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Staff Publications

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Archaeal and bacterial diversity and community composition from 18 phylogenetically divergent sponge species in Vietnam
Dat, Ton That Huu ; Steinert, Georg ; Cuc, Nguyen Thi Kim ; Smidt, Hauke ; Sipkema, Detmer - \ 2018
PeerJ 6 (2018). - ISSN 2167-8359
16S rRNA - Porifera - Prokaryotic diversity - Symbiosis - Vietnam
Sponge-associated prokaryotic diversity has been studied from a wide range of marine environments across the globe. However, for certain regions, e.g., Vietnam, Thailand, Cambodia, and Singapore, an overview of the sponge-associated prokaryotic communities is still pending. In this study we characterized the prokaryotic communities from 27 specimens, comprising 18 marine sponge species, sampled from the central coastal region of Vietnam. Illumina MiSeq sequencing of 16S ribosomal RNA (rRNA) gene fragments was used to investigate spongeassociated bacterial and archaeal diversity. Overall, 14 bacterial phyla and one archaeal phylum were identified among all 27 samples. The phylum Proteobacteria was present in all sponges and the most prevalent phylum in 15 out of 18 sponge species, albeit with pronounced differences at the class level. In contrast, Chloroflexi was the most abundant phylum in Halichondria sp., whereas Spirastrella sp. and Dactylospongia sp. were dominated by Actinobacteria. Several bacterial phyla such as Acidobacteria, Actinobacteria, Bacteroidetes, Chloroflexi, Deferribacteres, Gemmatimonadetes, and Nitrospirae were found in two-thirds of the sponge species. Moreover, the phylum Thaumarchaeota (Archaea), which is known to comprise nitrifying archaea, was highly abundant among the majority of the 18 investigated sponge species. Altogether, this study demonstrates that the diversity of prokaryotic communities associated with Vietnamese sponges is comparable to spongeprokaryotic assemblages from well-documented regions. Furthermore, the phylogenetically divergent sponges hosted species-specific prokaryotic communities, thus demonstrating the influence of host identity on the composition and diversity of the associated communities. Therefore, this high-throughput 16S rRNA gene amplicon analysis of Vietnamese sponge-prokaryotic communities provides a foundation for future studies on sponge symbiont function and sponge-derived bioactive compounds from this region.
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.
Strigolactone levels in dicot roots are determined by an ancestral symbiosis-regulated clade of the PHYTOENE SYNTHASE gene family
Stauder, Ron ; Welsch, Ralf ; Camagna, Maurizio ; Kohlen, Wouter ; Balcke, Gerd U. ; Tissier, Alain ; Walter, Michael H. - \ 2018
Frontiers in Plant Science 9 (2018). - ISSN 1664-462X
Apocarotenoids - Arbuscular mycorrhiza - Carotenoids - Medicago truncatula - Solanum lycopersicum - Strigolactones - Symbiosis
Strigolactones (SLs) are apocarotenoid phytohormones synthesized from carotenoid precursors. They are produced most abundantly in roots for exudation into the rhizosphere to cope with mineral nutrient starvation through support of root symbionts. Abscisic acid (ABA) is another apocarotenoid phytohormone synthesized in roots, which is involved in responses to abiotic stress. Typically low carotenoid levels in roots raise the issue of precursor supply for the biosynthesis of these two apocarotenoids in this organ. Increased ABA levels upon abiotic stress in Poaceae roots are known to be supported by a particular isoform of phytoene synthase (PSY), catalyzing the rate-limiting step in carotenogenesis. Here we report on novel PSY3 isogenes from Medicago truncatula (MtPSY3) and Solanum lycopersicum (SlPSY3) strongly expressed exclusively upon root interaction with symbiotic arbuscular mycorrhizal (AM) fungi and moderately in response to phosphate starvation. They belong to a widespread clade of conserved PSYs restricted to dicots (dPSY3) distinct from the Poaceae-PSY3s involved in ABA formation. An ancient origin of dPSY3s and a potential co-evolution with the AM symbiosis is discussed in the context of PSY evolution. Knockdown of MtPSY3 in hairy roots of M. truncatula strongly reduced SL and AM-induced C13 α-ionol/C14 mycorradicin apocarotenoids. Inhibition of the reaction subsequent to phytoene synthesis revealed strongly elevated levels of phytoene indicating induced flux through the carotenoid pathway in roots upon mycorrhization. dPSY3 isogenes are coregulated with upstream isogenes and downstream carotenoid cleavage steps toward SLs (D27, CCD7, CCD8) suggesting a combined carotenoid/apocarotenoid pathway, which provides “just in time”-delivery of precursors for apocarotenoid formation.
Enzyme activities at different stages of plant biomass decomposition in three species of fungusgrowing termites
Costa, Rafael R. da; Hu, Haofu ; Pilgaard, Bo ; Sabine, Sabine M. ; Schückel, Julia ; Pedersen, Kristine S.K. ; Kračun, Stjepan K. ; Busk, Peter K. ; Harholt, Jesper ; Sapountzis, Panagiotis ; Lange, Lene ; Aanen, Duur K. ; Poulsen, Michael - \ 2018
Applied and Environmental Microbiology 84 (2018)5. - ISSN 0099-2240
AZCL - Chromogenic substrates - HPLC - Macrotermes - Odontotermes - Peptide pattern recognition - Plant substrate - RNA-seq - Symbiosis - Termitomyces
Fungus-growing termites rely on mutualistic fungi of the genus Termitomyces and gut microbes for plant biomass degradation. Due to a certain degree of symbiont complementarity, this tripartite symbiosis has evolved as a complex bioreactor, enabling decomposition of nearly any plant polymer, likely contributing to the success of the termites as one of the main plant decomposers in the Old World. In this study, we evaluated which plant polymers are decomposed and which enzymes are active during the decomposition process in two major genera of fungus-growing termites. We found a diversity of active enzymes at different stages of decomposition and a consistent decrease in plant components during the decomposition process. Furthermore, our findings are consistent with the hypothesis that termites transport enzymes from the older mature parts of the fungus comb through young worker guts to freshly inoculated plant substrate. However, preliminary fungal RNA sequencing (RNA-seq) analyses suggest that this likely transport is supplemented with enzymes produced in situ. Our findings support that the maintenance of an external fungus comb, inoculated with an optimal mixture of plant material, fungal spores, and enzymes, is likely the key to the extraordinarily efficient plant decomposition in fungus-growing termites.
Low intraspecific genetic diversity indicates asexuality and vertical transmission in the fungal cultivars of ambrosia beetles
Peppel, L.J.J. van de; Aanen, D.K. ; Biedermann, P.H.W. - \ 2018
Fungal Ecology 32 (2018). - ISSN 1754-5048 - p. 57 - 64.
Ambrosia fungus - Ambrosiella - Anisandrus - Asexuality - Clonal fungiculture - Genetic diversity - Symbiosis - Vertical transmission - Xylosandrus
Ambrosia beetles farm ascomycetous fungi in tunnels within wood. These ambrosia fungi are regarded asexual, although population genetic proof is missing. Here we explored the intraspecific genetic diversity of Ambrosiella grosmanniae and Ambrosiella hartigii (Ascomycota: Microascales), the mutualists of the beetles Xylosandrus germanus and Anisandrus dispar. By sequencing five markers (ITS, LSU, TEF1α RPB2, β-tubulin) from several fungal strains, we show that X. germanus cultivates the same two clones of A. grosmanniae in the USA and in Europe, whereas A. dispar is associated with a single A. hartigii clone across Europe. This low genetic diversity is consistent with predominantly asexual vertical transmission of Ambrosiella cultivars between beetle generations. This clonal agriculture is a remarkable case of convergence with fungus-farming ants, given that both groups have a completely different ecology and evolutionary history.
Short communication : Growth of dairy isolates of Geobacillus thermoglucosidans in skim milk depends on lactose degradation products supplied by Anoxybacillus flavithermus as secondary species
Zhao, Y. ; Kumar, M. ; Caspers, M.P.M. ; Nierop Groot, M.N. ; Vossen, J.M.B.M. van der; Abee, T. - \ 2018
Journal of Dairy Science 101 (2018)2. - ISSN 0022-0302 - p. 1013 - 1019.
Symbiosis - Thermophile - Thermoresistant spore
Thermophilic bacilli such as Anoxybacillus and Geobacillus are important contaminants in dairy powder products. Remarkably, one of the common contaminants, Geobacillus thermoglucosidans, showed poor growth in skim milk, whereas significant growth of G. thermoglucosidans was observed in the presence of an Anoxybacillus flavithermus dairy isolate. In the present study, we investigated the underlying reason for this growth dependence of G. thermoglucosidans. Whole-genome sequences of 4 A. flavithermus strains and 4 G. thermoglucosidans strains were acquired, with special attention given to carbohydrate utilization clusters and proteolytic enzymes. Focusing on traits relevant for dairy environments, comparative genomic analysis revealed that all G. thermoglucosidans strains lacked the genes necessary for lactose transport and metabolism, showed poor growth in skim milk, and produced white colonies on X-gal plates, indicating the lack of β-galactosidase activity. The A. flavithermus isolates scored positive in these tests, consistent with the presence of a putative lactose utilization gene cluster. All tested isolates from both species showed proteolytic activity on milk plate count agar plates. Adding glucose or galactose to liquid skim milk supported growth of G. thermoglucosidans isolates, in line with the presence of the respective monosaccharide utilization gene clusters in the genomes. Analysis by HPLC of A. flavithermus TNO-09.006 culture filtrate indicated that the previously described growth dependence of G. thermoglucosidans in skim milk was based on the supply of glucose and galactose by A. flavithermus TNO-09.006.
The sponge microbiome project
Moitinho-Silva, Lucas ; Nielsen, Shaun ; Amir, Amnon ; Gonzalez, Antonio ; Ackermann, Gail L. ; Cerrano, Carlo ; Astudillo-Garcia, Carmen ; Easson, Cole ; Sipkema, Detmer ; Liu, Fang ; Steinert, Georg ; Kotoulas, Giorgos ; McCormack, Grace P. ; Feng, Guofang ; Bell, James J. ; Vicente, Jan ; Björk, Johannes R. ; Montoya, Jose M. ; Olson, Julie B. ; Reveillaud, Julie ; Steindler, Laura ; Pineda, Mari Carmen ; Marra, Maria V. ; Ilan, Micha ; Taylor, Michael W. ; Polymenakou, Paraskevi ; Erwin, Patrick M. ; Schupp, Peter J. ; Simister, Rachel L. ; Knight, Rob ; Thacker, Robert W. ; Costa, Rodrigo ; Hill, Russell T. ; Lopez-Legentil, Susanna ; Dailianis, Thanos ; Ravasi, Timothy ; Hentschel, Ute ; Li, Zhiyong ; Webster, Nicole S. ; Thomas, Torsten - \ 2017
GigaScience 6 (2017)10. - ISSN 2047-217X
16S rRNA gene - Archaea - Bacteria - Marine sponges - Microbial diversity - Microbiome - Symbiosis
Marine sponges (phylum Porifera) are a diverse, phylogenetically deep-branching clade known for forming intimate partnerships with complex communities of microorganisms. To date, 16S rRNA gene sequencing studies have largely utilised different extraction and amplification methodologies to target the microbial communities of a limited number of sponge species, severely limiting comparative analyses of sponge microbial diversity and structure. Here, we provide an extensive and standardised dataset that will facilitate sponge microbiome comparisons across large spatial, temporal, and environmental scales. Samples from marine sponges (n = 3569 specimens), seawater (n = 370), marine sediments (n = 65) and other environments (n = 29) were collected from different locations across the globe. This dataset incorporates at least 268 different sponge species, including several yet unidentified taxa. The V4 region of the 16S rRNA gene was amplified and sequenced from extracted DNA using standardised procedures. Raw sequences (total of 1.1 billion sequences) were processed and clustered with (i) a standard protocol using QIIME closed-reference picking resulting in 39 543 operational taxonomic units (OTU) at 97% sequence identity, (ii) a de novo clustering using Mothur resulting in 518 246 OTUs, and (iii) a new high-resolution Deblur protocol resulting in 83 908 unique bacterial sequences. Abundance tables, representative sequences, taxonomic classifications, and metadata are provided. This dataset represents a comprehensive resource of sponge-associated microbial communities based on 16S rRNA gene sequences that can be used to address overarching hypotheses regarding host-associated prokaryotes, including host specificity, convergent evolution, environmental drivers of microbiome structure, and the sponge-associated rare biosphere.
Fungi found in Mediterranean and North Sea sponges : How specific are they?
Naim, Mohd Azrul ; Smidt, Hauke ; Sipkema, Detmer - \ 2017
PeerJ 2017 (2017)9. - ISSN 2167-8359
Fungi - Malasseziales - Marine sponge - Symbiosis - Yeast
Fungi and other eukaryotes represent one of the last frontiers of microbial diversity in the sponge holobiont. In this study we employed pyrosequencing of 18S ribosomal RNA gene amplicons containing the V7 and V8 hypervariable regions to explore the fungal diversity of seven sponge species from the North Sea and the Mediterranean Sea. For most sponges, fungi were present at a low relative abundance averaging 0.75% of the 18S rRNA gene reads. In total, 44 fungal OTUs (operational taxonomic units) were detected in sponges, and 28 of these OTUs were also found in seawater. Twentytwo of the sponge-associated OTUs were identified as yeasts (mainly Malasseziales), representing 84% of the fungal reads. Several OTUs were related to fungal sequences previously retrieved from other sponges, but all OTUs were also related to fungi from other biological sources, such as seawater, sediments, lakes and anaerobic digesters. Therefore our data, supported by currently available data, point in the direction of mostly accidental presence of fungi in sponges and do not support the existence of a sponge-specific fungal community.
Predicting the HMA-LMA status in marine sponges by machine learning
Moitinho-Silva, Lucas ; Steinert, Georg ; Nielsen, Shaun ; Hardoim, Cristiane C.P. ; Wu, Yu Chen ; McCormack, Grace P. ; López-Legentil, Susanna ; Marchant, Roman ; Webster, Nicole ; Thomas, Torsten ; Hentschel, Ute - \ 2017
Frontiers in Microbiology 8 (2017). - ISSN 1664-302X - 14 p.
16S rRNA gene - Marine sponges - Microbial diversity - Microbiome - Random forest - Symbiosis

The dichotomy between high microbial abundance (HMA) and low microbial abundance (LMA) sponges has been observed in sponge-microbe symbiosis, although the extent of this pattern remains poorly unknown. We characterized the differences between the microbiomes of HMA (n = 19) and LMA (n = 17) sponges (575 specimens) present in the Sponge Microbiome Project. HMA sponges were associated with richer and more diverse microbiomes than LMA sponges, as indicated by the comparison of alpha diversity metrics. Microbial community structures differed between HMA and LMA sponges considering Operational Taxonomic Units (OTU) abundances and across microbial taxonomic levels, from phylum to species. The largest proportion of microbiome variation was explained by the host identity. Several phyla, classes, and OTUs were found differentially abundant in either group, which were considered "HMA indicators" and "LMA indicators." Machine learning algorithms (classifiers) were trained to predict the HMA-LMA status of sponges. Among nine different classifiers, higher performances were achieved by Random Forest trained with phylum and class abundances. Random Forest with optimized parameters predicted the HMA-LMA status of additional 135 sponge species (1,232 specimens) without a priori knowledge. These sponges were grouped in four clusters, from which the largest two were composed of species consistently predicted as HMA (n = 44) and LMA (n = 74). In summary, our analyses shown distinct features of the microbial communities associated with HMA and LMA sponges. The prediction of the HMA-LMA status based on the microbiome profiles of sponges demonstrates the application of machine learning to explore patterns of host-associated microbial communities.

Comparative analysis of spatial genetic structure in an ant-plant symbiosis reveals a tension zone and highlights speciation processes in tropical Africa
Blatrix, Rumsaïs ; Peccoud, Jean ; Born, Céline ; Piatscheck, Finn ; Benoit, Laure ; Sauve, Mathieu ; Djiéto-Lordon, Champlain ; Atteke, Christiane ; Wieringa, Jan J. ; Harris, David J. ; Mckey, Doyle - \ 2017
Journal of Biogeography 44 (2017)8. - ISSN 0305-0270 - p. 1856 - 1868.
Africa - Barteria - Climatic oscillations - Guinea-Congolian rainforest - Incipient speciation - Phylogeography - Pleistocene - Symbiosis - Tension zone - Tetraponera

Aim: Pleistocene climatic oscillations induced range fluctuations in African rain forest organisms and may have shaped species diversification through allopatric speciation events. We compared the spatial genetic structure of two forest species that live in obligate symbiosis and thus must have experienced the same range fluctuations, as a means to discriminate incipient speciation from transient differentiation simply resulting from past divergence. Location: Western central Africa. Methods: We genotyped 765 individuals of the tree Barteria fistulosa and 605 colonies of its symbiotic ant Tetraponera aethiops at 12 and 13 microsatellite loci, respectively. We compared the spatial genetic structure of the two symbionts by using Bayesian clustering algorithms, isolation-by-distance analyses and clines of synthetic alleles. We used species niche modelling (climatic and soil variables) to investigate ecological variables associated with genetic discontinuities in tree populations. Results: The trees and the ants showed congruent patterns of spatial genetic structure. However, the trees showed a very steep genetic discontinuity between groups north and south of latitude 1° N, which was much weaker in the ants. There was no evidence for effective gene flow between the two tree lineages in contact at the transition zone, despite the presence of a few hybrids. Niche modelling did not predict the occurrence of northern trees south of this genetic transition, and vice versa. Main conclusions: The genetic discontinuity near latitude 1° N is inferred to be a tension zone resulting from reproductive incompatibilities between previously allopatric tree lineages. This tension zone may have stabilized at a climatic transition (between boreal and austral seasonal regimes), and matches patterns of genetic structure previously observed in other forest plant species. Our results illustrate independent speciation between two species that live in specific and obligate symbiosis and suggest that a tension zone may separate lineages of several central African forest plants near the thermal equator.

Commonalities in Symbiotic Plant-Microbe Signalling
Holmer, R. ; Rutten, L.J.J. ; Kohlen, W. ; Velzen, R. van; Geurts, R. - \ 2017
Advances in Botanical Research 82 (2017). - ISSN 0065-2296 - p. 187 - 221.
Ectomycorrhiza - Endomycorrhiza - Frankia - Rhizobium - Symbiosis

Plants face the problem that they have to discriminate symbionts from a diverse pool of soil microbes, including pathogens. Studies on different symbiotic systems revealed commonalities in plant-microbe signalling. In this chapter we focus on four intimate symbiotic interactions: two mycorrhizal ones, with arbuscular- and ectomycorrhizal fungi, and two nitrogen-fixing ones, with rhizobium and Frankia bacteria. Comparing these systems uncovered commonalities in the way plants attract their symbiotic partners. Especially flavonoids, and in a lesser extent strigolactones, are pivotal plant signals that are perceived by the microsymbiont. In response, signal molecules are exuded by the microbes to trigger symbiotic responses in their host plant. Strikingly, microbes that establish an endosymbiotic relation with their host plant, namely arbuscular mycorrhizal fungi, rhizobium and Frankia bacteria, make use of a symbiotic signalling network that is highly conserved in plants. The use of flavonoids as attractants for symbiotic microbes, in combination with the use of a common plant signalling network to establish endosymbioses, raises questions about how plants manage to discriminate their microbial partners.

In four shallow and mesophotic tropical reef sponges from Guam the microbial community largely depends on host identity
Steinert, Georg ; Taylor, Michael W. ; Deines, Peter ; Simister, Rachel L. ; Voogd, Nicole J. De; Hoggard, Michael ; Schupp, Peter J. - \ 2016
PeerJ 2016 (2016)4. - ISSN 2167-8359
16S rRNA - Environmental variability - Microbial diversity - Porifera - Pyrosequencing - Symbiosis

Sponges (phylum Porifera) are important members of almost all aquatic ecosystems, and are renowned for hosting often dense and diverse microbial communities. While the specificity of the sponge microbiota seems to be closely related to host phylogeny, the environmental factors that could shape differences within local sponge-specific communities remain less understood. On tropical coral reefs, sponge habitats can span from shallow areas to deeper, mesophotic sites. These habitats differ in terms of environmental factors such as light, temperature, and food availability, as well as anthropogenic impact. In order to study the host specificity and potential influence of varying habitats on the sponge microbiota within a local area, four tropical reef sponges, Rhabdastrella globostellata, Callyspongia sp., Rhaphoxya sp., and Acanthella cavernosa, were collected from exposed shallow reef slopes and a deep reef drop-off. Based on 16S rRNA gene pyrosequencing profiles, beta diversity analyses revealed that each sponge species possessed a specific microbiota that was significantly different to those of the other species and exhibited attributes that are characteristic of high- and/or lowmicrobial- abundance sponges. These findings emphasize the influence of host identity on the associated microbiota. Dominant sponge- and seawater-associated bacterial phyla were Chloroflexi, Cyanobacteria, and Proteobacteria. Comparison of individual sponge taxa and seawater samples between shallow and deep reef sites revealed no significant variation in alpha diversity estimates, while differences in microbial beta diversity (variation in community composition) were significant for Callyspongia sp. sponges and seawater samples. Overall, the sponge-associated microbiota is significantly shaped by host identity across all samples, while the effect of habitat differentiation seems to be less predominant in tropical reef sponges.

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.

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