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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    Experimental demonstration of the benefits of somatic fusion and the consequences for allorecognition
    Bastiaans, E. ; Debets, A.J.M. ; Aanen, D.K. - \ 2015
    Evolution 69 (2015)4. - ISSN 0014-3820 - p. 1091 - 1099.
    vegetative incompatibility - neurospora-crassa - heterokaryon incompatibility - natural-populations - filamentous fungi - recognition - evolution - selection - genetics - cooperation
    Allorecognition, the ability to distinguish “self” from “nonself” based on allelic differences at allorecognition loci, is common in all domains of life. Allorecognition restricts the opportunities for social parasitism, and is therefore crucial for the evolution of cooperation. However, the maintenance of allorecognition diversity provides a paradox. If allorecognition is costly relative to cooperation, common alleles will be favored. Thus, the cost of allorecognition may reduce the genetic variation upon which allorecognition crucially relies, a prediction now known as “Crozier's paradox.” We establish the relative costs of allorecognition, and their consequences for the short-term evolution of recognition labels theoretically predicted by Crozier. We use fusion among colonies of the fungus Neurospora crassa, regulated by highly variable allorecognition genes, as an experimental model system. We demonstrate that fusion among colonies is mutually beneficial, relative to absence of fusion upon allorecognition. This benefit is due not only to absence of mutual antagonism, which occurs upon allorecognition, but also to an increase in colony size per se. We then experimentally demonstrate that the benefit of fusion selects against allorecognition diversity, as predicted by Crozier. We discuss what maintains allorecognition diversity
    Signal Transduction by a Fungal NOD-Like Receptor Based on Propagation of a Prion Amyloid Fold
    Daskalov, A. ; Habenstein, B. ; Martinez, D. ; Debets, A.J.M. ; Sabate, R. ; Loquet, A. ; Saupe, S.J. - \ 2015
    PloS Biology 13 (2015)2. - ISSN 1545-7885
    het-s prion - state nmr-spectroscopy - non-self recognition - heterokaryon incompatibility gene - glycolipid transfer protein - podospora-anserina - vegetative incompatibility - cell-death - het-s(218-289) prion - diversity
    In the fungus Podospora anserina, the [Het-s] prion induces programmed cell death by activating the HET-S pore-forming protein. The HET-s ß-solenoid prion fold serves as a template for converting the HET-S prion-forming domain into the same fold. This conversion, in turn, activates the HET-S pore-forming domain. The gene immediately adjacent to het-S encodes NWD2, a Nod-like receptor (NLR) with an N-terminal motif similar to the elementary repeat unit of the ß-solenoid fold. NLRs are immune receptors controlling cell death and host defense processes in animals, plants and fungi. We have proposed that, analogously to [Het-s], NWD2 can activate the HET-S pore-forming protein by converting its prion-forming region into the ß-solenoid fold. Here, we analyze the ability of NWD2 to induce formation of the ß-solenoid prion fold. We show that artificial NWD2 variants induce formation of the [Het-s] prion, specifically in presence of their cognate ligands. The N-terminal motif is responsible for this prion induction, and mutations predicted to affect the ß-solenoid fold abolish templating activity. In vitro, the N-terminal motif assembles into infectious prion amyloids that display a structure resembling the ß-solenoid fold. In vivo, the assembled form of the NWD2 N-terminal region activates the HET-S pore-forming protein. This study documenting the role of the ß-solenoid fold in fungal NLR function further highlights the general importance of amyloid and prion-like signaling in immunity-related cell fate pathways
    Natural Variation of Heterokaryon Incompatibility Gene het-c in Podospora anserina Reveals Diversifying Selection
    Bastiaans, E. ; Debets, A.J.M. ; Aanen, D.K. ; Diepeningen, A.D. van; Saupe, S.J. ; Paoletti, M. - \ 2014
    Molecular Biology and Evolution 31 (2014)4. - ISSN 0737-4038 - p. 962 - 974.
    plant immune-system - glycolipid transfer protein - chestnut blight fungus - amino-acid sites - vegetative incompatibility - neurospora-crassa - cell-death - cryphonectria-parasitica - membrane interaction - filamentous fungi
    In filamentous fungi, allorecognition takes the form of heterokaryon incompatibility, a cell death reaction triggered when genetically distinct hyphae fuse. Heterokaryon incompatibility is controlled by specific loci termed het-loci. In this article, we analyzed the natural variation in one such fungal allorecognition determinant, the het-c heterokaryon incompatibility locus of the filamentous ascomycete Podospora anserina. The het-c locus determines an allogenic incompatibility reaction together with two unlinked loci termed het-d and het-e. Each het-c allele is incompatible with a specific subset of the het-d and het-e alleles. We analyzed variability at the het-c locus in a population of 110 individuals, and in additional isolates from various localities. We identified a total of 11 het-c alleles, which define 7 distinct incompatibility specificity classes in combination with the known het-d and het-e alleles. We found that the het-c allorecognition gene of P. anserina is under diversifying selection. We find a highly unequal allele distribution of het-c in the population, which contrasts with the more balanced distribution of functional groups of het-c based on their allorecognition function. One explanation for the observed het-c diversity in the population is its function in allorecognition. However, alleles that are most efficient in allorecognition are rare. An alternative and not exclusive explanation for the observed diversity is that het-c is involved in pathogen recognition. In Arabidopsis thaliana, a homolog of het-c is a pathogen effector target, supporting this hypothesis. We hypothesize that the het-c diversity in P. anserina results from both its functions in pathogen-defense, and allorecognition
    Selection against somatic parasitism can maintain allorecognition in fungi
    Czaran, T. ; Hoekstra, R.F. ; Aanen, D.K. - \ 2014
    Fungal Genetics and Biology 73 (2014). - ISSN 1087-1845 - p. 128 - 137.
    vegetative incompatibility - neurospora-crassa - kin discrimination - filamentous fungi - self-recognition - botryllus-schlosseri - marine-invertebrates - ascomycete fungi - cell parasitism - genetic-control
    Fusion between multicellular individuals is possible in many organisms with modular, indeterminate growth, such as marine invertebrates and fungi. Although fusion may provide various benefits, fusion usually is restricted to close relatives by allorecognition, also called heterokaryon or somatic incompatibility in fungi. A possible selective explanation for allorecognition is protection against somatic parasites. Such mutants contribute less to colony functions but more to reproduction. However, previous models testing this idea have failed to explain the high diversity of allorecognition alleles in nature. These models did not, however, consider the possible role of spatial structure. We model the joint evolution of allorecognition and somatic parasitism in a multicellular organism resembling an asexual ascomycete fungus in a spatially explicit simulation. In a 1000-by-1000 grid, neighbouring individuals can fuse, but only if they have the same allotype. Fusion with a parasitic individual decreases the total reproductive output of the fused individuals, but the parasite compensates for this individual-level fitness reduction by a disproportional share of the offspring. Allorecognition prevents the invasion of somatic parasites, and vice versa, mutation towards somatic parasitism provides the selective conditions for extensive allorecognition diversity. On the one hand, if allorecognition diversity did not build up fast enough, somatic parasites went to fixation; conversely, once parasites had gone to fixation no allorecognition diversity built up. On the other hand, the mere threat of parasitism could select for high allorecognition diversity, preventing invasion of somatic parasites. Moderate population viscosity combined with weak global dispersal was optimal for the joint evolution of allorecognition and protection against parasitism. Our results are consistent with the widespread occurrence of allorecognition in fungi and the low degree of somatic parasitism. We discuss the implications of our results for allorecognition in other organism groups.
    Regular bottlenecks and restrictions to somatic fusion prevent the accumulation of mitochondrial defects in Neurospora
    Bastiaans, E. ; Aanen, D.K. ; Debets, A.J.M. ; Hoekstra, R.F. ; Lestrada, B. ; Maas, M.F.P.M. - \ 2014
    Philosophical Transactions of the Royal Society B. Biological sciences 369 (2014)1646. - ISSN 0962-8436
    vegetative incompatibility - filamentous fungi - dna mutations - hyphal fusion - evolution - populations - senescence - intermedia - selection - crassa
    The replication and segregation of multi-copy mitochondrial DNA (mtDNA) are not under strict control of the nuclear DNA. Within-cell selection may thus favour variants with an intracellular selective advantage but a detrimental effect on cell fitness. High relatedness among the mtDNA variants of an individual is predicted to disfavour such deleterious selfish genetic elements, but experimental evidence for this hypothesis is scarce. We studied the effect of mtDNA relatedness on the opportunities for suppressive mtDNA variants in the fungus Neurospora carrying the mitochondrial mutator plasmid pKALILO. During growth, this plasmid integrates into the mitochondrial genome, generating suppressive mtDNA variants. These mtDNA variants gradually replace the wild-type mtDNA, ultimately culminating in growth arrest and death. We show that regular sequestration of mtDNA variation is required for effective selection against suppressive mtDNA variants. First, bottlenecks in the number of mtDNA copies from which a 'Kalilo' culture started significantly increased the maximum lifespan and variation in lifespan among cultures. Second, restrictions to somatic fusion among fungal individuals, either by using anastomosis-deficient mutants or by generating allotype diversity, prevented the accumulation of suppressive mtDNA variants. We discuss the implications of these results for the somatic accumulation of mitochondrial defects during ageing
    High prevalence of a fungal prion
    Debets, A.J.M. ; Dalstra, H.J.P. ; Slakhorst, S.M. ; Koopmanschap-Memelink, A.B. ; Hoekstra, R.F. ; Saupe, S.J. - \ 2012
    Proceedings of the National Academy of Sciences of the United States of America 109 (2012)26. - ISSN 0027-8424 - p. 10432 - 10437.
    podospora-anserina - vegetative incompatibility - het-s - heterokaryon incompatibility - neurospora-crassa - meiotic drive - yeast prion - mechanism - diseases - genes
    Prions are infectious proteins that cause fatal diseases in mammals. Prions have also been found in fungi, but studies on their role in nature are scarce. The proposed biological function of fungal prions is debated and varies from detrimental to benign or even beneficial. [Het-s] is a prion of the fungus Podospora anserina. The het-s locus exists as two antagonistic alleles that constitute an allorecognition system: the het-s allele encoding the protein variant capable of prion formation and the het-S allele encoding a protein variant that cannot form a prion. We document here that het-s alleles, capable of prion formation, are nearly twice as frequent as het-S alleles in a natural population of 112 individuals. Then, we report a 92% prevalence of [Het-s] prion infection among the het-s isolates and find evidence of the role of the [Het-s]/het-S allorecognition system on the incidence of infection by a deleterious senescence plasmid. We explain the het-s/het-S allele ratios by the existence of two selective forces operating at different levels. We propose that during the somatic stage, the role of [Het-s]/HET-S in allorecognition leads to frequency-dependent selection for which an equilibrated frequency would be optimal. However, in the sexual cycle, the [Het-s] prion causes meiotic drive favoring the het-s allele. Our findings indicate that [Het-s] is a selected and, therefore, widespread prion whose activity as selfish genetic element is counteracted by balancing selection for allorecognition polymorphism
    The het-c heterokaryon incompatibility gene in Aspergillus niger
    Diepeningen, A.D. van; Pal, K. ; Lee, T. ; Hoekstra, R.F. ; Debets, A.J.M. - \ 2009
    Mycological Research 113 (2009)2. - ISSN 0953-7562 - p. 222 - 229.
    programmed cell-death - neurospora-crassa - vegetative incompatibility - filamentous fungi - podospora-anserina - mating-type - locus - nidulans - sequence - protein
    Heterokaryon incompatibility among Aspergillus niger strains is a widespread phenomenon that is observed as the inability to form stable heterokaryons. The genetic basis of heterokaryon incompatibility reactions is well established in some sexual filamentous fungi but largely unknown in presumed asexual species, such as A. niger. To test whether the genes that determine heterokaryon incompatibility in Neurospora crassa, such as het-c, vib-1 and pin-c, have a similar function in A. niger, we performed a short in silico search for homologues of these genes in the A. niger and several related genomes. For het-c, pin-c and vib-1 we did indeed identify putative orthologues. We then screened a genetically diverse worldwide collection of incompatible black Aspergilli for polymorphisms in the het-c orthologue. No size variation was observed in the variable het-c indel region that determines the specificity in N. crassa. Sequence comparison showed only minor variation in the number of glutamine coding triplets. However, introduction of one of the three N. crassa alleles (het-c2) in A. niger by transformation resulted in an abortive phenotype, reminiscent of the heterokaryon incompatibility in N. crassa. We conclude that although the genes required are present and the het-c homologue could potentially function as a heterokaryon incompatibility gene, het-c has no direct function in heterokaryon incompatibility in A. niger because the necessary allelic variation is absent
    The social evolution of somatic fusion
    Aanen, D.K. ; Debets, A.J.M. ; Visser, J.A.G.M. de; Hoekstra, R.F. - \ 2008
    Bioessays 30 (2008)11-12. - ISSN 0265-9247 - p. 1193 - 1203.
    conidial anastomosis tubes - programmed cell-death - double-stranded-rna - vegetative incompatibility - heterokaryon incompatibility - neurospora-crassa - filamentous fungi - podospora-anserina - aspergillus-nidulans - allorecognition specificity
    The widespread potential for somatic fusion among different conspecific multicellular individuals suggests that such fusion is adaptive. However, because recognition of non-kin (allorecognition) usually leads to a rejection response, successful somatic fusion is limited to close kin. This is consistent with kin-selection theory, which predicts that the potential cost of fusion and the potential for somatic parasitism decrease with increasing relatedness. Paradoxically, however, Crozier[1] found that, in the short term, positive-frequency-dependent selection eliminates the required genetic polymorphism at allorecognition loci. The Crozier paradox may be solved if allorecognition is based on extrinsically balanced polymorphisms, for example at immune loci. Alternatively, the assumption of most models that self fusion is mutually beneficial is wrong. If fusion is on average harmful, selection will promote unconditional rejection. However, we propose that fusion within individuals is beneficial, selecting for the ability to fuse, but fusion between individuals on average costly, selecting for non-self recognition (rather than non-kin recognition)
    Nonmendelian inheritance of the HET-s prion or HET-s prion domains determines the het-S spore killing system in Podospora anserina
    Dalstra, H.J.P. ; Zee, R.I. van der; Swart, K. ; Hoekstra, R.F. ; Saupe, S.J. ; Debets, A.J.M. - \ 2005
    Fungal Genetics and Biology 42 (2005)10. - ISSN 1087-1845 - p. 836 - 847.
    meiotic drive - heterokaryon incompatibility - vegetative incompatibility - in-vivo - protein - neurospora - fungi - organization - analog - genes
    Two alleles of the het-s/S locus occur naturally in the filamentous fungus Podospora anserina, het-s and het-S. The het-s encoded protein can form a prion that propagates a self-perpetuating amyloid aggregate, resulting in two phenotypes for the het-s strains. The prion-infected [Het-s] shows an antagonistic interaction to het-S whereas the prion-free [Het-s*] is neutral in interaction to het-S. The antagonism between [Het-s] and het-S is seen as heterokaryon incompatibility at the somatic level and as het-S spore killing in the sexual cycle. Two different domains of the HET-s and HET-S proteins have been identified, and a structure-function relationship has been established for interactions at the somatic level. In this study, we correlate accumulation of the HET-s and HET-S proteins (visualized using GFP) during the sexual cycle with timing of het-S spore abortion. Also, we present the structure-function relationship of the HET-s domains for interactions in the sexual cycle. We show that the constructs that ensure het-s incompatibility function in somatic mycelium are also active in het-S spore killing in the sexual cycle. In addition, paternal prion transmission and het-S spore killing has been found with the HET-s(157-289) truncated protein. The consequences of the unique transition from a coenocytic to a cellular state in the sexual phase and the timing, and localization of paternal and maternal HET-s and HET-S expression that are pertinent to prion transmission, and het-S spore killing are elaborated. These data further support our previously proposed model for het-S spore killing.
    Polymorphism for pKALILO based senescence in Hawaiian populations of Neurospora intermedia and Neurospora tetrasperma.
    Maas, M.F.P.M. ; Mourik, A. van; Hoekstra, R.F. ; Debets, A.J.M. - \ 2005
    Fungal Genetics and Biology 42 (2005)3. - ISSN 1087-1845 - p. 224 - 232.
    mitochondrial plasmids - vegetative incompatibility - natural-populations - nucleotide-sequence - fungus neurospora - kalilo plasmids - linear plasmids - dna - strains - crassa
    The natural population of Neurospora intermedia from Hawaii is polymorphic for the presence of the linear mitochondrial plasmid pKALILO that is associated with an infectious senescence syndrome. Although inter-specific horizontal transmission is experimentally possible, thus far pKALILO associated senescence has never been found outside N. intermedia in nature. Here, we demonstrate that it is not limited to the natural population of the heterothallic species N. intermedia, but also present in the sympatric population of its close relative, the pseudo-homothallic species Neurospora tetrasperma. We did a comparative analysis of the hallmarks of senescence in both species and show that: (1) Senescence is contagious in both species: the senescent state is efficiently transmitted between vegetatively compatible isolates. (2) All senescent isolates from both species contain the autonomously replicating linear mitochondrial senescence plasmid pKALILO. (3) In both species, senescent cultures contained copies of pKALILO inserted into the mitochondrial genome. Two of these inserts were characterized using semi-random two-step PCR, and were located within the large subunit mitochondrial rRNA gene. (4) However, pKALILO was less frequent in N. tetrasperma than in N. intermedia. (5) Also, the onset of senescence was significantly delayed in N. tetrasperma, compared to that in N. intermedia. We hypothesize how these differences in frequency and effect of pKALILO are connected to the respective life histories of their hosts.
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