotypes of A. thaliana for the root-knot nematode M. incognita. A nine-fold difference in susceptibility to M. incognita was found between the most and the least susceptible ecotypes. This quantitative variation can be caused by polymorphic levels of gene transcripts, and by allelic variation within transcripts of essential susceptibility genes. We conducted a genome wide association mapping study to determine loci that contribute to susceptibility of A. thaliana to M. incognita. Genes underlying these loci were investigated with T-DNA insertion mutation analysis to confirm their effect on nematode susceptibility of A. thaliana. Our data indicate that allelic variation can be used to breed for broad-spectrum nematode resistance.
Tuber yield, infestation and quality assessment of potato genotypes, partially resistant to Meloidogyne chitwoodi
Teklu, M.G. ; Schomaker, C.H. ; Been, T.H. - \ 2016
As part of developing a partial resistance test for potato genotypes resistant to M. chitwoodi; growth, fresh tuber weight, level of tuber infestation and quality loss were studied under greenhouse conditions. Results from four successive experiments were combined. The study involved 7 genotypes with resistance to M. chitwoodi and 1 with resistance to G. pallida. Désirée was used as a control. Plants were inoculated with densities ranging from 0.0625 to 256 J2 (g dry soil)-1 in a 2 log series. Height as growth indicator was measured every week while, fresh tuber weight, tuber infestation and quality were measured at harvest. Also, pots with different volume 10, 5, 3 and 2 kg were used to explore the idea of testing both resistance and yield plus quality loss in smaller and cheaper pots without affecting the nematode-plant system. All data were treated equally in a meta-analysis and relevant models were used to describe the pattern of the data. Plant height showed normal logistic growth in all experiments. Plant height was positively affected by increasing Pi and negatively by pot size. In general growth was delayed. Tuber yield was not affected in four out of 8 genotypes. The four other genotypes and cv. Désirée showed a decrease of fresh tuber weight with minimum yields ranging from 0.40 to 0.84 and 0.75, respectively. In two tested starch potato genotypes an additional decrease of starch content was measured. Tuber infestation levels were reduced and quality was improved compared to the susceptible control and MDG2, with more than 90% of the pots containing clean tubers, with the exception of genotype 2011M1. Quality, expressed as Tuber-Knot Index, was well below < 10, indicating that all genotypes were acceptable for industrial processing.
Are positively-selected effectors of the root-knot nematode Meloidogyne incognita involved in plant resistance
Verhoeven, Ava ; Prins, J.C.P. ; Finkers-Tomczak, A.M. ; Varossieau, K. ; Raaij, D.R. van; Pomp, H. ; Goverse, A. ; Smant, G. - \ 2016

The tropical root-knot nematode Meloidogyne incognita is a global problem in tomato and many other vegetable crops. The obligate endoparasitic M. incognita can cause about 5% crop loss annually. Chemical pesticides can no longer be used to control M. incognita because of environmental and public health concerns. Meanwhile, the most frequently used Mi-1 resistance in tomato is increasingly being broken by virulent populations of M. incognita. Virulent root knot nematodes are thought to have acquired effectors that enable them to avoid recognition by resistance proteins in plants. Therefore, insight into the repertoire of effectors of M. incognita can help to identify new sources of resistance to which the field populations of nematodes in tomato-producing areas have not yet adapted.

To identify positively-selected effector families in the genome sequence of M. incognita, a bioinformatics pipeline centred on the algorithms PRANK, Codeml, and Phobius was constructed. In total, 77 positively-selected clusters of paralogous genes were identified in the genome of M. incognita, which encode a total of 254 secretory proteins. The effectiveness of the pipeline was demonstrated by the fact that several positively-selected clusters of paralogous genes have been identified as effectors of M. incognita in earlier studies. Highly ranking candidate effectors from the pipeline are currently being functionally characterized in plants using transient and stable overexpression and using host-delivered RNA-interference in nematodes.

Redirection of auxin flow in Arabidopsis thaliana roots after infection by root-knot nematodes
Kyndt, Tina ; Goverse, Aska ; Haegeman, Annelies ; Warmerdam, Sonja ; Wanjau, Cecilia ; Jahani, Mona ; Engler, Gilbert ; Almeida Engler, Janice De; Gheysen, Godelieve - \ 2016
Journal of Experimental Botany 67 (2016)15. - ISSN 0022-0957 - p. 4559 - 4570.
Plant-parasitic root-knot nematodes induce the formation of giant cells within the plant root, and it has been recognized that auxin accumulates in these feeding sites. Here, we studied the role of the auxin transport system governed by AUX1/LAX3 influx proteins and different PIN efflux proteins during feeding site development in Arabidopsis thaliana roots. Data generated via promoter–reporter line and protein localization analyses evoke a model in which auxin is being imported at the basipetal side of the feeding site by the concerted action of the influx proteins AUX1 and LAX3, and the efflux protein PIN3. Mutants in auxin influx proteins AUX1 and LAX3 bear significantly fewer and smaller galls, revealing that auxin import into the feeding sites is needed for their development and expansion. The feeding site development in auxin export (PIN) mutants was only slightly hampered. Expression of some PINs appears to be suppressed in galls, probably to prevent auxin drainage. Nevertheless, a functional PIN4 gene seems to be a prerequisite for proper nematode development and gall expansion, most likely by removing excessive auxin to stabilize the hormone level in the feeding site. Our data also indicate a role of local auxin peaks in nematode attraction towards the root
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