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Willig, J.-J.

Publications and source records attributed to Willig, J.-J..

8 recordsLinked to original sources

Mapping, stacking and characterization of a novel resistance haplotype against GpaVvrn-virulent Globodera pallida derived from wild potato relative Solanum brevicaule

Potato production is threatened by pests and pathogens. Among the most harmful are the potato cyst nematodes (PCN), including Globodera pallida. The major control measures are potato cultivars harbouring resistance genes. However, virulent nematode populations are breaking through the most broadly applied resistance genes, and therefore novel resistance genes are required to keep control of G. pallida. In this study we map a resistance locus in wild potato relative Solanum brevicaule to the bottom of chromosome 11 (42.83 - 42.85 Mb) using a k-mer based bulked segregant analysis and name the resistant haplotype GpaXIbrc. The presence of the GpaXIbrc marker in the potato genome significantly increases resistance against a GpaVvrn-virulent G. pallida population (AMPOP01). Furthermore, the GpaXIbrc haplotype was stacked with three other resistance haplotypes: GpaXItar, GpaVvrn, and GpaIXvrn. Stacking of the novel GpaXIbrc haplotype to these other resistance haplotypes resulted in a significant increase in resistance. The largest effect was seen in combinations with 'major' resistance haplotypes GpaVvrn + GpaIXvrn and GpaXItar + GpaXIbrc. To determine whether we are dealing with a novel allele, the resistance mechanism underlying the GpaXIbrc haplotype was described after performing an in vitro bioassay. The resistance mechanism was different from GpaXIspl as described in literature, which is also localized at the bottom of chromosome 11. Therefore, we conclude that we found a novel resistance allele originating from S. brevicaule.

genetics↗

Interspecific adaptations in root system architecture define host tolerance of Arabidopsis to biotic stresses by root feeding nematodes

Belowground, plants are exposed to a wide range of biotic stresses that vary in severity and nature, including tissue damage, disruption of vascular connectivity, and depletion of assimilates. How plants adapt their root systems to cope with different types of belowground biotic stresses is not well known. In this paper we compare above- and belowground plant adaptations to three nematode species with distinct tissue migration and feeding behaviours to study mechanisms underlying tolerance to different types of biotic stresses. We monitored both green canopy growth and changes in root system architecture of Arabidopsis inoculated with Pratylenchus penetrans, Heterodera schachtii, and Meloidogyne incognita. This revealed three distinct phases in aboveground plant responses: (i) initial growth inhibition associated with host invasion and tissue damage, (ii) persistent growth reduction associated with nematode sedentarism, and (iii) late growth stimulus in more advanced stages of infection. Specific adaptations in the root systems further revealed fundamentally different stress coping strategies. Tissue damage and intermittent feeding by P. penetrans in the root cortex did not induce significant changes in root system architecture. Tissue damage to the root cortex and prolonged feeding on host vascular cells by H. schachtii induced secondary root formation compensating for primary root growth inhibition. Prolonged feeding on host vascular cell by M. incognita alone did not induce secondary root formation, but was accompanied by typical local tissue swelling instead. Our data suggest that local secondary root formation and tissue swelling are two distinct compensatory mechanisms underlying tolerance to sedentarism by root-feeding nematodes. HighlightHow plants utilize root system plasticity to cope with different types of biotic stresses by root feeding nematodes remains largely unknown. Here, we report on specific adaptive growth responses in Arabidopsis roots to three nematode species, Pratylenchus penetrans, Heterodera schachtii, and Meloidogyne incognita, with fundamentally different strategies for host invasion, subsequent migration through host tissue, and feeding on host cells.

plant biology↗

Plant parasitic cyst nematodes respond to viral infection through RNA interference

Plant-parasitic nematodes (PPN) cause yield losses to multiple important crop species and counteractive measures are only partially successful. Recently the first viruses that infect PPN were discovered, presenting new research opportunities to understand and halt PPN. A critical step in this process is to identify how PPN respond to viruses. Here, two PPN species, the potato cyst nematode Globodera rostochiensis and the beet cyst nematode Heterodera schachtii, were used to study PPN-virus interactions. Viral discovery based on bioinformatic analyses indicated three putative viral genomes present in G. rostochiensis (a Toti-like, Xinzhou-like, and Picorna-like virus) and five putative viral genomes in H. schachtii (a Bunya-like, Tobamo-like, Picorna-like, and two Nyami-like viruses). A genome composition analysis and RT-PCR data confirmed that these viruses infect the nematodes and not their host plants. Subsequently, antiviral RNAi activity was detected in both H. schachtii and G. rostochiensis using small RNA sequencing. For G. rostochiensis two distinct genotypes were investigated. These strongly differed in their RNAi response: Ro5-line 22 produced roughly 40 times more antiviral viRNAs than Ro1-line 19. Our measurement of an active antiviral response represents the first indication of antiviral activity in PPN. Author summaryPlant-parasitic nematodes (PPN) are key agricultural pests and although some PPN viruses have been discovered recently, it is still unknown if and how PPN respond to viral infection. Here we find three viruses in the potato cyst nematode (Globodera rostochiensis) and five viruses in the beet cyst nematode (Heterodera schachtii). Of these viruses, six are newly discovered. Genome and molecular analyses confirm that all found viruses specifically infect nematodes and not their host plants. By measuring small RNA profiles, it was confirmed that PPN react to viral infection by means of RNAi, except for a weak response against two negatively stranded Nyami-like viruses. Moreover, distinct RNAi profiles were found for two potato cyst nematode lines, giving the first insight into which genes might be involved in RNAi in PPN. Together, this research provides the first proof of an active antiviral response in PPN. Thereby this finding opens new opportunities for biological control and gene editing tools.

molecular biology↗

Stationary phloem proteins and their effects on viruses, aphids, and cyst nematodes in Arabidopsis

The phloem is a specialized tissue that facilitates systemic transport of carbohydrates and signal molecules, making it a common target for viruses, phloem-feeding insects, and cyst nematodes. In Arabidopsis, the stationary phloem-associated SIEVE ELEMENT-LINING CHAPERONE1 (SLI1) and RESTRICTED TEV MOVEMENT (RTM) proteins restrict insect phloem-feeding and potyviruses systemic transport, respectively. However, their broader roles in plant-attacker interactions remain largely unexplored. We investigated the roles of SLI1, RTM1, RTM2, and RTM3 in tobacco etch virus (TEV) infection, as well as in Myzus persicae and Heterodera schachtii infestations using Arabidopsis mutants. Systemic TEV movement was quantified, aphid behaviour and reproduction were assessed, and cyst nematode infection was monitored. SLI1 did not restrict TEV systemic movement, RTM3 reduced M. persicae reproduction without altering feeding behaviour, SLI1, RTM2, and RTM3 supported H. schachtii infection and feeding site expansion, and confocal images indicated a possible role of the proteins in de novo synthesis of sieve tubes around syncytia. These findings reveal that stationary phloem proteins exert dual and target-specific effects, limiting some attackers while inadvertently facilitating others. This highlights the complexity of phloem-based immunity and underscores the need to unravel its underlying mechanisms to develop strategies to reduce multiple pest and pathogen burdens simultaneously. HighlightStationary phloem proteins SLI1, RTM1, RTM2, and RTM3 exert dual and target-specific effects against tobacco etch virus, Myzus persicae, and Heterodera schachtii.

plant biology↗

WOX11-mediated cell size control in Arabidopsis attenuates fecundity of endoparasitic cyst nematodes

O_LICyst nematodes establish permanent feeding structures called syncytia inside host root vasculature, disrupting the flow of water and minerals. In response, plants form WOX11-mediated adventitious lateral roots at nematode infection sites. WOX11-adventitious lateral rooting modulates tolerance to nematode infections, however, whether this also benefits nematode parasitism remains unknown. C_LIO_LIHere, we report on bioassays using a 35S::WOX11-SRDX transcriptional repressor mutant to investigate whether WOX11-adventitious lateral rooting promotes syncytium development and thereby female fecundity. Moreover, we chemically inhibited cellulose biosynthesis to verify if WOX11 directly modulates cell wall plasticity in syncytia. Finally, we performed histochemical analyses to test if WOX11 mediates syncytial cell wall plasticity via reactive oxygen species (ROS). C_LIO_LIRepression of WOX11-mediated transcription specifically enhanced the radial expansion of syncytial elements, increasing both syncytium size and female offspring. The enhanced syncytial hypertrophy observed in the 35S::WOX11-SRDX mutant could be phenocopied by chemical inhibition of cellulose biosynthesis and was associated with elevated levels of ROS at nematode infection sites. C_LIO_LIWe therefore conclude that WOX11 restricts radial expansion of nematode feeding structures and female fecundity, likely by modulating ROS-mediated cell wall plasticity mechanisms. Remarkably, this novel role of WOX11 in plant cell size control is independent of WOX11-adventitious rooting underlying disease tolerance. C_LI

plant biology↗

WOX11-mediated adventitious lateral root formation modulates tolerance of Arabidopsis to cyst nematode infections

The transcription factor WUSCHEL-RELATED HOMEOBOX 11 (WOX11) in Arabidopsis initiates the formation of adventitious lateral roots upon mechanical injury in primary roots. Root-invading nematodes also induce de novo root organogenesis leading to excessive root branching, but it is not known if this symptom of disease involves mediation by WOX11 and if it benefits the plant. Here, we show with targeted transcriptional repression and reporter gene analyses in Arabidopsis that the beet cyst nematode Heterodera schachtii activates WOX11-adventitious lateral rooting from primary roots close to infection sites. The activation of WOX11 in nematode-infected roots occurs downstream of jasmonic acid-dependent damage signaling via ETHYLENE RESPONSIVE FACTOR109, linking adventitious lateral root formation to nematode damage to host tissues. By measuring different root system components, we found that WOX11-mediated formation of adventitious lateral roots compensates for nematode-induced inhibition of primary root growth. Our observations further demonstrate that WOX11-mediated rooting reduces the impact of nematode infections on aboveground plant development and growth. Altogether, we conclude that the transcriptional regulation by WOX11 modulates root system plasticity under biotic stress, which is one of the key mechanisms underlying tolerance of Arabidopsis to cyst nematode infections.

plant biology↗

From root to shoot; Quantifying nematode tolerance in Arabidopsis thaliana by high-throughput phenotyping of plant development

Nematode migration, feeding site formation, withdrawal of plant assimilates, and activation of plant defence responses have a significant impact on plant growth and development. Plants display intraspecific variation in tolerance limits for root-feeding nematodes. Although disease tolerance has been recognised as a distinct trait in biotic interactions of mainly crops, we lack mechanistic insights. Progress is hampered by difficulties in quantification and laborious screening methods. We turned to the model plant Arabidopsis thaliana, since it offers extensive resources to study the molecular and cellular mechanisms underlying nematode-plant interactions. Through imaging of tolerance-related parameters the green canopy area was identified as an accessible and robust measure for assessing damage due to cyst nematode infection. Subsequently, a high-throughput phenotyping platform simultaneously measuring the green canopy area growth of 960 A. thaliana plants was developed. This platform can accurately measure cyst- and root-knot nematode tolerance limits in A. thaliana through classical modelling of tolerance limits. Furthermore, real-time monitoring provided data for a novel view of tolerance, identifying a compensatory growth response. These findings show that our phenotyping platform will enable further studies into a mechanistic understanding of tolerance to below-ground biotic stress. HighlightThe mechanisms of tolerance to root-parasitic nematodes remain unknown. We developed a high-throughput phenotyping system that enables unravelling the underlying mechanisms of tolerance to nematodes.

plant biology↗

Root architecture plasticity in response to endoparasitic cyst nematodes is mediated by damage signaling

O_LIPlant root architecture plasticity in response to biotic stresses has not been thoroughly investigated. Infection by the endoparasitic cyst nematodes induces root architectural changes that involve the formation of secondary roots at infection sites. However, the molecular mechanisms regulating secondary root formation in response to cyst nematode infection remain largely unknown. C_LIO_LIWe first assessed whether secondary roots form in a nematode-density dependent manner by challenging wild type Arabidopsis plants with increasing numbers of cyst nematodes (Heterodera schachtii). Next, by using jasmonate-related reporter lines and knock-out mutants, we tested if tissue damage by nematodes triggers secondary root formation. Finally, we verified whether damage-induced secondary root formation depends on local auxin biosynthesis at nematode infection sites. C_LIO_LIIntracellular host invasion by H. schachtii triggers a transient local increase in jasmonates, which activates the expression of ERF109 in a COI1-dependent manner. Knock-out mutations in COI1 and ERF109 disrupt the nematode-density dependent increase of secondary roots observed in wildtype plants. Furthermore, ERF109 regulates secondary root formation upon H. schachtii infection via local auxin biosynthesis. C_LIO_LIHost invasion by H. schachtii triggers secondary root formation via the damage-induced jasmonate-dependent ERF109 pathway. This points at a novel mechanism underlying plant root plasticity in response to biotic stress. C_LI

plant biology↗