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.

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    SNARE Complexity in Arbuscular Mycorrhizal Symbiosis
    Huisman, Rik ; Hontelez, Jan ; Bisseling, Ton ; Limpens, Erik - \ 2020
    Frontiers in Plant Science 11 (2020). - ISSN 1664-462X
    arbuscular mycorrhiza - exocytosis - Medicago - membrane - SNARE - symbiosis - syntaxin - VAMP

    How cells control the proper delivery of vesicles and their associated cargo to specific plasma membrane (PM) domains upon internal or external cues is a major question in plant cell biology. A widely held hypothesis is that expansion of plant exocytotic machinery components, such as SNARE proteins, has led to a diversification of exocytotic membrane trafficking pathways to function in specific biological processes. A key biological process that involves the creation of a specialized PM domain is the formation of a host–microbe interface (the peri-arbuscular membrane) in the symbiosis with arbuscular mycorrhizal fungi. We have previously shown that the ability to intracellularly host AM fungi correlates with the evolutionary expansion of both v- (VAMP721d/e) and t-SNARE (SYP132α) proteins, that are essential for arbuscule formation in Medicago truncatula. Here we studied to what extent the symbiotic SNAREs are different from their non-symbiotic family members and whether symbiotic SNAREs define a distinct symbiotic membrane trafficking pathway. We show that all tested SYP1 family proteins, and most of the non-symbiotic VAMP72 members, are able to complement the defect in arbuscule formation upon knock-down/-out of their symbiotic counterparts when expressed at sufficient levels. This functional redundancy is in line with the ability of all tested v- and t-SNARE combinations to form SNARE complexes. Interestingly, the symbiotic t-SNARE SYP132α appeared to occur less in complex with v-SNAREs compared to the non-symbiotic syntaxins in arbuscule-containing cells. This correlated with a preferential localization of SYP132α to functional branches of partially collapsing arbuscules, while non-symbiotic syntaxins accumulate at the degrading parts. Overexpression of VAMP721e caused a shift in SYP132α localization toward the degrading parts, suggesting an influence on its endocytic turn-over. These data indicate that the symbiotic SNAREs do not selectively interact to define a symbiotic vesicle trafficking pathway, but that symbiotic SNARE complexes are more rapidly disassembled resulting in a preferential localization of SYP132α at functional arbuscule branches.

    Biomarker Research in ADHD: the Impact of Nutrition (BRAIN) – 16S data set
    Stobernack, Tim ; Frankena, Klaas ; Rodrigues Pereira, Rob ; Schrama, Rosan P.H. ; Baarlen, Peter van; Kleerebezem, Michiel ; Pelsser, Lidy ; Hontelez, Saartje - \ 2020
    Wageningen University & Research
    ADHD - few-foods diet - biomarker - 16S metagenomics
    Metagenomic 16S amplicon sequencing data for 79 children included in the Biomarker Research in ADHD: the Impact of Nutrition (BRAIN) study, an open-label trial during which children with ADHD followed a few-foods diet (FFD). Sampling was done during screening (t0), before the FFD (t1) and after 5 weeks of FFD (t2).
    Biomarker Research in ADHD: the Impact of Nutrition (BRAIN) – lncRNA data set
    Stobernack, Tim ; Frankena, Klaas ; Rodrigues Pereira, Rob ; Schrama, Rosan P.H. ; Baarlen, Peter van; Kleerebezem, Michiel ; Pelsser, Lidy ; Hontelez, Saartje - \ 2020
    Wageningen University & Research
    ADHD - few-foods diet - biomarker - lncRNA - coding RNA
    Long non-coding RNA and coding RNA sequencing data for 79 children included in the Biomarker Research in ADHD: the Impact of Nutrition (BRAIN) study, an open-label trial during which children with ADHD followed a few-foods diet (FFD). Sampling was done before the FFD (t1) and after 5 weeks of FFD (t2).
    Biomarker Research in ADHD: the Impact of Nutrition (BRAIN) – smallRNA data set
    Stobernack, Tim ; Frankena, Klaas ; Rodrigues Pereira, Rob ; Schrama, Rosan P.H. ; Baarlen, Peter van; Kleerebezem, Michiel ; Pelsser, Lidy ; Hontelez, Saartje - \ 2020
    Wageningen University & Research
    ADHD - few-foods diet - biomarker - IncRNA - coding RNA
    Small RNA sequencing data for 79 children included in the Biomarker Research in ADHD: the Impact of Nutrition (BRAIN) study, an open-label trial during which children with ADHD followed a few-foods diet (FFD). Sampling was done before the FFD (t1) and after 5 weeks of FFD (t2).
    Biomarker Research in ADHD: the Impact of Nutrition (BRAIN) – Metagenomics data set
    Stobernack, Tim ; Frankena, Klaas ; Rodrigues Pereira, Rob ; Schrama, Rosan P.H. ; Baarlen, Peter van; Kleerebezem, Michiel ; Pelsser, Lidy ; Hontelez, Saartje - \ 2020
    Wageningen University & Research
    ADHD - few-foods diet - biomarker - metagenomics
    Metagenomics sequencing data for 79 children included in the Biomarker Research in ADHD: the Impact of Nutrition (BRAIN) study, an open-label trial during which children with ADHD followed a few-foods diet (FFD). Sampling was done before the FFD (t1) and after 5 weeks of FFD (t2).
    Biomarker Research in ADHD: the Impact of Nutrition (BRAIN) – Metabolomics data
    Stobernack, Tim ; Frankena, Klaas ; Rodrigues Pereira, Rob ; Schrama, Rosan P.H. ; Baarlen, Peter van; Kleerebezem, Michiel ; Pelsser, Lidy ; Hontelez, Saartje - \ 2020
    Wageningen University & Research
    ADHD - few-foods diet - biomarker - metabolomics
    Small-molecule profiling data for 79 children included in the Biomarker Research in ADHD: the Impact of Nutrition (BRAIN) study, an open-label trial during which children with ADHD followed a few-foods diet (FFD). Sampling was done before the FFD (t1) and after 5 weeks of FFD (t2).
    Biomarker Research in ADHD: the Impact of Nutrition (BRAIN) – MultiplexELISA data
    Stobernack, Tim ; Frankena, Klaas ; Rodrigues Pereira, Rob ; Schrama, Rosan P.H. ; Baarlen, Peter van; Kleerebezem, Michiel ; Pelsser, Lidy ; Hontelez, Saartje - \ 2020
    Wageningen University & Research
    ADHD - few-foods diet - biomarker - immunology - metabolism - hormones
    Multiplex ELISA data of immune, metabolism and hormone related molecules for 79 children included in the Biomarker Research in ADHD: the Impact of Nutrition (BRAIN) study, an open-label trial during which children with ADHD followed a few-foods diet (FFD). Sampling was done before the FFD (t1) and after 5 weeks of FFD (t2).
    Biomarker Research in ADHD: the Impact of Nutrition (BRAIN) – Behaviour scores
    Stobernack, Tim ; Frankena, Klaas ; Rodrigues Pereira, Rob ; Schrama, Rosan P.H. ; Baarlen, Peter van; Kleerebezem, Michiel ; Pelsser, Lidy ; Hontelez, Saartje - \ 2020
    Wageningen University & Research
    ADHD - ODD - few-foods diet - biomarker
    Symptom scores of ADHD and ODD for 79 children included in the Biomarker Research in ADHD: the Impact of Nutrition (BRAIN) study, an open-label trial during which children with ADHD followed a few-foods diet (FFD). Sampling was done before the FFD (t1) and after 5 weeks of FFD (t2).
    Biomarker Research in ADHD: The Impact of Nutrition (BRAIN) - Study protocol of an open-label trial to investigate the mechanisms underlying the effects of a few-foods diet on ADHD symptoms in children
    Stobernack, Tim ; Vries, Stefan P.W. De; Rodrigues Pereira, Rob ; Pelsser, Lidy M. ; Braak, Cajo J.F. Ter; Aarts, Esther ; Baarlen, Peter Van; Kleerebezem, Michiel ; Frankena, Klaas ; Hontelez, Saartje - \ 2019
    BMJ Open 9 (2019)11. - ISSN 2044-6055
    ADHD - biomarker - brain activity - few-foods diet - fMRI - microbiota

    Introduction Attention deficit hyperactivity disorder (ADHD) is the most common childhood behavioural disorder, causing significant impediment to a child's development. It is a complex disorder with numerous contributing (epi)genetic and environmental factors. Currently, treatment consists of behavioural and pharmacological therapy. However, ADHD medication is associated with several side effects, and concerns about long-term effects and efficacy exist. Therefore, there is considerable interest in the development of alternative treatment options. Double-blind research investigating the effects of a few-foods diet (FFD) has demonstrated a significant decrease in ADHD symptoms following an FFD. However, an FFD requires a considerable effort of both child and parents, limiting its applicability as a general ADHD treatment. To make FFD intervention less challenging or potentially obsolete, we need to understand how, and in which children, an FFD affects ADHD behaviour and, consequently, the child's well-being. We hypothesise that an FFD affects brain function, and that the nutritional impact on ADHD is effectuated by a complex interplay between the microbiota, gut and brain, that is, the microbiota-gut-brain axis. Methods and analysis The Biomarker Research in ADHD: the Impact of Nutrition (BRAIN) study is an open-label trial with researchers blinded to changes in ADHD symptoms during sample processing and initial data analyses. Ethics and dissemination The Medical Research and Ethics Committee of Wageningen University has approved this study (NL63851.081.17, application 17/24). Results will be disseminated through peer-reviewed journal publications, conference presentations, (social) media and the BRAIN study website. A summary of the findings will be provided to the participants. Trial registration number NCT03440346. Study dates Collection of primary outcome data started in March 2018 and will be ongoing until 100 children have participated in the study. Sample data analysis will start after all samples have been collected.

    Data from: Comparative genomics of the nonlegume Parasponia reveals insights into evolution of nitrogen-fixing rhizobium symbioses
    Velzen, R. van; Holmer, R. ; Bu, F. ; Rutten, L.J.J. ; Zeijl, A.L. van; Liu, W. ; Santuari, L. ; Cao, Q. ; Sharma, Trupti ; Shen, D. ; Roswanjaya, Yuda ; Wardhani, T. ; Seifi Kalhor, M. ; Jansen, Joelle ; Hoogen, D.J. van den; Gungor, Berivan ; Hartog, M.V. ; Hontelez, Jan ; Verver, J.W.G. ; Yang, Wei-Cai ; Schijlen, E.G.W.M. ; Repin, Rimi ; Schilthuizen, M. ; Schranz, M.E. ; Heidstra, R. ; Miyata, Kana ; Fedorova, E. ; Kohlen, W. ; Bisseling, A.H.J. ; Smit, S. ; Geurts, R. - \ 2018
    Wageningen University & Research
    comparative genomics - copy number variation - evolution - nitrogen fixation - symbiosis - Parasponia andersonii - Parasponia rigada - Parasponia rugosa - Trema levigata - Trema orientalis - Trema tomentosa
    Nodules harboring nitrogen-fixing rhizobia are a well-known trait of legumes, but nodules also occur in other plant lineages, with rhizobia or the actinomycete Frankia as microsymbiont. It is generally assumed that nodulation evolved independently multiple times. However, molecular-genetic support for this hypothesis is lacking, as the genetic changes underlying nodule evolution remain elusive. We conducted genetic and comparative genomics studies by using Parasponia species (Cannabaceae), the only nonlegumes that can establish nitrogen-fixing nodules with rhizobium. Intergeneric crosses between Parasponia andersonii and its nonnodulating relative Trema tomentosa demonstrated that nodule organogenesis, but not intracellular infection, is a dominant genetic trait. Comparative transcriptomics of P. andersonii and the legume Medicago truncatula revealed utilization of at least 290 orthologous symbiosis genes in nodules. Among these are key genes that, in legumes, are essential for nodulation, including NODULE INCEPTION (NIN) and RHIZOBIUM-DIRECTED POLAR GROWTH (RPG). Comparative analysis of genomes from three Parasponia species and related nonnodulating plant species show evidence of parallel loss in nonnodulating species of putative orthologs of NIN, RPG, and NOD FACTOR PERCEPTION. Parallel loss of these symbiosis genes indicates that these nonnodulating lineages lost the potential to nodulate. Taken together, our results challenge the view that nodulation evolved in parallel and raises the possibility that nodulation originated ∼100 Mya in a common ancestor of all nodulating plant species, but was subsequently lost in many descendant lineages. This will have profound implications for translational approaches aimed at engineering nitrogen-fixing nodules in crop plants
    Host- and stage-dependent secretome of the arbuscular mycorrhizal fungus Rhizophagus irregularis
    Zeng, Tian ; Holmer, Rens ; Hontelez, Jan ; Lintel-Hekkert, Bas te; Marufu, Lucky ; Zeeuw, Thijs de; Wu, Fangyuan ; Schijlen, Elio ; Bisseling, Ton ; Limpens, Erik - \ 2018
    The Plant Journal 94 (2018)3. - ISSN 0960-7412 - p. 411 - 425.
    Arbuscular mycorrhizal fungi form the most wide‐spread endosymbiosis with plants. There is very little host‐specificity in this interaction, however host preferences as well as varying symbiotic efficiencies have been observed. We hypothesize that secreted proteins (SPs) may act as fungal effectors to control symbiotic efficiency in a host‐dependent manner. Therefore, we studied whether AM fungi adjust their secretome in a host‐ and stage‐dependent manner to contribute to their extremely wide host‐range. We investigated the expression of SP‐encoding genes of Rhizophagus irregularis in three evolutionary distantly‐related plant species, Medicago truncatula, Nicotiana benthamiana and Allium schoenoprasum. In addition we used laser microdissection in combination with RNAseq to study SP expression at different stages of the interaction in Medicago. Our data indicate that most expressed SPs show roughly equal expression levels in the interaction with all three host plants. In addition, a subset shows significant differential expression depending on the host plant. Furthermore, SP expression is controlled locally in the hyphal network in response to host dependent cues. Overall, this study presents a comprehensive analysis of the R. irregularis secretome, which now offers a solid basis to direct functional studies on the role of fungal SPs in AM symbiosis.
    Comparative genomics of the nonlegume Parasponia reveals insights into evolution of nitrogen-fixing rhizobium symbioses
    Velzen, R. van; Holmer, R. ; Bu, F. ; Rutten, L.J.J. ; Zeijl, A.L. van; Liu, W. ; Santuari, L. ; Cao, Q. ; Sharma, Trupti ; Shen, Defeng ; Purwana Roswanjaya, Yuda ; Wardhani, T. ; Seifi Kalhor, M. ; Jansen, Joelle ; Hoogen, D.J. van den; Güngör, Berivan ; Hartog, M.V. ; Hontelez, J. ; Verver, Jan ; Yang, Wei-Cai ; Schijlen, E.G.W.M. ; Repin, Rimi ; Schilthuizen, M. ; Schranz, M.E. ; Heidstra, R. ; Miyata, Kana ; Fedorova, E. ; Kohlen, W. ; Bisseling, A.H.J. ; Smit, S. ; Geurts, R. - \ 2018
    Proceedings of the National Academy of Sciences of the United States of America 115 (2018)20. - ISSN 0027-8424 - p. E4700 - E4709.
    Nodules harboring nitrogen-fixing rhizobia are a well-known trait of legumes, but nodules also occur in other plant lineages, with rhizobia or the actinomycete Frankia as microsymbiont. It is generally assumed that nodulation evolved independently multiple times. However, molecular-genetic support for this hypothesis is lacking, as the genetic changes underlying nodule evolution remain elusive. We conducted genetic and comparative genomics studies by using Parasponia species (Cannabaceae), the only nonlegumes that can establish nitrogen-fixing nodules with rhizobium. Intergeneric crosses between Parasponia andersonii and its nonnodulating relative Trema tomentosa demonstrated that nodule organogenesis, but not intracellular infection, is a dominant genetic trait. Comparative transcriptomics of P. andersonii and the legume Medicago truncatula revealed utilization of at least 290 orthologous symbiosis genes in nodules. Among these are key genes that, in legumes, are essential for nodulation, including NODULE INCEPTION (NIN) and RHIZOBIUM-DIRECTED POLAR GROWTH (RPG). Comparative analysis of genomes from three Parasponia species and related nonnodulating plant species show evidence of parallel loss in nonnodulating species of putative orthologs of NIN, RPG, and NOD FACTOR PERCEPTION. Parallel loss of these symbiosis genes indicates that these nonnodulating lineages lost the potential to nodulate. Taken together, our results challenge the view that nodulation evolved in parallel and raises the possibility that nodulation originated ∼100 Mya in a common ancestor of all nodulating plant species, but was subsequently lost in many descendant lineages. This will have profound implications for translational approaches aimed at engineering nitrogen-fixing nodules in crop plants.
    Parallel loss of symbiosis genes in relatives of nitrogen-fixing non-legume Parasponia
    Velzen, R. van; Holmer, R. ; Bu, F. ; Rutten, L.J.J. ; Zeijl, A.L. van; Liu, W. ; Santuari, L. ; Cao, Q. ; Sharma, Trupti ; Shen, D. ; Purwana Roswanjaya, Yuda ; Wardhani, T. ; Seifi Kalhor, M. ; Jansen, Joelle ; Hoogen, D.J. van den; Gungor, Berivan ; Hartog, M.V. ; Hontelez, J. ; Verver, J.W.G. ; Yang, W.C. ; Schijlen, E.G.W.M. ; Repin, Rimi ; Schilthuizen, M. ; Schranz, M.E. ; Heidstra, R. ; Miyata, Kana ; Fedorova, E. ; Kohlen, W. ; Bisseling, A.H.J. ; Smit, S. ; Geurts, R. - \ 2017
    BioRxiv - 88 p.
    Rhizobium nitrogen-fixing nodules are a well-known trait of legumes, but nodules also occur in other plant lineages either with rhizobium or the actinomycete Frankia as microsymbiont. The widely accepted hypothesis is that nodulation evolved independently multiple times, with only a few losses. However, insight in the evolutionary trajectory of nodulation is lacking. We conducted comparative studies using Parasponia (Cannabaceae), the only non-legume able to establish nitrogen fixing nodules with rhizobium. This revealed that Parasponia and legumes utilize a large set of orthologous symbiosis genes. Comparing genomes of Parasponia and its non-nodulating relative Trema did not reveal specific gene duplications that could explain a recent gain of nodulation in Parasponia. Rather, Trema and other non-nodulating species in the order Rosales show evidence of pseudogenization or loss of key symbiosis genes. This demonstrates that these species have lost the potential to nodulate. This finding challenges a long-standing hypothesis on evolution of nitrogen-fixing symbioses, and has profound implications for translational approaches aimed at engineering nitrogen-fixing nodules in crop plants.
    A symbiosis-dedicated SYNTAXIN OF PLANTS 13II isoform controls the formation of a stable host-microbe interface in symbiosis
    Huisman, Rik ; Hontelez, Jan ; Mysore, Kirankumar S. ; Wen, Jiangqi ; Bisseling, Ton ; Limpens, Erik - \ 2016
    New Phytologist 211 (2016)4. - ISSN 0028-646X - p. 1338 - 1351.
    Alternative splicing - Arbuscular mycorrhiza (AM) - Arbuscule - Host-microbe interface - N-ethylmaleimide-sensitive factor-attachment protein receptor (SNARE) - Rhizobium - Symbiosis - Symbiosome

    Arbuscular mycorrhizal (AM) fungi and rhizobium bacteria are accommodated in specialized membrane compartments that form a host-microbe interface. To better understand how these interfaces are made, we studied the regulation of exocytosis during interface formation. We used a phylogenetic approach to identify target soluble N-ethylmaleimide-sensitive factor-attachment protein receptors (t-SNAREs) that are dedicated to symbiosis and used cell-specific expression analysis together with protein localization to identify t-SNAREs that are present on the host-microbe interface in Medicago truncatula. We investigated the role of these t-SNAREs during the formation of a host-microbe interface. We showed that multiple syntaxins are present on the peri-arbuscular membrane. From these, we identified SYNTAXIN OF PLANTS 13II (SYP13II) as a t-SNARE that is essential for the formation of a stable symbiotic interface in both AM and rhizobium symbiosis. In most dicot plants, the SYP13II transcript is alternatively spliced, resulting in two isoforms, SYP13IIα and SYP13IIβ. These splice-forms differentially mark functional and degrading arbuscule branches. Our results show that vesicle traffic to the symbiotic interface is specialized and required for its maintenance. Alternative splicing of SYP13II allows plants to replace a t-SNARE involved in traffic to the plasma membrane with a t-SNARE that is more stringent in its localization to functional arbuscules.

    CREB expression in the brains of two closely related parasitic wasp species that differ in long-term memory formation
    Berg, M. van den; Verbaarschot, P.G.H. ; Hontelez, S. ; Vet, L.E.M. ; Dicke, M. ; Smid, H.M. - \ 2010
    Insect Molecular Biology 19 (2010)3. - ISSN 0962-1075 - p. 367 - 379.
    element-binding-protein - camp-response element - transcription factor creb - central-nervous-system - snail lymnaea-stagnalis - cyclic-amp - messenger-rna - cotesia-glomerata - drosophila-melanogaster - targeted mutation
    The cAMP/PKA signalling pathway and transcription factor cAMP response element-binding protein (CREB) play key roles in long-term memory (LTM) formation. We used two closely related parasitic wasp species, Cotesia glomerata and Cotesia rubecula, which were previously shown to be different in LTM formation, and sequenced at least nine different CREB transcripts in both wasp species. The splicing patterns, functional domains and amino acid sequences were similar to those found in the CREB genes of other organisms. The predicted amino acid sequences of the CREB isoforms were identical in both wasp species. Using real-time quantitative PCR we found that two low abundant CREB transcripts are differentially expressed in the two wasps, whereas the expression levels of high abundant transcripts are similar.
    Medicago truncatula ENOD40-1 and ENOD40-2 are both involved in nodule initiation and bacteroid development
    Wan, X. ; Hontelez, J. ; Lillo, A. ; Guarnerio, C. ; Peut, D. van de; Fedorova, E. ; Bisseling, T. ; Franssen, H. - \ 2007
    Journal of Experimental Botany 58 (2007)8. - ISSN 0022-0957 - p. 2033 - 2041.
    legume root-nodules - gene enod40 - alfalfa nodules - lotus-japonicus - expression - rna - nodulation - induction - growth - organogenesis
    The establishment of a nitrogen-fixing root nodule on legumes requires the induction of mitotic activity of cortical cells leading to the formation of the nodule primordium and the infection process by which the bacteria enter this primordium. Several genes are up-regulated during these processes, among them ENOD40. Here it is shown, by using gene-specific knock-down of the two Medicago truncatula ENOD40 genes, that both genes are involved in nodule initiation. Further, during nodule development, both genes are essential for bacteroid development.
    Expression of ENOD40 during tomato plant development
    Vleghels, I.J.E. ; Hontelez, J.G.J. ; Ribeiro, A. ; Fransz, P.F. ; Bisseling, T. ; Franssen, H.G.J.M. - \ 2003
    Planta 218 (2003). - ISSN 0032-0935 - p. 42 - 49.
    nodule development - medicago-truncatula - seed-germination - lotus-japonicus - binding protein - genes - patterns - mutant - pachytene - symbiosis
    In legumes, ENOD40 expression is increased upon interaction of plants with rhizobia. Little is known of the expression pattern of ENOD40 during other stages of the plant life cycle. Studies of ENOD40 expression in non-legume development may give an indication of the function of the gene. To investigate the ENOD40 expression pattern during plant development, a fusion between the beta-glucuronidase (GUS) reporter gene and 150 bp of the 5' untranslated region plus 3,000 bp of 5' untranscribed tomato ENOD40 sequence was constructed and introduced into Lycopersicon esculentum Miller. Based on the observed GUS expression patterns in transgenic tomato we speculate that ENOD40 in tomato has a role in counteracting ethylene-provoked responses.
    Endotoxins: health-based recommended occupational exposure limit.
    Feron, V.J. ; Beems, R.B. ; Brokamp, J.J.A.M. ; Heederik, D.J.J. ; Henderson, P.T. ; Hontelez, L.C.M.P. ; Jong, G. de; Mik, G. de; Molier-Bloot, J. - \ 1998
    Unknown Publisher
    Paracentromeric sequences on tomato chromosome 6 show homology to human satellite III and to the mammalian CENP-B binding box.
    Weide, R. ; Hontelez, J. ; Kammen, A. van; Koornneef, M. ; Zabel, P. - \ 1998
    Molecular and General Genetics 259 (1998). - ISSN 0026-8925 - p. 190 - 197.
    Genetic and physical localization of the root-knot nematode resistance locus Mi in tomato.
    Kaloshian, I. ; Yaghoobi, J. ; Liharska, T. ; Hontelez, J. ; Hanson, D. ; Hogan, P. ; Jesse, T. ; Wijbrandi, J. ; Simons, G. ; Vos, P. ; Zabel, P. ; Williamson, V.M. - \ 1998
    Molecular and General Genetics 257 (1998). - ISSN 0026-8925 - p. 376 - 385.
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