The Role of Helminthophagous Fungi in the Biological Control of Human and Zoonotic Intestinal Helminths.

Nematophagous, or helminthophagous fungi of the genera Duddingtonia, Arthrobotrys, Monacrosporium, Pochonia, Paecilomyces, and Mucor, have been used over the years in in vitro and in vivo experiments to control helminth parasites that are potentially zoonotic. These fungi have shown efficacy against the following helminth genera: Ancylostoma, Toxocara, Enterobius, Strongyloides, Angiostrongylus, Taenia, Fasciola, and Schistosoma. The results obtained from these experiments, together with studies on soil contamination, suggest the viability of their use as a sustainable and effective strategy to reduce environmental contamination by these zoonotic parasites. Therefore, the aim of this review was to address the role of helminthophagous fungi in the biological control of potentially zoonotic helminths. To this end, we describe (1) a brief history of helminthophagous fungi; (2) a discussion of some potentially zoonotic intestinal parasites; (3) the importance of helminthophagous fungi in the control of nematodes, cestodes, and trematodes; and (4) the potential of helminthophagous fungi as a practical and sustainable strategy.

Design, synthesis, and nematicidal activity of novel 1,2,4-oxadiazole derivatives containing amide fragments.

Plant-parasitic nematodes are seriously affecting agricultural production worldwide and there are few highly effective and low-risk nematicides to control nematode diseases. In order to discover new nematicides, a series of 1,2,4-oxadiazole derivatives containing amide fragments have been designed and synthesized with the principle of active substructure splicing. The nematicidal activity of the target compounds was evaluated in vitro and it indicated that compound C3 exhibited the most nematicidal activity against Bursaphelenchus xylophilus, Aphelenchoides besseyi, and Ditylenchus destructor with the LC50 values of 37.2, 36.6, and 43.4 µg/mL, respectively, which were superior to positive agent tioxazafen. The preliminary mechanism results revealed that compound C3 not only inhibited the reproduction of B. xylophilus populations, but also affected the production of ROS and the accumulation of lipofuscin and lipids. Furthermore, compound C3 showed good inhibition of succinate dehydrogenase (SDH) with the IC50 value of 45.5 µmol/L. Molecular docking indicated that compound C3 had excellent binding to amino acids around the SDH active pocket. This work indicated that 1,2,4-oxadiazole derivative containing amide fragment is a promising template for the discovery of new nematicides and compound C3 can be used as a potential nematicide candidate.

Assessing performance of simplified bioassays for soil-borne pathogens in smallholder systems of western Kenya.

Introduction: Soil-borne pathogens cause considerable crop losses and food insecurity in smallholder systems of sub-Saharan Africa. Soil and crop testing is critical for estimating pathogen inoculum levels and potential for disease development, understanding pathogen interactions with soil nutrient and water limitations, as well as for developing informed soil health and disease management decisions. However, formal laboratory analyses and diagnostic services for pathogens are often out of reach for smallholder farmers due to the high cost of testing and a lack of local laboratories. Methods: To address this challenge, we assessed the performance of a suite of simplified soil bioassays to screen for plant parasitic nematodes (e.g., Meloidogyne, Pratylenchus) and other key soil-borne pathogens (Pythium and Fusarium). We sampled soils from on-farm trials in western Kenya examining the impact of distinct nutrient inputs (organic vs. synthetic) on bean production. Key soil health parameters and common soil-borne pathogens were evaluated using both simple bioassays and formal laboratory methods across eleven farms, each with three nutrient input treatments (66 samples in total). Results and Discussion: The soil bioassays, which involved counting galls on lettuce roots and lesions on soybean were well correlated with the abundance of gall forming (Meloidogyne) and root lesion nematodes (e.g., Pratylenchus) recovered in standard laboratory-based extractions. Effectiveness of a Fusarium bioassay, involving the counting of lesions on buried bean stems, was verified via sequencing and a pathogenicity test of cultured Fusarium strains. Finally, a Pythium soil bioassay using selective media clearly distinguished pathogen infestation of soils and infected seeds. When examining management impact on nematode communities, soils amended with manure had fewer plant parasites and considerably more bacterivore and fungivore nematodes compared to soils amended with synthetic N and P. Similarly, Pythium presence was 35% lower in soils amended with manure, while the Fusarium assays indicated 23% higher Fusarium infection in plots with amended manure. Our findings suggest that relatively simple bioassays can be used to help farmers assess soil-borne pathogens in a timely manner, with minimal costs, thus enabling them to make informed decisions on soil health and pathogen management.

Plant-nematode battle: engagement of complex signaling network.

Plant-parasitic nematodes (PPNs) are widely distributed and highly adaptable. To evade the invasion and infection of PPNs, plants initiate a series of defense responses. In turn, PPNs secrete effectors into the host tissues to suppress plant defense. In this ongoing battle between PPNs and plants, complex signal transduction processes are typically involved. This article aims to review the plant signaling network involved in host perception by the nematode, nematode perception, and downstream activation of plant defense signaling and how nematodes attempt to interfere with this network. Our goal is to establish a foundation for elucidating the signaling and regulatory mechanisms of plant-nematode interactions, and to provide insights and tools for developing PPN-resistant crops and technologies.

Biocontrol of plant parasitic nematodes by bacteria and fungi: a multi-omics approach for the exploration of novel nematicides in sustainable agriculture.

Plant parasitic nematodes (PPNs) pose a significant threat to global crop productivity, causing an estimated annual loss of US $157 billion in the agriculture industry. While synthetic chemical nematicides can effectively control PPNs, their overuse has detrimental effects on human health and the environment. Biocontrol agents (BCAs), such as bacteria and fungi in the rhizosphere, are safe and promising alternatives for PPNs control. These BCAs interact with plant roots and produce extracellular enzymes, secondary metabolites, toxins, and volatile organic compounds (VOCs) to suppress nematodes. Plant root exudates also play a crucial role in attracting beneficial microbes toward infested roots. The complex interaction between plants and microbes in the rhizosphere against PPNs is mostly untapped which opens new avenues for discovering novel nematicides through multi-omics techniques. Advanced omics approaches, including metagenomics, transcriptomics, proteomics, and metabolomics, have led to the discovery of nematicidal compounds. This review summarizes the status of bacterial and fungal biocontrol strategies and their mechanisms for PPNs control. The importance of omics-based approaches for the exploration of novel nematicides and future directions in the biocontrol of PPNs are also addressed. The review highlighted the potential significance of multi-omics techniques in biocontrol of PPNs to ensure sustainable agriculture.

Plant-parasitic nematode disease complexes as overlooked challenges to crop production.

Plant diseases are caused by various microorganisms such as bacteria, fungi, viruses, and nematodes. These diseases impact crop growth, reduce produce quality, and lead to financial losses. Plant disease can be caused by single pathogens or by interactions called "disease complexes", involving two or more pathogens. In these cases, the disease severity caused by the pathogens combined is greater than the sum of the disease caused by each pathogen alone. disease complexes formed among plant-parasitic nematodes (PPNs) with bacteria, fungi, or viruses, can occur. PPNs either enhance the other pathogen incidence and severity or are necessary for disease symptoms to be expressed. PPNs can do so by being wounding agents, vectors, modifiers of plant biochemistry and physiology, or altering the rhizosphere microbiome. This review identifies several PPNs-plant pathogens disease complexes in crop production to discuss how understanding such interactions is key for improving management practices.

Advanced screening methods for assessing motility and hatching in plant-parasitic nematodes.

BACKGROUND: Plant-parasitic nematodes are economically important pests responsible for substantial losses in agriculture. Researchers focusing on plant-parasitic nematodes, especially on finding new ways of their control, often need to assess basic parameters such as their motility, viability, and reproduction. Traditionally, these assays involve visually counting juveniles and eggs under a dissecting microscope, making this investigation time-consuming and laborious. RESULTS: In this study, we established a procedure to efficiently determine the motility of two plant-parasitic nematode species, Heterodera schachtii and Ditylenchus destructor, using the WMicrotracker ONE platform. Additionally, we demonstrated that hatching of the cyst nematode H. schachtii can be evaluated using both the WMicrotracker ONE and by assessing the enzymatic activity of chitinase produced during hatching. CONCLUSIONS: We present fast and straightforward protocols for studying nematode motility and hatching that allow us to draw conclusions about viability and survival. Thus, these methods are useful tools for facilitating fast and efficient evaluation in various fields of research focused on plant-parasitic nematodes.

Distinct changes in tomato-associated multi-kingdom microbiomes during Meloidogyne incognita parasitism.

BACKGROUND: The interplay between root-knot nematode (RKN) parasitism and the complex web of host-associated microbiota has been recognized as pivotal for effective management of the pest. However, studies assessing this relationship have focussed on the bacterial and fungal communities, neglecting the unicellular eukaryotic members. Here, we employed amplicon sequencing analysis of the bacterial 16S rRNA, fungal ITS and eukaryotic 18S rRNA genes, and comprehensively examined how the microbiome composition, diversity and networking developed with time in the rhizospheres and roots of RKN-inoculated and non-inoculated tomato plants. RESULTS: As expected, infection with the RKN Meloidogyne incognita decreased plant growth. At individual timepoints, we found distinct bacterial, fungal and eukaryote community structures in the RKN-inoculated and non-inoculated rhizospheres and roots, and RKN inoculation affected several taxa in the root-associated microbiome differentially. Correlation analysis revealed several bacterial and fungal and few protist taxa that correlated negatively or positively with M. incognita. Moreover, network analysis using bacterial, fungal and eukaryotic data revealed more dynamic networks with higher robustness to disturbances in the RKN-inoculated than in the non-inoculated rhizospheres/roots. Hub taxa displayed a noticeable successional pattern that coincided with different phases of M. incognita parasitism. We found that fungal hubs had strong negative correlations with bacteria and eukaryotes, while positive correlations characterized hub members within individual kingdoms. CONCLUSION: Our results reveal dynamic tomato-associated microbiomes that develop along different trajectories in plants suffering M. incognita infestation and non-infested plants. Overall, the results identify stronger associations between RKN and bacterial and fungal taxa than between eukaryotic taxa and RKN, suggesting that fungal and bacterial communities could play a larger role in the regulation of RKN. The study identifies several putative RKN-antagonistic bacterial and fungal taxa and confirms the antagonistic potential previously identified in other taxa.

Plant-Parasitic Nematode Genera Associated with Turfgrass in Maryland Golf Courses and Athletic Fields.

Field surveys were conducted to assess the occurrence and diversity of plant-parasitic nematodes (PPNs) in golf courses and athletic fields across Maryland, USA, during 2022 and 2023. A total of 28 golf courses and ten athletic fields were surveyed, revealing the prevalence and abundance of 13 PPNs taxa in the region. Criconemoides was identified as the most prevalent (94.9%) and Tylenchorhynchus as the most abundant (2.3) across all samples. Central golf courses (west side of the Chesapeake Bay) exhibited a high prevalence of Criconemoides and Tylenchorhynchus, while Eastern Shore golf courses and athletic fields displayed a higher prevalence of Helicotylenchus and Criconemoides. Further, Belonolaimus longicaudatus was reported for the first time from turfgrass in Maryland, raising concerns due to its potential to cause severe damage on both cool- and warm-season turfgrass. Biodiversity analysis indicated that richness (R2) was higher in athletic fields, while diversity (H') and evenness (J') were significantly greater in golf courses. This study provides baseline information for monitoring PPNs distribution in Maryland and also for the development of effective nematode management approaches in turfgrass ecosystems.

Advances in Migratory Plant Endoparasitic Nematode Effectors.

Unlike sedentary plant-parasitic nematodes, migratory plant endoparasitic nematodes (MPENs) are unable to establish permanent feeding sites, and all developmental stages (except eggs) can invade and feed on plant tissues and can be easily overlooked because of the unspecific symptoms. They cause numerous economic losses in agriculture, forestry, and horticulture. In order to understand the pathogenetic mechanism of MPENs, here we describe research on functions and host targets focused on currently identified effectors from six MPENs, namely Radopholus similis, Pratylenchus spp., Ditylenchus destructor, Bursaphelenchus xylophilus, Aphelenchoides besseyi, and Hirschmanniella oryzae. This information will provide valuable insights into understanding MPEN effectors and for future fostering advancements in plant protection.

Phytochemical Volatiles as Potential Bionematicides with Safer Ecotoxicological Properties.

The management of plant-parasitic nematodes (PPNs) still relies on traditional nematicides that threaten the environment and human health. Novel solutions are urgently needed for PPN pest management that are effective while safeguarding non-target organisms. Volatile phytochemicals belong to a structurally diverse group of bioactive metabolites that are believed to hold safer environmental characteristics than synthetic pesticides. Nonetheless, not many studies have analysed the potential environmental benefits of shifting to these novel bionematicides. In the present study, 20 phytochemical volatiles with reported nematicidal activity were compared to traditional pesticides using specific parameters of environmental and human health safety available on applied online databases and predicted in silico through specialised software. Overall, the reviewed nematicidal phytochemicals were reportedly less toxic than synthetic nematicides. They were predicted to disperse to the air and soil environmental compartments and were reported to have a lower toxicity on aquatic organisms. On the contrary, the synthetic nematicides were reportedly toxic to aquatic organisms while showing a predicted high affinity to the water environmental compartment. As alternatives, ß-keto or fatty acid derivatives, e.g., aliphatic alcohols or ketones, showed more adequate properties. This study highlights the importance of complementing studies on nematicidal activity with a risk assessment-based analysis to allow for a faster selection of nematicidal phytochemical volatiles and to leverage the development and implementation of bionematicides.

The Use of Caenorhabditis elegans as a Model for Plant-Parasitic Nematodes: What Have We Learned?

Nematoda is a diverse phylum that is estimated to contain more than a million species. More than 4,100 of these species have the ability to parasitize plants and cause agricultural losses estimated at US $173 billion annually. This has led to considerable research into their biology to minimize crop losses via control methods. At the infancy of plant-parasitic nematode molecular biology, researchers compared nematode genomes, genes, and biological processes to the model nematode species Caenorhabditis elegans, which is a free-living bacterial feeder. This well-annotated and researched model nematode assisted the molecular biology research, e.g., with genome assemblies, of plant-parasitic nematodes. However, as research into these plant parasites progressed, the necessity of relying on the free-living relative as a reference has reduced. This is partly driven by revealing the considerable divergence between the two types of nematodes both genomically and anatomically, forcing comparisons to be redundant as well as the increased quality of molecular plant nematology proposing more suitable model organisms for this clade of nematode. The major irregularity between the two types of nematodes is the unique anatomical structure and effector repertoire that plant nematodes utilize to establish parasitism, which C. elegans lacks, therefore reducing its value as a heterologous system to investigate parasitic processes. Despite this, C. elegans remains useful for investigating conserved genes via its utility as an expression system because of the current inability to transform plant-parasitic nematodes. Unfortunately, owing to the expertise that this requires, it is not a common and/or accessible tool. Furthermore, we believe that the application of C. elegans as an expression system for plant nematodes will be redundant once tools are established for stable reverse-genetics in these plant parasites. This will remove the restraints on molecular plant nematology and allow it to excel on par with the capabilities of C. elegans research.

Silencing of the T-type voltage-gated calcium channel α1 subunit by fungus-mediated RNAi altered the structure of F-actin and caused defective behaviors in Ditylenchus destructor.

BACKGROUND: T-type calcium channels, characterized as low-voltage activated (LVA) calcium channels, play crucial physiological roles across a wide range of tissues, including both the neuronal and nonneuronal systems. Using in situ hybridization and RNA interference (RNAi) techniques in vitro, we previously identified the tissue distribution and physiological function of the T-type calcium channel α1 subunit (DdCα1G) in the plant-parasitic nematode Ditylenchus destructor. METHODS AND RESULTS: To further characterize the functional role of DdCα1G, we employed a combination of immunohistochemistry and fungus-mediated RNAi and found that DdCα1G was clearly distributed in stylet-related tissue, oesophageal gland-related tissue, secretory-excretory duct-related tissue and male spicule-related tissue. Silencing DdCα1G led to impairments in the locomotion, feeding, reproductive ability and protein secretion of nematodes. To confirm the defects in behavior, we used phalloidin staining to examine muscle changes in DdCα1G-RNAi nematodes. Our observations demonstrated that defective behaviors are associated with related muscular atrophy. CONCLUSION: Our findings provide a deeper understanding of the physiological functions of T-type calcium channels in plant-parasitic nematodes. The T-type calcium channel can be considered a promising target for sustainable nematode management practices.

Genome-wide RNA interference of the nhr gene family in barber's pole worm identified members crucial for larval viability in vitro.

Nuclear hormone receptors (NHRs) are emerging target candidates against nematode infection and resistance. However, there is a lack of comprehensive information on NHR-coding genes in parasitic nematodes. In this study, we curated the nhr gene family for 60 major parasitic nematodes from humans and animals. Compared with the free-living model organism Caenorhabditis elegans, a remarkable contraction of the nhr family was revealed in parasitic species, with genetic diversification and conservation unveiled among nematode Clades I (10-13), III (16-42), IV (33-35) and V (25-64). Using an in vitro biosystem, we demonstrated that 40 nhr genes in a blood-feeding nematode Haemonchus contortus (clade V; barber's pole worm) were responsive to host serum and one nhr gene (i.e., nhr-64) was consistently stimulated by anthelmintics (i.e., ivermectin, thiabendazole and levamisole); Using a high-throughput RNA interference platform, we knocked down 43 nhr genes of H. contortus and identified at least two genes that are required for the viability (i.e., nhr-105) and development (i.e., nhr-17) of the infective larvae of this parasitic nematode in vitro. Harnessing this preliminary functional atlas of nhr genes for H. contortus will prime the biological studies of this gene family in nematode genetics, infection, and anthelmintic metabolism within host animals, as well as the promising discovery of novel intervention targets.

Diversity and evolution of transposable elements in the plant-parasitic nematodes.

BACKGROUND: Transposable elements (TEs) are mobile DNA sequences that propagate within genomes, occupying a significant portion of eukaryotic genomes and serving as a source of genetic variation and innovation. TEs can impact genome dynamics through their repetitive nature and mobility. Nematodes are incredibly versatile organisms, capable of thriving in a wide range of environments. The plant-parasitic nematodes are able to infect nearly all vascular plants, leading to significant crop losses and management expenses worldwide. It is worth noting that plant parasitism has evolved independently at least three times within this nematode group. Furthermore, the genome size of plant-parasitic nematodes can vary substantially, spanning from 41.5 Mbp to 235 Mbp. To investigate genome size variation and evolution in plant-parasitic nematodes, TE composition, diversity, and evolution were analysed in 26 plant-parasitic nematodes from 9 distinct genera in Clade IV. RESULTS: Interestingly, despite certain species lacking specific types of DNA transposons or retrotransposon superfamilies, they still exhibit a diverse range of TE content. Identification of species-specific TE repertoire in nematode genomes provides a deeper understanding of genome evolution in plant-parasitic nematodes. An intriguing observation is that plant-parasitic nematodes possess extensive DNA transposons and retrotransposon insertions, including recent sightings of LTR/Gypsy and LTR/Pao superfamilies. Among them, the Gypsy superfamilies were found to encode Aspartic proteases in the plant-parasitic nematodes. CONCLUSIONS: The study of the transposable element (TE) composition in plant-parasitic nematodes has yielded insightful discoveries. The findings revealed that certain species exhibit lineage-specific variations in their TE makeup. Discovering the species-specific TE repertoire in nematode genomes is a crucial element in understanding the evolution of genomes in plant-parasitic nematodes. It allows us to gain a deeper insight into the intricate workings of these organisms and their genetic makeup. With this knowledge, we are gaining a fundamental piece in the puzzle of understanding the evolution of these parasites. Moreover, recent transpositions have led to the acquisition of new TE superfamilies, especially Gypsy and Pao retrotransposons, further expanding the diversity of TEs in these nematodes. Significantly, the widely distributed Gypsy superfamily possesses proteases that are exclusively associated with parasitism during nematode-host interactions. These discoveries provide a deeper understanding of the TE landscape within plant-parasitic nematodes.

Biosecurity risks to human food supply associated with plant-parasitic nematodes.

Biosecurity in agriculture is essential for preventing the introduction and spread of plant-parasitic nematodes (PPNs) which threaten global food security by reducing crop yields and facilitating disease spread. These risks are exacerbated by increased global trade and climate change, which may alter PPN distribution and activity, increasing their impact on agricultural systems. Addressing these challenges is vital to maintaining the integrity of the food supply chain. This review highlights significant advancements in managing PPN-related biosecurity risks within the food supply chain, particularly considering climate change's evolving influence. It discusses the PPN modes of transmission, factors increasing the risk of infestation, the impact of PPNs on food safety and security, and traditional and emerging approaches for detecting and managing these pests. Literature suggests that implementing advanced biosecurity measures could decrease PPN infestation rates by up to 70%, substantially reducing crop yield losses and bolstering food security. Notably, the adoption of modern detection and management techniques, (molecular diagnostics and integrated pest management) and emerging geospatial surveillance and analysis systems (spectral imaging, change-detection analysis) has shown greater effectiveness than traditional methods. These innovations offer promising avenues for enhancing crop health and securing the food supply chain against environmental shifts. The integration of these strategies is crucial, demonstrating the potential to transform biosecurity practices and sustain agricultural productivity in the face of changing climatic conditions. This analysis emphasizes the importance of adopting advanced measures to protect crop health and ensure food supply chain resilience, providing valuable insights for stakeholders across the agricultural sector.

Phytoparasitic Nematodes of Musa spp. with Emphasis on Sources of Genetic Resistance: A Systematic Review.

Bananas are a staple food that considerably contributes to both food security and income generation, especially in countries of Africa, Asia, and Central and South America. The banana plant (Musa spp.) is affected by various pathogens, of main concern being the plant-parasitic nematodes associated with the rhizosphere, the most important of which are Radopholus similis (burrowing nematode), Helicotylenchus sp. (spiral nematode), Pratylenchus sp. (root lesion nematode), and Meloidogyne sp. (gall nematode). Infected plants reduce their ability to absorb water and nutrients, which can lead to delayed flowering, fewer bunches, and lower fruit mass. Obtaining nematode-resistant banana cultivars through genetic improvement is an effective and sustainable option compared with chemical control with nematicides. Here, we provide the first systematic review of existing banana sources of resistance to nematodes to aid the management and control of nematodes in banana and plantain crops. Articles selected from different databases were evaluated, and searches were conducted using pre-established inclusion and exclusion criteria. We found 69 studies dealing with genetic improvement for nematode resistance in banana cultivation. Our findings revealed that sources of resistance are currently under investigation to combat the diseases caused by different nematode species in banana plants.

Parasitic Nematodes of Sugarcane: A Major Productivity Impediment and Grand Challenges in Management.

Sugarcane is an important cash crop grown in 137 countries, accounting for 80% of global sugar production. It supports the livelihood of more than 100 million people and up to 25% of the rural population in some countries. Plant-parasitic nematodes are one significant constraint in sugarcane production and can lead to a loss of up to 30% in productivity. More than 300 species of parasitic nematodes have been discovered in sugarcane soil. Owing to limited data, the potential damage to sugarcane crops caused by parasitic nematodes is often underestimated. The main nematodes present in sugarcane fields are root-lesion (Pratylenchus spp.), spiral (Helicotylenchus spp.), root-knot (Meloidogyne spp.), dagger (Xiphinema spp.), stunt (Tylenchorhynchus spp.), ring (Criconemella spp.), and stubby (Paratrichodorus spp.). Among these, Meloidogyne javanica and Pratylenchus zeae are the most damaging nematode species. Management of nematodes is a challenging task as there are no clear symptoms of their presence, and they often come in multiple species with varying levels of pathogenicity. Moreover, the management options available are not always effective. Integrated nematode management is a sustainable strategy for controlling nematode infestations. It involves using all possible methods to suppress the parasitic nematode population in a compatible manner and reduce it below economic threshold levels. This article focuses on the challenges of managing nematodes in sugarcane and highlights the opportunity for implementing a sustainable nematode management strategy.

VND Genes Redundantly Regulate Cell Wall Thickening during Parasitic Nematode Infection.

Plant parasitic root-knot nematodes are major agricultural pests worldwide, as they infect plant roots and cause substantial damages to crop plants. Root-knot nematodes induce specialized feeding cells known as giant cells (GCs) in the root vasculature, which serve as nutrient reservoirs for the infecting nematodes. Here, we show that the cell walls of GCs thicken to form pitted patterns that superficially resemble metaxylem cells. Interestingly, VASCULAR-RELATED NAC-DOMAIN1 (VND1) was found to be upregulated, while the xylem-type programmed cell death marker XYLEM CYSTEINE PEPTIDASE 1 was downregulated upon nematode infection. The vnd2 and vnd3 mutants showed reduced secondary cell wall pore size, while the vnd1 vnd2 vnd3 triple mutant produced significantly fewer nematode egg masses when compared with the wild type. These results suggest that the GC development pathway likely shares common signaling modules with the metaxylem differentiation pathway and VND1, VND2, and VND3 redundantly regulate plant-nematode interaction through secondary cell wall formation.

The other side of the coin: systemic effects of Serendipita indica root colonization on development of sedentary plant-parasitic nematodes in Arabidopsis thaliana.

MAIN CONCLUSION: Upon systemic S. indica colonization in split-root system cyst and root-knot nematodes benefit from endophyte-triggered carbon allocation and altered defense responses what significantly facilitates their development in A. thaliana. Serendipita indica is an endophytic fungus that establishes mutualistic relationships with different plants including Arabidopsis thaliana. It enhances host's growth and resistance to different abiotic and biotic stresses such as infestation by the cyst nematode Heterodera schachtii (CN). In this work, we show that S. indica also triggers similar direct reduction in development of the root-knot nematode Meloidogyne javanica (RKN) in A. thaliana. Further, to mimick the natural situation occurring frequently in soil where roots are unequally colonized by endophytes we used an in vitro split-root system with one half of A. thaliana root inoculated with S. indica and the other half infected with CN or RKN, respectively. Interestingly, in contrast to direct effects, systemic effects led to an increase in number of both nematodes. To elucidate this phenomenon, we focused on sugar metabolism and defense responses in systemic non-colonized roots of plants colonized by S. indica. We analyzed the expression of several SUSs and INVs as well as defense-related genes and measured sugar pools. The results show a significant downregulation of PDF1.2 as well as slightly increased sucrose levels in the non-colonized half of the root in three-chamber dish. Thus, we speculate that, in contrast to direct effects, both nematode species benefit from endophyte-triggered carbon allocation and altered defense responses in the systemic part of the root, which promotes their development. With this work, we highlight the complexity of this multilayered tripartite relationship and deliver new insights into sugar metabolism and plant defense responses during S. indica-nematode-plant interaction.