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Holterman, M.

Publications and source records attributed to Holterman, M..

5 recordsLinked to original sources

Comparative genomics among three cyst nematode species reveals distinct evolutionary histories among effector families and an irregular distribution of effector-associated promoter motifs

Potato cyst nematodes (PCNs), an umbrella term used for two species, Globodera pallida and G. rostochiensis, belong worldwide to the most harmful pathogens of potato. Pathotype-specific host plant resistances are an essential handle for PCN control. However, the poor delineation of G. pallida pathotypes hampers the efficient use of available host plant resistances. Long-read sequencing technology allowed us to generate a new reference genome of G. pallida population D383 and, as compared to the current reference, the new genome assembly is 42 times less fragmented. For comparison of diversification patterns of six effector families between G. pallida and G. rostochiensis, an additional reference genome was generated for an outgroup, the beet cyst nematode Heterodera schachtii (IRS population). Large evolutionary contrasts in effector family topologies were observed. While VAPs diversified before the split between the three cyst nematode species, the families GLAND5 and GLAND13 only expanded in PCN after their separation from the genus Heterodera. Although DNA motifs in the promoter regions thought to be involved in the orchestration of effector expression ( DOG boxes) were present in all three cyst nematode species, their presence is not a necessity for dorsal gland-produced effectors. Notably, DOG box dosage was only loosely correlated with expression level of individual effector variants. Comparison of the G. pallida genome with those of two other cyst nematodes underlined the fundamental differences in evolutionary history between effector families. Re-sequencing of PCN populations with deviant virulence characteristics will allow for the linking of these characteristics with the composition of the effector repertoire as well as for the mapping of PCN diversification patterns resulting from extreme anthropogenic range expansion.

genomics↗

The genome and lifestage-specific transcriptomes of a plant-parasitic nematode and its host reveal susceptibility genes involved in trans-kingdom synthesis of vitamin B.

Plant-parasitic nematodes are a major, and in some cases a dominant, threat to crop production in all agricultural systems. The relative scarcity of classical resistance genes highlights a pressing need to identify new ways to develop nematode-resistant germplasm. Here, we sequence and assemble a high-quality genome of the model cyst nematode Heterodera schachtii to provide a platform for the first system-wide dual analysis of host and parasite gene expression over time, covering all major stages of the interaction. This novel approach enabled the analysis of the hologenome of the infection site, to identify metabolic pathways that were incomplete in the parasite but complemented by the host. Using a combination of bioinformatic, genetic, and biochemical approaches, we show that the highly atypical completion of vitamin B5 biosynthesis by the parasitic animal, putatively enabled by a horizontal gene transfer from a bacterium, is critically important for parasitism. Knockout of either the plant-encoded or the now nematode-encoded steps in the pathway blocks parasitism. Our experiments establish a reference for cyst nematodes, use this platform to further our fundamental understanding of the evolution of plant-parasitism by nematodes, and show that understanding congruent differential expression of metabolic pathways represents a new way to find nematode susceptibility genes, and thereby, targets for future genome editing-mediated generation of nematode-resistant crops.

genetics↗

Comparative Genomics of two Inbred Lines of the Potato Cyst Nematode Globodera rostochiensis reveals disparate Effector Family-specific Diversification Patterns

BackgroundPotato cyst nematodes belong to the most harmful pathogens in potato, and durable management of these soil-borne parasites largely depends on host-plant resistances. These resistances are pathotype specific. The current Globodera rostochiensis pathotype scheme that defines five pathotypes (Ro1 - Ro5) is for fundamental and practical reasons barely useful. As a result, resistant potato varieties are worldwide used in a non-informed manner. ResultsWe generated two novel reference genomes of G. rostochiensis inbred lines derived from a Ro1 and a Ro5 population. These genome sequences comprise 173 and 189 scaffolds respectively, marking a {approx} 24-fold reduction in fragmentation as compared to the current reference genome. We provide copy number variations for 18 effector families. Four dorsal gland effector families were investigated in more detail. SPRYSECs, known to be implicated in immune suppression, constitute by far the most diversified family with 60 and 99 variants in Ro1 and Ro5 distributed over 18 and 26 scaffolds. In contrast, CLEs, effectors involved in feeding site induction, show strong physical clustering. The 10 and 16 variants cluster on respectively 2 and 1 scaffolds. Given that pathotypes are defined by their effectoromes, we pinpoint the disparate nature of the contributing effector families in terms of sequence diversification and loss and gain of variants. ConclusionTwo novel reference genomes allow for nearly complete inventories of effector diversification and physical organisation within and between pathotypes. Combined with insights we provide on effector family-specific diversification patterns, this constitutes a solid basis for an effectorome-based virulence scheme for this notorious pathogen.

genomics↗

SIZ1 is a nuclear host target of the nematode effector GpRbp1 from Globodera pallida that acts as a negative regulator of basal plant defense to cyst nematodes

Soil-borne cyst nematodes are obligatory sedentary parasites that cause severe losses to cultivation of major crops such as potato and soybean. Cyst nematodes establish specialised permanent feeding sites within the roots of their host by manipulating plant morphology and physiology through secreted effectors. Here we identified host targets of effector GpRbp-1 and studied their roles in plant-nematode interactions. GpRbp-1 was found to interact in yeast and in planta with the potato and Arabidopsis homologues of Siz/PIAS-type E3 SUMO ligase SIZ1. Our results show that a pathogen effector targets the master regulator SIZ1 in plant cells, which has not been demonstrated earlier to our knowledge. The interaction of GpRbp-1 and SIZ1 localizes to the plant nucleus, suggesting that the nuclear functions of SIZ1 as regulator of plant immunity and physiology may be modulated by GpRbp-1. Furthermore, nematode infection assays and transcriptomic profiling indicate that SIZ1 is required for susceptibility to cyst nematodes. So, these data indicate that E3 SUMO ligases may play an important role in plant-nematode interactions. Based on the prediction of SUMO acceptor and interaction sites in GpRbp-1, a model is proposed in which the effector may recruit SIZ1 to be SUMOylated for full functionality in host cells.\n\nSignificance statementHere we show that a pathogen effector can target SIZ1, a key protein involved in regulating several aspects of plant biology, most likely to manipulate the SUMOylation of host proteins for successful infection of plants.

plant biology↗

Mapping of long-term impact of conventional and organic soil management on resident and active fractions of rhizosphere communities of barley (Hordeum vulgare)

Soil biota plays an essential role in ecosystem services such as carbon fixation, nitrogen and phosphorous cycling, and disease suppressiveness. Conventional soil management with large inputs of mineral fertilizers and pesticides have a significant impact on primary decomposer communities (bacteria and fungi), as well as on protists and metazoa, representatives of the next trophic level. Organic soil management is thought to contribute to a more diverse and stable soil food web. However, information to pinpoint this supposed beneficial effect is sparse and fragmented. Keeping in mind that a substantial fraction of the soil biota is dormant, we set out to map both the resident and the active the bacterial, fungal, protozoan and metazoan communities under various soil management regimes in two distinct soil types with barley as main crop. For all four organismal groups, the contrast between resident (rDNA-based) and active (rRNA-based) was the most important explanatory variable explaining 22%, 14%, 21% and 25% of the variance among bacterial, fungal, protozoan, and metazoan communities. Less prominent were the effects of soil management and soil type, however significant as well for all four organismal groups. LEfSe was used to identify indicator taxa for both the contrasts between resident and active communities, and the effects of soil management. Our results suggest that - next to DNA-based community characterisation - mapping of the active microbial community could provide essential insights in the effects of variables such as crop and soil management on the soil living community.

ecology↗