Several prominent examples suggest that the evolution of parasitism is accompanied by nervous system simplification. However, it is unclear if this is a generalizable rule and whether parasite-associated simplification occurs at the level of synaptic connectivity. The nematode esophagus is a specialized neuromuscular feeding organ that varies with diet and lifestyle. Plant-parasitic nematodes are major agricultural pests that feed through a protrusible stylet and release of extensive glandular effectors; however, the neuronal mechanisms controlling parasite feeding are unclear. Here, we used serial-section electron microscopy to reconstruct the esophageal connectome of the infective second-stage juvenile of the soybean cyst nematode, Heterodera glycines, and compared it with those of the free-living species Caenorhabditis elegans and Pristionchus pacificus. Similar to these species, H. glycines has 20 esophageal neurons with relatively conserved cell body positions. Despite this conservation, the H. glycines chemical synaptic network is highly reduced in output to musculature. A unique ensheathment of neurons by a gland cell facilitates novel synaptic connectivity in H. glycines. The H. glycines esophageal network is strongly biased toward monadic synapses and shows a greater proportion of neuron-neuron and neuron-gland connections. Consistent with a reduction in motor output, network analysis indicates that the H. glycines esophageal network is smaller and less clustered than free-living species. Using centrality analysis and synthetic ablation, we predict that control of multiple feeding modules in H. glycines depends on distinct neurons compared to free-living species. These findings show how parasitism reshapes a feeding circuit and identify candidate species-specific circuits for parasite control.
Despite their diversity in habitats, nematodes are often considered to have a highly conserved neuroanatomy. This premise is based on only a subset of the nematode phylogenetic tree within the subclass Chromadoria, which includes the model organism Caenorhabditis elegans, thereby limiting our understanding of macroevolutionary trends in nervous system structure. To approach this problem, we used nuclear morphology to quantify the number of neurons in the nematode ventral nerve cord (VNC) across the phylum and identified evolutionary patterns in neuroanatomical organization. Nuclear staining revealed that Dorylaimia has significantly more VNC neuronal nuclei than other taxa in Enoplia and Chromadoria, with some species having four times the number of neurons as C. elegans. These results suggest at least two independent transitions in VNC neuron number across subclasses. To further examine developmental patterns and potential variation in nervous system architecture of species with substantially more neurons than C. elegans, we established an isogenic culture of Mononchus aquaticus (Dorylaimia). We found that while M. aquaticus contained four times as many VNC neuronal nuclei as C. elegans, the VNC had a similar developmental timeline during post-embryonic stages. However, dye-filling assays also revealed an extensive distribution of neurons along the lateral body wall of M. aquaticus, which have no obvious homologs in C. elegans. We further found that M. aquaticus is capable of sustained movement following bisection and speculate that this ability results from a more decentralized neuronal network. Our results provide a roadmap for understanding phylum-wide nervous system evolution and demonstrate large-scale differences in neuroanatomy across the phylum.
Exserohilum turcicum, the causal agent of northern corn leaf blight and sorghum leaf blight, exhibits host-specific interactions at both the species and genotype levels. Although maize- and sorghum-adapted strains are generally restricted to their respective hosts, further specificity is observed in maize through gene-for-gene interactions with Ht resistance genes. In this study, we characterized the infection process of E. turcicum across three interaction types: unadapted (sorghum-specific strain on maize, or maize-specific strain on sorghum), adapted-susceptible (each strain on its respective host), and adapted-resistant (maize-specific strain on the Ht1 maize differential). We collected quantitative data for the early colonization phenotypes using epifluorescence and confocal fluorescence microscopy. There were significant differences between adapted and unadapted interactions at multiple infection steps. In the unadapted interactions, the pathogen formed more appressoria, and the host had more dead cells under the appressoria, suggesting a stronger hypersensitive response. Adapted-susceptible interactions exhibited higher levels of xylem and mesophyll penetration and colonization than unadapted and adapted-resistant interactions. Moreover, successful xylem penetration without colonization was observed in unadapted interactions, whereas adapted-resistant interactions demonstrated both xylem penetration and colonization without secondary mesophyll colonization. Progeny strains adapted to one or both hosts confirmed these patterns and showed no fitness cost associated with dual host adaptation. These findings provide new insights into the basis of host specificity and resistance to E. turcicum and highlight the potential for discovering novel resistance mechanisms by studying unadapted interactions across host species.
Interoceptive paraneurons are neuron-like cells located within internal epithelial cell surfaces that sense internal stimuli to evoke specific behavioral or physiological responses. The elucidation of terminal differentiation programs of paraneurons is expected to provide insights into how epithelial cells acquire neuron-like features during development and possibly also over evolutionary time. We define here the transcriptional programs that control the terminal differentiation of an interoceptive paraneuron class in the nematode Caenorhabditis elegans, called uv1. We show that, as in canonical neurons, the neuron-like secretory features of uv1 are controlled by a combination of CUT homeobox genes, while the combinatorial terminal gene battery that defines the unique functional features of uv1 is jointly controlled by a combination of at least three transcription factors: a LIM homeodomain (LIN-11), a SoxD (EGL-13) and a Pax (EGL-38) family protein. These factors act in a terminal selector-type manner to jointly co-regulate the many distinct uv1-paraneuron specific molecular features, such as sensory and neuromodulatory receptors, neuropeptides, and tyramine synthesis machinery. Our findings demonstrate notable similarities in the dichotomous architecture of gene regulatory programs of neurons and paraneurons.
The success of plant-parasitic nematodes (PPNs) depends on the integration of sensory cues and neuromuscular motor outputs, leading to behaviors such as hatching, host-finding, locomotion, feeding, and reproduction. Although the nervous system is often a target for control, much of our knowledge of PPN nervous system structure and function has been inferred from the free-living nematode Caenorhabditis elegans. However, the past two decades have seen substantial advances in our understanding of PPN nervous systems. These suggest that although many features of PPN neurobiology are conserved across nematodes, the behavioral repertoire of PPNs also requires distinct neuronal, structural, and functional properties that have diverged from their free-living ancestors. This review focuses on host-finding and feeding behaviors and their underlying neuronal basis; however, the diversity of PPNs implies there is much to be discovered in the rich repertoire of PPN behaviors.
Sarcomere networks (formed by lateral connections between myofibrils) are essential for force distribution in striated muscle. Yet, whether these networks remodel to meet changing mechanical demands or contribute to muscle pathology is unclear. Using C. elegans body-wall muscles, we show that sarcomeres form interconnected networks via actin-, myosin-, and actinin-rich junctions that dynamically remodel in response to locomotor activity. Swimming, which imposes greater mechanical demands, enhances sarcomere branching compared to crawling. In dystrophin-deficient dys-1(eg33) mutants, impaired longitudinal anchorage combined with persistent lateral tension leads to myofibrillar buckling and wavy fiber deformation, echoing features of Duchenne muscular dystrophy. These results position C. elegans as a tractable model for dissecting the biomechanical roles of sarcomere networks in muscle adaptation and disease.
Experimental organisms such as the nematode Caenorhabditis elegans are fundamental to biological discovery. The success of C. elegans research has been greatly enabled by infrastructure that allows thousands of scientists to share and access research materials and unpublished information efficiently. Here, we celebrate the worm by interweaving vignettes describing four Nobel Prize-winning discoveries with descriptions of how the major NIH-supported research resources-the Caenorhabditis Genetics Center, WormBase, and WormAtlas-provide invaluable support for all C. elegans research. The synergy between investigation and the availability of shared resources for the C. elegans community is a paradigm for all model organism research, and the continued support of such community research resources will be essential for maximizing impactful discoveries in the future.
Perennial Glycine species are potentially valuable genetic resources that can be used to improve disease resistance in soybean by gene transfer techniques. From a previous screening of perennial Glycine species, we found that G. latifolia plant introduction (PI) 559300 showed a high level of resistance to the southern root-knot nematode (Meloidogyne incognita). Here, we identified a quantitative trait locus (QTL) associated with resistance to M. incognita in G. latifolia by phenotyping recombinant inbred lines (RILs) derived from resistant (PI 559300) and susceptible (PI 559298) G. latifolia accessions and single-nucleotide polymorphism (SNP) markers generated through genotyping by sequencing. The analysis identified a single locus of 1.66 Mb associated with M. incognita resistance on G. latifolia chromosome (Chr) 13 that explained 33.3% of the phenotypic variance. This region contains 114 putative genes, including 16 leucine-rich repeat-containing genes and 7 defense-related genes. F1 hybrids generated from crosses between parental lines showed a comparable resistance level to the resistant parents, suggesting that the identified locus is dominantly inherited. To validate the identified QTL, we developed high-resolution melting (HRM) markers linked to an SNP within this locus. HRM genotyping distinguished homozygous and heterozygous alleles and predicted RIL phenotypes with approximately 80% accuracy. Interestingly, the QTL is syntenic with a locus on G. max Chr13 previously found associated with resistance to root-knot nematodes and other non-nematode pathogens. In summary, the newly discovered locus in the wild perennial G. latifolia has the potential for enhancing M. incognita resistance in soybean.
Strongyloides stercoralis, commonly known as the human threadworm, is a skin-penetrating gastrointestinal parasitic nematode that infects hundreds of millions of people worldwide. Like other Strongyloides species, S. stercoralis is capable of cycling through a single free-living generation. Although S. stercoralis and the free-living nematode Caenorhabditis elegans are evolutionarily distant, the free-living adults of S. stercoralis are similar enough in size and morphology to C. elegans adults that techniques for generating transgenics and knockouts in C. elegans have been successfully adapted for use in S. stercoralis. High-quality genomic and transcriptomic data are also available for S. stercoralis. Thus, one can use a burgeoning array of functional genomic tools in S. stercoralis to probe questions about parasitic nematode development, physiology, and behavior. Knowledge gained from S. stercoralis will inform studies of other parasitic nematodes such as hookworms that are not yet amenable to genetic manipulation. This review describes the basic anatomy of S. stercoralis.
The effects of a fluopyram seed treatment on lesion nematodes (Pratylenchus spp.) and other plant-parasitic nematodes (PPNs) were evaluated on corn in multiple field locations in 2020 and 2021. The highest rate of fluopyram seed treatment (0.15 mg seed −1 ) reduced early season population density of lesion nematodes compared with the base treatment control in 2020 only. However, fluopyram did not affect late season lesion nematode population density and corn yields. Fluopyram seed treatment also had minimal or nonsignificant effects on other PPN species. Based on these results, the effects of fluopyram were tested in vitro on Pratylenchus penetrans. Results demonstrated that fluopyram severely affected motility in P. penetrans. The sensitivity of P. penetrans second-stage juveniles (J2s) to fluopyram was significantly higher than at J4 and adult, suggesting that sensitivity to fluopyram is dependent on developmental stage. In addition, the effects of fluopyram were reversible at an EC 50 but were irreversible at the maximum concentration (25 μg/ml). Overall, our results indicate that fluopyram has potential for controlling P. penetrans, but its efficacy is variable depending on nematode developmental stage and chemical concentration. Further research is needed to determine if these impacts can translate to field scenarios.
Associations between nitrogen (N) management and losses with soil health indicators (SHI) are widely presumed but relatively untested. An on-farm experiment conducted in central Illinois was conducted to test potential relationships of SHI with agroecosystem outcomes of maize (Zea mays L.) yield and N losses under bounding N-fertilization rates of 168 and 252 kg/ha. Chemical (n = 19), physical (n = 11), and biological (n = 14) SHI were measured at 24 locations within a 30 ha field at five timepoints (V3, V10, RT, R6, and post-harvest). Yields did not necessarily reflect N-fertilization rates, with lowest yields (14.5 Mg/ha) under 224 kg/ha. Flow-weighted nitrate-N concentrations were significantly higher under 168 kg N/ha (10.6 mg/L) relative to higher application rates, though cumulative tile nitrate-N loads were similar. SHI varied more by sampling location and time than by N fertilization rate. Depending on the time of sampling, distinct SHI were related to yield and tile N losses. Total soil carbon and permanganate oxidizable carbon (POXC) best explained yield variation, whereas POXC and sand content best explained variation in nitrate-N loss. Nematode indices helped explain variability in yield (Simpson and Shannon indices) and nitrate-N losses (maturity index), supporting recent propositions to integrate nematode measures into soil health assessments. This study provides a basis for expanding to multiyear assessments of SHI linkages with nutrient losses and crop productivity in the North Central United States. Nitrogen (N)-fertilization rates had a limited effect on maize yield and tile drain nitrate-N loss.Maize yield and tile drain nitrate-N loss are related to different soil health indicators (SHI).Combination of SHI associated with yield and nitrate-N loss varied by sampling time.Maize yield was sensitive to the N-fertilization rate at the VT sampling stage.Nematode indices have the potential to serve as SHI.
Plant-parasitic nematodes conduct a series of sophisticated behaviors to complete their life cycles. Among these, locomotion behaviors, including finding the host and migrating to the feeding site, directly affect the success of parasitism. Thus, disrupting locomotion behaviors has the potential to control these parasites. γ-Aminobutyric acid (GABA) is the prominent inhibitory neurotransmitter in nematodes. GABA-immunoreactive neurons are mostly found in motor neurons, where they regulate behaviors in the model nematode C. elegans. However, the GABA system in most stylet-bearing nematodes has received little attention. Using immunohistochemistry, we found variation in the pattern of GABA-immunoreactivity among two major plant-parasites and a fungal feeder. Some of these GABA-immunoreactive neurons lack clear homologs to C. elegans. Pharmaceutical assays showed that applying GABA, its agonist, and its antagonist, can disrupt the locomotion behaviors of these nematodes, although sensitivity to a given compound varied between species. Our data suggest that the GABA system is a potential target for the control of plant-parasitic nematodes.
Root-knot (Meloidogyne incognita (Kofoid & White) Chitwood), reniform (Rotylenchulus reniformis Lindford & Oliveira), and lesion nematodes (Pratylenchus penetrans (Cobb) Filipjev & Schuurmans Stekhoven) are plant-parasitic nematodes that feed on soybean (Glycine max (L.) Merr.) roots, limiting seed production. The availability of resistance in soybeans to these nematodes is limited. However, new sources of resistance can be discovered in wild relatives of agronomic crops. Perennial Glycine species, wild relatives to soybean, are a source of valuable genetic resources with the potential to improve disease resistance in soybean. To determine if these perennials have resistance against nematodes, 18 accessions of 10 perennial Glycine species were evaluated for their response to M. incognita and R. reniformis, and eight accessions of six perennial Glycine species were evaluated for their response to P. penetrans. Pot experiments were conducted for M. incognita and R. reniformis in a growth chamber and in vitro experiments were conducted for P. penetrans. We found both shared and distinct interactions along the resistance-susceptible continuum in response to the three plant-parasitic nematode species. Ten and 15 accessions were classified as resistant to M. incognita based on eggs per gram of root and gall index, respectively. Among them, G. tomentella plant introductions (PIs) 446983 and 339655 had a significantly lower gall index than the resistant soybean check cv. Forrest. Of three R. reniformis resistant accessions identified in this study, G. tomentella PI 441001 showed significantly greater resistance to R. reniformis than the resistant check cv. Forrest based on nematodes per gram of root. In contrast, no resistance to P. penetrans was recorded in any perennial Glycine species.
Lymphatic filariasis (LF) is a chronic debilitating neglected tropical disease (NTD) caused by mosquito-transmitted nematodes that afflicts over 60 million people. Control of LF relies on routine mass drug administration with antiparasitics that clear circulating larval parasites but are ineffective against adults. The development of effective adulticides is hampered by a poor understanding of the processes and tissues driving parasite survival in the host. The adult filariae head region contains essential tissues that control parasite feeding, sensory, secretory, and reproductive behaviors, which express promising molecular substrates for the development of antifilarial drugs, vaccines, and diagnostics. We have adapted spatial transcriptomic approaches to map gene expression patterns across these prioritized but historically intractable head tissues. Spatial and tissue-resolved data reveal distinct biases in the origins of known drug targets and secreted antigens. These data were used to identify potential new drug and vaccine targets, including putative hidden antigens expressed in the alimentary canal, and to spatially associate receptor subunits belonging to druggable families. Spatial transcriptomic approaches provide a powerful resource to aid gene function inference and seed antiparasitic discovery pipelines across helminths of relevance to human and animal health.
Plant-parasitic nematodes feed on soybean roots resulting in potential yield losses. Surveys of nematodes in certified organic soybean fields have been infrequent compared with surveys in nonorganic soybean fields. We conducted a nematode survey from certified organic soybean fields in northern and central Illinois and southern Wisconsin to determine the frequency and population densities of plant-parasitic and free-living nematodes. Fields surveyed included both long-term (with soybean planted every fifth year or longer in the rotation) and short-term (with soybean planted every third year in the rotation). A total of 27 composite soil samples, each consisting of multiple cores to a depth of 20 cm, were collected from 14 fields in 2019. Common plant-parasitic nematode taxa included spiral (Helicotylenchus spp.), lesion (Pratylenchus spp.), cyst (Heteroderidae), stunt (Tylenchorhynchus spp.), dagger (Xiphinema spp.), and pin nematodes (Paratylenchus spp.). Among the taxa, spiral, lesion, and dagger nematodes were above previously reported damage threshold levels in some fields. From the summer season–sampled soils, cyst nematode population densities and nematode abundance were significantly higher and lower, respectively, from fields under short-term versus long-term rotation with soybean. From the fall season–sampled soils, the structure index but not the other diversity and community indices of free-living nematodes were significantly higher from fields under long-term versus short-term rotation with soybean. Overall, these results provide evidence for the occurrence of plant-parasitic and free-living nematodes from organically farmed soybean fields in Illinois and Wisconsin that varied in rotation length.
The Featured Creatures collection provides in-depth profiles of insects, nematodes, arachnids and other organisms relevant to Florida. These profiles are intended for the use of interested laypersons with some knowledge of biology as well as academic audiences. Rice root-knot disease is caused by different Meloidogyne species (Meloidogyne graminicola, M. hainanensis, M. incognita, M. javanica, M. arenaria, M. oryzae, M. salasi, and M. tryticoryzae). However, Meloidogyne graminicola is considered the most damaging root-knot species to Asian rice cultivation due to its ability to survive under flooded soil conditions. This nematode has been found in rice nurseries, rainfed upland rice and lowland rice but is also widespread in deep-water, irrigated rice production systems. Yield loss due to Meloidogyne graminicola ranges from 28%–87% depending on disease severity and cultivar.
Nervous systems are incredibly complex networks that, in order to understand, we rely on models like Caenorhabditis elegans to deconstruct. Due to the prevalence of C. elegans and other derived nematode research, it was long assumed that nematode nervous systems were highly conserved across the phylum. Previous evidence revealed that within the derived clades, the assumption of conservation was wrong and that the timing of neuronal development varied. As these previous accountings disregarded the basal clades except for some sporadic observations, this research endeavored to corroborate that the nervous systems of basal nematodes are in fact the most complex and there is a nervous system simplification from the basal to the derived clades. My findings did indeed reveal a simplification of the nerve cord, specifically there appears to be a decrease in ventral nerve cord neurons between the basal and derived clades, which adds further evidence that class Enoplea bears most similarity to the nematode ancestor. A potential reason for nervous system simplification could lie in marine pressures as large marine nematodes are adapted to move through sediment and have more neurons in their ventral nerve cords while smaller marine worms can navigate the water column and were observed to have less neurons, though this hypothesis needs to be more thoroughly investigated. In addition, ventral nerve cord development within Mononchidae appears to be consistent with derived clades and despite basal clade indeterminate development, Mononchidae nervous systems are invariant as adults. Considering all instances of recorded ventral nerve cord development, it appears the precise timing of development shifts but there is always a moment of rapid neurogenesis, often preceding a molt, like what was observed within Mononchidae. These ABSTRACT Comparative analyses of the nematode ventral nerve cord have been limited to essentially only the derived clades. These investigations found that in spite of the long-running belief that the nematode nervous system is highly conserved, there was variety within the derived clade ventral nerve cords. This study endeavors to expand upon the derived clade data by including the basal clades and drawing comparisons between not only the two groupings but also between classes Enoplea and Chromadorea. In addition, I investigate Mononchus laminatus ventral nerve cord development to compare it against previous reports. The findings indicate that there was a significant depression of ventral nerve cord neurons from Enoplea to Chromadorea as well as from basal to derived clades. M. laminatus also features rapid neurogenesis during ventral nerve cord development, which is consistent with derived species experiencing a spike in neurons prior to a molt, though the timing varied between species. Together, these results represent that the nematode nervous system is not as highly conserved as previously argued; in fact, neuron numbers and neuron developmental timing are subject to change.