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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Livestock-Associated meticillin-resistant Staphylococcus aureus in a young harbour seal (Phoca vitulina) with endocarditis
Rubio-Garcia, Ana ; Rossen, John W.A. ; Wagenaar, Jaap A. ; Friedrich, Alex W. ; Zeijl, Jan H. Van - \ 2019
Veterinary Record Case Reports 7 (2019)3. - ISSN 2052-6121
Bacterial diseases - Endocarditis - Infection - Marine mammals - MRSA - Phoca vitulina

A five-month-old male harbour seal was admitted for rehabilitation to the Sealcentre Pieterburen on November 16, 2015. During initial veterinary examination parasitic pneumonia and secondary bacterial pneumonia were suspected. Therefore, the seal received antiparasitic and antimicrobial treatment and appeared to recover but died unexpectedly after several weeks. Postmortem examination revealed a perforation in the aortic wall and histopathological examination of the aorta revealed mural necrosis with haemorrhage and suppurative to mixed inflammation. Bacterial culture resulted in isolation of a meticillin-resistant Staphylococcus aureus (MRSA) from the pericardial effusion. Subsequent culture of rectal swabs collected at arrival and during rehabilitation showed that the animal was already colonised with MRSA when admitted to the Sealcentre. MRSA has been isolated from marine mammals before, however, to our knowledge this is the first report of MRSA-Associated endocarditis in seals and the first time that livestock-Associated MRSA is reported in seals.

Transforming, Genome Editing and Phenotyping the Nitrogen-fixing Tropical Cannabaceae Tree Parasponia andersonii
Wardhani, Titis A.K. ; Roswanjaya, Yuda Purwana ; Dupin, Simon ; Li, Huchen ; Linders, Sidney ; Hartog, Marijke ; Geurts, Rene ; Zeijl, Arjan van - \ 2019
Journal of Visualized Experiments (2019)150. - ISSN 1940-087X - 17 p.

Parasponia andersonii is a fast-growing tropical tree that belongs to the Cannabis family (Cannabaceae). Together with 4 additional species, it forms the only known non-legume lineage able to establish a nitrogen-fixing nodule symbiosis with rhizobium. Comparative studies between legumes and P. andersonii could provide valuable insight into the genetic networks underlying root nodule formation. To facilitate comparative studies, we recently sequenced the P. andersonii genome and established Agrobacterium tumefaciens-mediated stable transformation and CRISPR/Cas9-based genome editing. Here, we provide a detailed description of the transformation and genome editing procedures developed for P. andersonii. In addition, we describe procedures for the seed germination and characterization of symbiotic phenotypes. Using this protocol, stable transgenic mutant lines can be generated in a period of 2-3 months. Vegetative in vitro propagation of T0 transgenic lines allows phenotyping experiments to be initiated at 4 months after A. tumefaciens co-cultivation. Therefore, this protocol takes only marginally longer than the transient Agrobacterium rhizogenes-based root transformation method available for P. andersonii, though offers several clear advantages. Together, the procedures described here permit P. andersonii to be used as a research model for studies aimed at understanding symbiotic associations as well as potentially other aspects of the biology of this tropical tree.

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
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
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.
CRISPR/cas9-mediated mutagenesis of four putative symbiosis genes of the tropical tree parasponia andersonii reveals novel phenotypes
Zeijl, Arjan Van; Wardhani, Titis A.K. ; Seifi Kalhor, Maryam ; Rutten, Luuk ; Bu, Fengjiao ; Hartog, Marijke ; Linders, Sidney ; Fedorova, Elena E. ; Bisseling, Ton ; Kohlen, Wouter ; Geurts, Rene - \ 2018
Frontiers in Plant Science 9 (2018). - ISSN 1664-462X
CRISPR/Cas9 - Nodule - Parasponia andersonii - Rhizobium - Stable transformation - Symbiosis
Parasponia represents five fast-growing tropical tree species in the Cannabaceae and is the only plant lineage besides legumes that can establish nitrogen-fixing nodules with rhizobium. Comparative analyses between legumes and Parasponia allows identification of conserved genetic networks controlling this symbiosis. However, such studies are hampered due to the absence of powerful reverse genetic tools for Parasponia. Here, we present a fast and efficient protocol for Agrobacterium tumefaciens-mediated transformation and CRISPR/Cas9 mutagenesis of Parasponia andersonii. Using this protocol, knockout mutants are obtained within 3 months. Due to efficient micro-propagation, bi-allelic mutants can be studied in the T0 generation, allowing phenotypic evaluation within 6 months after transformation. We mutated four genes – PanHK4, PanEIN2, PanNSP1, and PanNSP2 – that control cytokinin, ethylene, or strigolactone hormonal networks and that in legumes commit essential symbiotic functions. Knockout mutants in Panhk4 and Panein2 displayed developmental phenotypes, namely reduced procambium activity in Panhk4 and disturbed sex differentiation in Panein2 mutants. The symbiotic phenotypes of Panhk4 and Panein2 mutant lines differ from those in legumes. In contrast, PanNSP1 and PanNSP2 are essential for nodule formation, a phenotype similar as reported for legumes. This indicates a conserved role for these GRAS-type transcriptional regulators in rhizobium symbiosis, illustrating the value of Parasponia trees as a research model for reverse genetic studies.
RNAseq analysis of susceptible zone of the Medicago truncatula root from wild-type and Mtcre1 mutant plants 3 hours after stimulation by Rhizobium lipo-chitin oligosaccharide
Geurts, R. ; Zeijl, A.L. van - \ 2017
Wageningen University & Research
E-MTAB-3007 - Medicago truncatula - ERP105151 - PRJEB23399
RNAseq analysis of Medicago truncatula WT and Mtcre1 3h post rhizobium LCO application 4 sample with 3 biological replicates each, sequenced in both directions
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.
Dissecting hormonal pathways in nitrogen-fixing rhizobium symbioses
Zeijl, Arjan van - \ 2017
Wageningen University. Promotor(en): T. Bisseling, co-promotor(en): R. Geurts. - Wageningen : Wageningen University - ISBN 9789463436311 - 231
plants - root nodules - rhizobium - symbiosis - cytokinins - plant-microbe interactions - biosynthesis - mutagenesis - genes - nodulation - planten - wortelknolletjes - rhizobium - symbiose - cytokininen - plant-microbe interacties - biosynthese - mutagenese - genen - knobbelvorming

Nitrogen is a key element for plant growth. To meet nitrogen demands, some plants establish an endosymbiotic relationship with nitrogen-fixing rhizobium or Frankia bacteria. This involves formation of specialized root lateral organs, named nodules. These nodules are colonized intracellularly, which creates optimal physiological conditions for the fixation of atmospheric nitrogen by the microbial symbiont. Nitrogen-fixing endosymbioses are found among four related taxonomic orders that together form the nitrogen-fixation clade. Within this clade, nodulation is restricted to ten separate lineages that are scattered among mostly non-nodulating plant species. This limited distribution suggests that genetic adaptations that allowed nodulation to evolve occurred in a common ancestor.

A major aim of the scientific community is to unravel the evolutionary trajectory towards a nitrogen-fixing nodule symbiosis. The formation of nitrogen-fixing root nodules is best studied in legumes (Fabaceae, order Fabales); especially in Lotus japonicus and Medicago truncatula, two species that serve as model. Legumes and Parasponia (Cannabaceae, order Rosales) represent the only two lineages that can form nodules with rhizobium bacteria. Studies on M. truncatula, L. japonicus and Parasponia showed, amongst others, that nodule formation is initiated upon perception of rhizobial secreted lipo-chitooligosaccharide (LCO) signals. These signals are structurally related to the symbiotic signals produced by arbuscular mycorrhizal fungi. These obligate biotropic fungi colonize roots of most land plants and form dense hyphal structures inside existing root cortical cells.

Rhizobial and mycorrhizal LCOs are perceived by LysM-domain-containing receptor-like kinases. These activate a signaling pathway that is largely shared between both symbioses. Symbiotic LCO receptors are closely related to chitin innate immune receptors, and some receptors even function in symbiotic as well as innate immune signaling. In Chapter 2, I review the intertwining of symbiotic LCO perception and chitin-triggered immunity. Furthermore, I discuss how rhizobia and mycorrhiza might employ LCO signaling to modulate plant immunity. In a perspective, I speculate on a role for plant hormones in immune modulation, besides an important function in nodule organogenesis.

In legumes, nodule organogenesis requires activation of cytokinin signaling. Mutants in the orthologous cytokinin receptor genes MtCRE1 and LjLHK1 in M. truncatula and L. japonicus, respectively, are severely affected in nodule formation. However, how cytokinin signaling is activated in response to rhizobium LCO perception and to what extent this contributes to rhizobium LCO-induced signaling remained elusive. In Chapter 3, I show that the majority of transcriptional changes induced in wild-type M. truncatula, upon application of rhizobium LCOs, are dependent on activation of MtCRE1-mediated cytokinin signaling. Among the genes induced in wild type are several involved in cytokinin biosynthesis. Consistently, cytokinin measurements indicate that cytokinins rapidly accumulate in M. truncatula roots upon treatment with rhizobium LCOs. This includes the bioactive cytokinins isopentenyl adenine and trans-zeatin. Therefore, I argue that cytokinin accumulation represents a key step in the pathway leading to legume root nodule organogenesis.

Strigolactones are plant hormones of which biosynthesis is increased in response to nutrient limitation. In rice (Oryza sativa) and M. truncatula, this response requires the GRAS-type transcriptional regulators NSP1 and NSP2. Both proteins regulate expression of DWARF27 (D27), which encodes an enzyme that performs the first committed step in strigolactone biosynthesis. NSP1 and NSP2 are also essential components of the signaling cascade that controls legume root nodule formation. In line with this, I questioned whether the NSP1-NSP2-D27 regulatory module functions in rhizobium symbiosis. In Chapter 4, I show that in M. truncatula MtD27 expression is induced within hours after treatment with rhizobium LCOs. Spatiotemporal expression studies revealed that MtD27 is expressed in the dividing cells of the nodule primordium. At later stages, its expression becomes confined to the meristem and distal infection zone of the mature nodule. Analysis of the expression pattern of MtCCD7 and MtCCD8, two additional strigolactone biosynthesis genes, showed that these genes are co-expressed with MtD27 in nodule primordia and mature nodules. Additionally, I show that symbiotic expression of MtD27 requires MtNSP1 and MtNSP2. This suggests that the NSP1-NSP2-D27 regulatory module is co-opted in rhizobium symbiosis.

Comparative studies between legumes and nodulating non-legumes could identify shared genetic networks required for nodule formation. We recently adopted Parasponia, the only non-legume lineage able to engage in rhizobium symbiosis. However, to perform functional studies, powerful reverse genetic tools for Parasponia are essential. In Chapter 5, I describe the development of a fast and efficient protocol for CRISPR/Cas9-mediated mutagenesis in Agrobacterium tumefaciens-transformed Parasponia andersonii plants. Using this protocol, stable mutants can be obtained in a period of three months. These mutants can be effectively propagated in vitro, which allows phenotypic evaluation already in the T0 generation. As such, phenotypes can be obtained within six months after transformation. As proof-of-principle, we mutated PanHK4, PanEIN2, PanNSP1 and PanNSP2. These genes are putatively involved in cytokinin and ethylene signaling and regulation of strigolactone biosynthesis, respectively. Additionally, orthologues of these genes perform essential symbiotic functions in legumes. Panhk4 and Panein2 knockout mutants display developmental phenotypes associated with reduced cytokinin and ethylene signaling. Analysis of Pannsp1 and Pannsp2 mutants revealed a conserved role for NSP1 and NSP2 in regulation of the strigolactone biosynthesis genes D27 and MAX1 and root nodule organogenesis. In contrast, symbiotic mutant phenotypes of Panhk4 and Panein2 mutants are different from their legume counterparts. This illustrates the value of Parasponia as comparative model - besides legumes - to study the genetics underlying rhizobium symbiosis.

Phylogenetic reconstruction showed that the Parasponia lineage is embedded in the non-nodulating Trema genus. This close relationship suggests that Parasponia and Trema only recently diverged in nodulation ability. In Chapter 6, I exploited this close relationship to question whether the nodulation trait is associated with gene expression differentiation. To this end, I sequenced root transcriptomes of two Parasponia and three Trema species. Principal component analysis separated all Parasponia samples from those of Trema along the first principal component. This component explains more than half of the observed variance, indicating that the root transcriptomes of two Parasponia species are distinct from that of the Trema sister species T. levigata, as well as the outgroup species T. orientalis and T. tomentosa. To determine, whether the transcriptional differences between Parasponia and Trema are relevant in a symbiotic context, I compared the list of differentially expressed genes to a list of genes that show nodule-enhanced expression in P. andersonii. This revealed significant enrichment of nodule-enhanced genes among genes that lower expressed in roots of Parasponia compared to Trema. Among the genes differentially expressed between Parasponia and Trema roots are several involved in mycorrhizal symbiosis as well as jasmonic acid biosynthesis. Measurements of hormone concentrations, showed that Parasponia and Trema roots harbor a difference in jasmonic acid/salicylic acid balance. However, mutants in jasmonic acid biosynthesis are unaffected in nodule development. Therefore, it remains a challenge to determine whether the difference in root transcriptomes between Parasponia and Trema are relevant in a symbiotic context.

In Chapter 7, I review hormone function in nitrogen-fixing nodule symbioses in legumes, Parasponia and actinorhizal species. In this chapter, I question whether different nodulating lineages recruited the same hormonal networks to function in nodule formation. Additionally, I discuss whether nodulating species harbor genetic adaptations in hormonal pathways that correlate with nodulation capacity.

Biochemical characterization of the tomato phosphatidylinositol-specific phospholipase C (PI-PLC) family and its role in plant immunity
Abd-El-Haliem, Ahmed ; Vossen, J.H. ; Zeijl, Arjan van; Dezhsetan, Sara ; Testerink, Christa ; Seidl, M.F. ; Beck, Martina ; Strutt, James ; Robatzek, Silke ; Joosten, M.H.A.J. - \ 2016
Biochimica et Biophysica Acta. Molecular and Cell Biology of Lipids 1861 (2016)9 Part B. - ISSN 1388-1981 - p. 1365 - 1378.
Defence response - Immune receptors - Phospholipids - PLC enzymes - Signal transduction

Plants possess effective mechanisms to quickly respond to biotic and abiotic stresses. The rapid activation of phosphatidylinositol-specific phospholipase C (PLC) enzymes occurs early after the stimulation of plant immune-receptors. Genomes of different plant species encode multiple PLC homologs belonging to one class, PLCζ. Here we determined whether all tomato homologs encode active enzymes and whether they can generate signals that are distinct from one another. We searched the recently completed tomato (Solanum lycopersicum) genome sequence and identified a total of seven PLCs. Recombinant proteins were produced for all tomato PLCs, except for SlPLC7. The purified proteins showed typical PLC activity, as different PLC substrates were hydrolysed to produce diacylglycerol. We studied SlPLC2, SlPLC4 and SlPLC5 enzymes in more detail and observed distinct requirements for Ca2+ ions and pH, for both their optimum activity and substrate preference. This indicates that each enzyme could be differentially and specifically regulated in vivo, leading to the generation of PLC homolog-specific signals in response to different stimuli. PLC overexpression and specific inhibition of PLC activity revealed that PLC is required for both specific effector- and more general "pattern"-triggered immunity. For the latter, we found that both the flagellin-triggered response and the internalization of the corresponding receptor, Flagellin Sensing 2 (FLS2) of Arabidopsis thaliana, are suppressed by inhibition of PLC activity. Altogether, our data support an important role for PLC enzymes in plant defence signalling downstream of immune receptors.This article is part of a Special Issue entitled: Plant Lipid Biology edited by Kent D. Chapman and Ivo Feussner.

The strigolactone biosynthesis gene DWARF27 is co-opted in rhizobium symbiosis
Zeijl, A.L. van; Liu, W. ; Xiao, T.T. ; Kohlen, W. ; Yang, W.C. ; Bisseling, T. ; Geurts, R. - \ 2015
BMC Plant Biology 15 (2015). - ISSN 1471-2229 - 15 p.
Background Strigolactones are a class of plant hormones whose biosynthesis is activated in response to phosphate starvation. This involves several enzymes, including the carotenoid cleavage dioxygenases 7 (CCD7) and CCD8 and the carotenoid isomerase DWARF27 (D27). D27 expression is known to be responsive to phosphate starvation. In Medicago truncatula and rice (Oryza sativa) this transcriptional response requires the GRAS-type proteins NSP1 and NSP2; both proteins are essential for rhizobium induced root nodule formation in legumes. In line with this, we questioned whether MtNSP1-MtNSP2 dependent MtD27 regulation is co-opted in rhizobium symbiosis. Results We provide evidence that MtD27 is involved in strigolactone biosynthesis in M. truncatula roots upon phosphate stress. Spatiotemporal expression studies revealed that this gene is also highly expressed in nodule primordia and subsequently becomes restricted to the meristem and distal infection zone of a mature nodules. A similar expression pattern was found for MtCCD7 and MtCCD8. Rhizobium lipo-chitooligosaccharide (LCO) application experiments revealed that of these genes MtD27 is most responsive in an MtNSP1 and MtNSP2 dependent manner. Symbiotic expression of MtD27 requires components of the symbiosis signaling pathway; including MtDMI1, MtDMI2, MtDMI3/MtCCaMK and in part MtERN1. This in contrast to MtD27 expression upon phosphate starvation, which only requires MtNSP1 and MtNSP2. Conclusion Our data show that the phosphate-starvation responsive strigolactone biosynthesis gene MtD27 is also rapidly induced by rhizobium LCO signals in an MtNSP1 and MtNSP2-dependent manner. Additionally, we show that MtD27 is co-expressed with MtCCD7 and MtCCD8 in nodule primordia and in the infection zone of mature nodules.
Lipochitooligosaccharides modulate plant host immunity to enable endosymbioses
Limpens, E.H.M. ; Zeijl, A.L. van; Geurts, R. - \ 2015
Annual Review of Phytopathology 53 (2015). - ISSN 0066-4286 - p. 311 - 334.
Symbiotic nitrogen-fixing rhizobium bacteria and arbuscular mycorrhizal fungi use lipochitooligosaccharide (LCO) signals to communicate with potential host plants. Upon a compatible match, an intimate relation is established during which the microsymbiont is allowed to enter root (-derived) cells. Plants perceive microbial LCO molecules by specific LysM-domain-containing receptor-like kinases. These do not only activate a common symbiosis signaling pathway that is shared in both symbioses but also modulate innate immune responses. Recent studies revealed that symbiotic LCO receptors are closely related to chitin innate immune receptors, and some of these receptors even function in symbiosis as well as immunity. This raises questions about how plants manage to translate structurally very similar microbial signals into different outputs. Here, we describe the current view on chitin and LCO perception in innate immunity and endosymbiosis and question how LCOs might modulate the immune system. Furthermore, we discuss what it takes to become an endosymbiont.
Rhizobium lipo-chitooligosaccharide signaling triggers accumulation of cytokinins in Medicago truncatula roots
Zeijl, A.L. van; Camp, R.H.M. Op den; Deinum, E.E. ; Charnikhova, T. ; Franssen, H. ; Camp, H.J.M. op den; Bouwmeester, H.J. ; Kohlen, W. ; Bisseling, T. ; Geurts, R. - \ 2015
Molecular Plant 8 (2015)8. - ISSN 1674-2052 - p. 1213 - 1226.
Legume rhizobium symbiosis is initiated upon perception of bacterial secreted lipo-chitooligosaccharides (LCOs). Perception of these signals by the plant initiates a signaling cascade that leads to nodule formation. Several studies have implicated a function for cytokinin in this process. However, whether cytokinin accumulation and subsequent signaling are an integral part of rhizobium LCO signaling remains elusive. Here, we show that cytokinin signaling is required for the majority of transcriptional changes induced by rhizobium LCOs. In addition, we demonstrate that several cytokinins accumulate in the root susceptible zone 3 h after rhizobium LCO application, including the biologically most active cytokinins, trans-zeatin and isopentenyl adenine. These responses are dependent on calcium- and calmodulin-dependent protein kinase (CCaMK), a key protein in rhizobial LCO-induced signaling. Analysis of the ethylene-insensitive Mtein2/Mtsickle mutant showed that LCO-induced cytokinin accumulation is negatively regulated by ethylene. Together with transcriptional induction of ethylene biosynthesis genes, it suggests a feedback loop negatively regulating LCO signaling and subsequent cytokinin accumulation. We argue that cytokinin accumulation is a key step in the pathway leading to nodule organogenesis and that this is tightly controlled by feedback loops.
Conceptualising joint knowledge production in regional climate change adaptation projects: success conditions and levers for action
Hegger, D.L.T. ; Lamers, M.A.J. ; Zeijl-Rozema, A. van; Dieperink, C. - \ 2012
Environmental Science & Policy 18 (2012)4. - ISSN 1462-9011 - p. 52 - 65.
klimaatverandering - organisatie van onderzoek - wetenschappelijke samenwerking - climatic change - organization of research - scientific cooperation - transdisciplinary research - water-management - science-policy - sustainable development - boundary organizations - environmental-policy - governance - coproduction - stakeholders - perspectives
Matching supply and demand for knowledge in the fields of global change and sustainability is a daunting task. Science and public policy differ in their timeframes, epistemologies, objectives, process-cycles and criteria for judging the quality of knowledge, while global change and sustainability issues involve value pluralities and large uncertainties. In literature and in practice, it is argued that joint knowledge production in projects through collaboration between (and within) science and policy serves as a means to bridge the gap between the two domains. However, an assessment framework for analysing the merits and limitations of such projects, identifying good practices and enabling adaptive management as well as social learning had not yet been developed. This paper aims to develop such a framework. We portray joint knowledge production projects as policy arrangements in which the degree of success depends on the actors involved, contents of dominant discourses, presence of rules and the availability of resources. Literature was discussed to specify these four dimensions into seven success conditions for joint knowledge production. Scholars, boundary organizations and actors in projects can use the framework for retrospective analyses of projects, providing joint knowledge production with the empirical basis it still requires. The framework can also be used for promoting reflection in action as well as for formative assessments enabling social learning.
Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: Another below-ground role for strigolactones?
Ruyter-Spira, C.P. ; Kohlen, W. ; Charnikhova, T. ; Zeijl, A. van; Bezouwen, L. van; Ruijter, N.C.A. de; Cardoso, C. ; Lopez Raez, J.A. ; Matusova, R. ; Bours, R.M.E.H. ; Verstappen, F.W.A. ; Bouwmeester, H.J. - \ 2011
Plant Physiology 155 (2011)2. - ISSN 0032-0889 - p. 721 - 734.
dependent auxin gradients - vascular differentiation - phosphate starvation - apical dominance - acts downstream - transport - efflux - initiation - thaliana - biosynthesis
In this study, the role of the recently identified class of phytohormones, strigolactones, in shaping root architecture was addressed. Primary root lengths of strigolactone-deficient and -insensitive Arabidopsis (Arabidopsis thaliana) plants were shorter than those of wild-type plants. This was accompanied by a reduction in meristem cell number, which could be rescued by application of the synthetic strigolactone analog GR24 in all genotypes except in the strigolactone-insensitive mutant. Upon GR24 treatment, cells in the transition zone showed a gradual increase in cell length, resulting in a vague transition point and an increase in transition zone size. PIN1/3/7-green fluorescent protein intensities in provascular tissue of the primary root tip were decreased, whereas PIN3-green fluorescent protein intensity in the columella was not affected. During phosphate-sufficient conditions, GR24 application to the roots suppressed lateral root primordial development and lateral root forming potential, leading to a reduction in lateral root density. Moreover, auxin levels in leaf tissue were reduced. When auxin levels were increased by exogenous application of naphthylacetic acid, GR24 application had a stimulatory effect on lateral root development instead. Similarly, under phosphate-limiting conditions, endogenous strigolactones present in wild-type plants stimulated a more rapid outgrowth of lateral root primordia when compared with strigolactone-deficient mutants. These results suggest that strigolactones are able to modulate local auxin levels and that the net result of strigolactone action is dependent on the auxin status of the plant. We postulate that the tightly balanced auxin-strigolactone interaction is the basis for the mechanism of the regulation of the plants’ root-to-shoot ratio.
Workshop on integrated land use modelling: issue driven research
Zeijl, A. van; Schoorl, J.M. - \ 1997
LUCC Newsletter (1997)1. - ISSN 1137-5558 - p. 13 - 13.
Land use and land cover change: The LUCC science plan in Europe
Zeijl, A. van; Fresco, L.O. - \ 1997
LUCC Newsletter 1 (1997). - ISSN 1137-5558 - p. 11 - 12.
Land use and cover change (LUCC). Open science meeting.
Fresco, L.O. ; Leemans, R. ; Turner Ii, B.L. ; Skole, D. ; Zeijl-Rozema, A.E. van; Haarmann, V. - \ 1997
In: Land Use and Cover Change (LUCC) Open Science Meeting Proceedings: Amsterdam, The Netherlands, January 29th - 31th, 1996 / Fresco, L., Barcelona : Institut Cartogràfic de Catalunya (LUCC report series 1)
The dynamics of land use change.
Fresco, L.O. ; Leemans, R. ; Zeijl-Rozema, A.E. van - \ 1996
Land Use Policy 13 (1996). - ISSN 0264-8377 - p. 332 - 334.
An inventory of land use research.
Zeijl-Rozema, A.E. van; Fresco, L.O. ; Berg, M.M. van den - \ 1996
Change 32 (1996). - ISSN 0925-5478 - p. 14 - 16.
Land use and cover change as an overarching topic in the Dutch National Research Programme on Global Air Pollution and Climate Change : issues for implementation
Fresco, L.O. ; Berg, M.M. van den; Zeijl-Rozema, A.E. van - \ 1996
Bilthoven : RIVM (Report / RIVM 410 200 005) - 42
ruimtelijke ordening - landgebruik - zonering - klimaatverandering - paleoklimatologie - physical planning - land use - zoning - climatic change - palaeoclimatology
The integration study 'Land Use and Cover Change as an overarching topic in the Dutch National Research Programme on Global Air Pollution and Climate Change (NRP)' aims at identifying research fields in which the NRP can contribute most effectively to the international scientific know-how of the interactions between land use/cover and global change. Goals of the study were: the initiation of integration of NRP land use/cover projects; the formulation of Dutch views on national and international research on land use and cover change (LUCC); and the preparation of an NRP agenda for research on land use/cover in relation to climate change. Land use/cover change is a very broad field of research and it is impossible to cover the whole subject within the NRP. Important Dutch land use/cover research topics are at present: the influence of the land cover on biogeochemical cycles; land cover distribution; the influence of climate change on crop growth; the use of biomass for energy supply; and land use/cover modelling. Tropical areas as well as the Netherlands, Europe and the global perspective are studied. Within the NRP, the biophysical side of land use/cover change has received most attention. A concerted effort is required to focus Dutch Land Use/Cover research more effectively in order to: optimise the Dutch inputs into the international arena (IGBP, IHDP, etc.). Define areas of complementarity in which Dutch research and policy can best benefit directly or indirectly from international research efforts.
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