The review focuses on three nematode groups with sharply different parasitic lifestyles. Root-knot nematodes of the genus Meloidogyne are sedentary endoparasites that dominate tropical and subtropical soils and attack a wide range of legumes including soybean, chickpea, common bean, pea and cowpea. Cyst nematodes of the genus Heterodera, also sedentary endoparasites, are chiefly temperate-region specialists of soybean, pea, lentil and chickpea. Root-lesion nematodes of the genus Pratylenchus are migratory endoparasites that roam through root tissues across temperate and subtropical zones, leaving necrotic trails in their wake. Each group penetrates roots as second-stage juveniles, but what happens next determines the character of the damage, the difficulty of diagnosis and the breeding strategies needed for control.

Root-knot and cyst nematodes are master manipulators of plant development. After entering the root, they migrate to the vascular cylinder and induce permanent feeding structures that reprogram host cells. Root-knot nematodes trigger giant cells, formed by repeated nuclear division without cell division, producing large multinucleate cells packed with dense cytoplasm and proliferating organelles, all embedded within the familiar root galls. Cyst nematodes instead fuse adjacent cortical and vascular cells into a syncytium, a single metabolically hyperactive feeding organ sustained for weeks or months. Both structures are orchestrated by nematode-secreted effectors, including cell wall-modifying enzymes, cytoskeleton-binding proteins and hormonal mimics that hijack auxin, cytokinin, salicylic acid and jasmonic acid pathways. The nematodes even co-opt developmental regulators such as LBD16, which governs lateral root initiation, and WRKY23, a transcription factor involved in auxin redistribution, effectively redirecting the plant’s own root-building machinery toward parasite nutrition.

Fascinating histological work in chickpea shows that different Meloidogyne species build subtly different feeding sites. Meloidogyne artiellia, a Mediterranean specialist of cool-season legumes, induces smaller galls with limited cortical hyperplasia compared with M. arenaria, M. incognita or M. javanica, and its giant cells contain fewer but substantially larger nuclei, with distinctive amoeboid protuberances absent from the feeding cells of other species. Intriguingly, gall size depends on the specific host-parasite pairing rather than the nematode alone: M. artiellia produces large galls on chickpea but only small ones on faba bean, while the reverse holds for M. incognita. Meanwhile M. hapla, the northern root-knot nematode adapted to cool temperate regions, reproduces by facultative meiotic parthenogenesis, giving it greater capacity for genetic recombination and adaptation to host resistance than the strictly mitotic parthenogens.

Root-lesion nematodes play a different game. Rather than settling down, Pratylenchus species move inter- and intracellularly through the root cortex, feeding with their stylets and secreting cell wall-degrading enzymes that cause extensive necrosis. Because all motile stages can feed and migrate, the damage accumulates through repeated cycles of invasion. The result is chronic stress: impaired water and nutrient uptake, reduced nodulation, and wounds that open the door to fungal pathogens such as Fusarium and Rhizoctonia. In rainfed, low-input systems, where many legumes are grown precisely because they require few external inputs, these migratory parasites are particularly devastating, and their populations can build across successive seasons in continuous or poorly diversified rotations.

Perhaps the most consequential finding of the review is how nematode infection sabotages the legume-rhizobia symbiosis itself. Nitrogen fixation is an energetically expensive, precisely coordinated process, and nematodes disrupt it at every level. They compete with rhizobia for infection sites and host resources, reducing nodule number and efficiency. They divert photoassimilates toward their feeding structures, which act as powerful metabolic sinks. At the molecular level, infection alters the expression of key symbiosis genes including NIN, ENOD40, CCaMK, NFR5 and SYMRK, and suppresses calcium spiking within the common symbiosis signalling pathway. The nematodes are also hypothesised to prematurely activate the autoregulation of nodulation pathway, a systemic feedback loop involving CLE peptides and shoot receptors such as HAR1, thereby repressing nodule initiation across the whole root system. In parallel, altered flavonoid biosynthesis impairs the chemical signals that attract rhizobia to the root. The outcome is a sophisticated molecular hijacking in which parasitism is favoured over mutualism, and biological nitrogen fixation plummets.

Against this arsenal of parasitism, legumes deploy layered defences. Pre-infection resistance includes structural barriers such as lignin and suberin deposition in epidermal and cortical cell walls, which are especially effective against migratory nematodes, as demonstrated in lentil and pea. Root exudates containing flavonoids, phenolics and triterpenoid saponins can disrupt nematode chemosensation or repel infective juveniles, while also recruiting beneficial microbes such as Pseudomonas, Bacillus and mycorrhizal fungi. Once nematodes breach the root, post-infection defences take over: the hypersensitive response kills cells around the feeding site, reactive oxygen species accumulate as both antimicrobials and signals, and legumes synthesise nematicidal phytoalexins such as glyceollin in soybean and pisatin in pea. Hormonal crosstalk is central here, with salicylic acid dominating defence against cyst nematodes and jasmonic acid and ethylene driving responses to migratory species and root-knot nematodes.

The genetic basis of resistance is best understood in soybean, where the rhg1 locus, whose effect depends on copy number variation of genes encoding an amino acid transporter, the alpha-SNAP protein and WI12, works synergistically with Rhg4, which encodes a serine hydroxymethyltransferase, to defeat the soybean cyst nematode. In cowpea, the major Rk locus confers resistance to root-knot nematodes, while in Medicago truncatula the CRE1 gene triggers a hypersensitive response that blocks feeding-site establishment. Resistance to root-lesion nematodes, by contrast, is typically quantitative and polygenic; in chickpea, valuable sources of resistance to Pratylenchus thornei have been found in wild Cicer species, with QTLs on chromosomes Ca4 and Ca7 now supported by SNP markers for marker-assisted selection. Notably, some chickpea accessions such as ICC 14216K and UC 27 show combined resistance to both M. artiellia and the fungal pathogen Fusarium oxysporum f. sp. ciceris, and lupin species consistently reduce Meloidogyne hapla populations, making them potential dead-end trap crops in rotation.

The breeding toolbox is expanding rapidly. Marker-assisted selection has already delivered resistant soybean and chickpea cultivars, and genomic selection, which captures the cumulative effect of thousands of genome-wide markers, is proving well suited to polygenic resistance traits, with high predictive accuracies reported in common bean and chickpea. CRISPR/Cas9 editing offers a route to durable resistance by knocking out susceptibility genes that nematodes exploit, such as sugar transporters and cell-wall-loosening proteins; recent knockout of GmSNAP14 in soybean enhanced resistance to the soybean cyst nematode, confirming vesicular trafficking as a viable editing target. High-throughput phenotyping, from rhizotrons and 3D root imaging to drone-mounted multispectral sensors, is accelerating the measurement of galling, lesion severity and nodulation damage, and coupling phenomics with genomic prediction promises faster selection cycles.

The authors also point toward a holistic future in which breeding embraces the soil itself. Trichoderma fungi suppress nematodes through chitinases and induced systemic resistance, Bacillus species produce nematicidal lipopeptides, and arbuscular mycorrhizal fungi prime legume defences while improving nodulation. Because plant genotype shapes the rhizosphere microbiome, microbiome-recruitment traits may be heritable and selectable, and intercropping with marigold or maize can add allelopathic suppression of root-knot nematodes. Yet major gaps remain: minor and winter legumes are poorly characterised, resistance to root-lesion nematodes is far less understood than for sedentary species, and microbiome-based resistance has been demonstrated mostly under controlled conditions. For low-value legume crops grown on marginal lands, where nematicides are economically unfeasible, the review concludes that breeding for resistance is not merely one option among many but often the only practical path to protecting the nitrogen-fixing partnership on which sustainable agriculture depends.

Subject of Research: Interactions between root-knot, root-lesion and cyst nematodes and legume crops, and breeding strategies for nematode resistance

Article Title: Interactions of root-knot, root-lesion and cyst nematodes with legumes and implications for plant-breeding

Article References: Córdoba-Sánchez, M., Rubiales, D., Castillo, P., & Palomares-Rius, J. E. (2026). Interactions of root-knot, root-lesion and cyst nematodes with legumes and implications for plant-breeding. Journal of Agriculture and Food Research, Article 103358. https://doi.org/10.1016/j.jafr.2026.103358

Image Credits: AI Generated

DOI: 10.1016/j.jafr.2026.103358

Keywords: legumes, plant-parasitic nematodes, root-knot nematodes, cyst nematodes, root-lesion nematodes, nitrogen fixation, rhizobia symbiosis, plant breeding, marker-assisted selection, genomic selection, CRISPR, soil microbiome

The two most intensively studied feeding structures are giant cells and syncytia, and their developmental strategies could hardly be more different. Root-knot nematodes induce giant cells through rounds of mitosis that lack cytokinesis, combined with repeated endoreduplication, producing enlarged, multinucleate cells stuffed with dense cytoplasm. These cells develop wall ingrowths resembling xylem transfer cells, dramatically increasing the plasma membrane surface area available for solute exchange. Cyst nematodes, by contrast, dissolve the cell walls of neighboring root cells and fuse their protoplasts into a syncytium, a single continuous multinucleate compartment that can eventually encompass more than two hundred cells. Remarkably, three-dimensional reconstructions have shown that individual giant cells can expand roughly sixty-fold in volume between three and forty days after infection, a transformation driven by cell wall loosening and continuous cytoskeletal rearrangement.

None of this happens by accident. The engine of the entire process is the nematode’s stylet, a hollow, protrusible spear connected to esophageal gland cells that secrete a cocktail of effector proteins directly into host tissue. These effectors include cell wall-degrading enzymes such as cellulases, hemicellulases, and pectinases that ease penetration and migration, but the more intriguing molecules are those that manipulate host physiology from within. Once inside plant cells, effectors travel to the nucleus, the cytoplasm, or the apoplast, where they bind host proteins and bend gene expression to the parasite’s advantage. In compatible interactions, the host’s normal developmental pathways are subverted: the cell cycle is reactivated, cell wall architecture is remodeled, and metabolism is redirected toward feeding site construction.

Plant hormones sit at the center of this manipulation. Local auxin accumulation is a master switch for feeding site formation, and nematodes have evolved multiple ways to boost it. The cyst nematode effector 19C07 interacts with the auxin influx transporter LAX3 to enhance auxin flow into selected cells and upregulate cell wall-degrading enzymes, while the effector 10A07 binds the auxin response repressor IAA16, destabilizing its suppressive grip on auxin response factors and even recruiting a host kinase, IPK, to shepherd it into the nucleus. Cytokinin plays an equally critical role in driving cell cycle reactivation at the G1/S transition. Strikingly, Heterodera schachtii carries its own isopentenyltransferase gene, effectively synthesizing cytokinin from the parasite’s side of the interface; silencing that gene suppresses feeding site expansion, and Arabidopsis mutants lacking the cytokinin receptors AHK3 and AHK4 show markedly reduced susceptibility. Ethylene plays a double game, sometimes attracting nematodes to roots and promoting syncytial cell wall expansion, yet also capable of reducing infection through interactions with the receptor ETR1, a contradiction the review flags as an open question.

At the same time, nematodes must dismantle the plant’s immune system, which operates in two layers. Pattern-triggered immunity begins when cell surface receptors detect pathogen-associated molecular patterns, triggering reactive oxygen species production, MAP kinase cascades, and cell wall reinforcement. A deeper layer, effector-triggered immunity, mediated by intracellular resistance proteins, produces localized cell death that starves the parasite. Nematode effectors attack both layers with surgical precision. In rice, the Meloidogyne graminicola effector MgMO237 suppresses pattern-triggered immunity by binding multiple defense-related host proteins, while MgMO289 manipulates the host’s reactive oxygen system through the copper metallochaperone OsHPP04. The M. javanica effector MjTTL5 recruits the thioredoxin reductase subunit AtFTRc to scavenge ROS during the oxidative burst, and the sugar beet cyst nematode effector 10A06 targets spermidine synthase 2 to bolster antioxidant capacity at the infection site. In Globodera rostochiensis, the ubiquitin carboxyl extension protein GrUBCEP12 suppresses flg22-induced immunity, and the effector Gr29D09 disables the potato hexokinase StHXK1.

The review devotes particular attention to transcription factors, the master regulators that nematodes either hijack or exploit as part of the plant’s own response. Functional studies in Arabidopsis and tomato have identified fifteen co-regulated transcription factor hubs during infection, spanning the MYB, WRKY, and ARF families. One especially revealing case is DEL1, an atypical E2F factor that suppresses salicylic acid accumulation and lignin biosynthesis during root-knot infection by repressing EDS5, a gene encoding a salicylic acid transporter. del1 mutants accumulate more salicylic acid, lignify their galls more heavily, and resist infection, while the nematode’s own effector Mi-ISC-1 independently attacks the isochorismate pathway that feeds salicylic acid synthesis. The convergence of host and parasite manipulation on the same pathway underscores how central it is to the outcome of infection.

The WRKY family illustrates the bewildering duality of transcriptional control in these interactions. WRKY11 and WRKY17 act as positive defenders in Arabidopsis, with mutants of either gene showing heightened susceptibility to both cyst and root-knot nematodes. Yet in tomato, SlWRKY16 and SlWRKY31 behave as negative regulators, and their overexpression enhances infection while suppressing defense-related genes. SlWRKY45 goes further: it interacts with JAZ repressor proteins and, once released, binds the promoter of the jasmonic acid biosynthesis gene AOC, throttling jasmonate production and opening the door to the parasite. Meanwhile, WRKY23 promotes feeding site formation by inducing auxin-responsive genes, and bHLH25 and bHLH27 act synergistically to support syncytium development in cyst nematode infection. The same family can thus contain both shields and traitors, and which role a given member plays depends on species, tissue, and developmental stage.

Effectors also reach deep into the plant’s information-processing machinery. The M. incognita effector Mi16D10 binds SCARECROW-like GRAS transcription factors to accelerate giant cell formation, and Mi2G02 hijacks the trihelix factor GT-3a, converting it into a transcriptional inhibitor that silences cell development genes through the 26S proteasome pathway. The cyst nematode effector 30D08 targets AtSMU2, a spliceosome component, perturbing pre-mRNA splicing across thousands of transcripts, and MiEFF18 attacks the core spliceosomal protein SmD1 to fine-tune transcripts governing the cell cycle and cytoskeleton. Indeed, root-knot nematodes induce splicing reprogramming of roughly 2,898 genes involving more than 9,065 transcripts during gall formation. Beyond transcription, epigenetic mechanisms add another layer of control: DNA hypomethylation occurs early in infection, potentially activating stress genes, while the effector Hs32E03 interacts with the histone deacetylase HDT1 to alter acetylation patterns in ribosomal DNA regions, reshaping chromatin to favor parasitism.

What makes the review compelling is its translational ambition. The authors argue that understanding these molecular vulnerabilities opens concrete routes to resistance: CRISPR/Cas editing of transcription factors that mediate feeding site formation, breeding informed by epigenetic marks associated with defense, and host-induced gene silencing that knocks out essential nematode effectors. They also champion single-cell and single-nucleus RNA sequencing as the next frontier, since bulk transcriptomics averages away the cellular heterogeneity that defines galls and syncytia, and functional redundancy among transcription factors often masks the effect of silencing any single gene. Gland-cell-specific transcriptomics is meanwhile expanding the catalog of known effectors, offering a moving target that breeders and biotechnologists must track.

The bigger picture is one of an evolutionary arms race fought at the level of gene regulation. Nematodes exploit conserved host hubs, from the COP9 signalosome to JAZ proteins and translation initiation factors, that other pathogens also target, suggesting shared vulnerabilities that could yield broadly durable resistance. Plants, for their part, retain the capacity to resist when their immune signaling outpaces the parasite’s reprogramming, as resistant interactions shift the sex ratio of developing nematodes toward males and curtail reproduction. Decoding the precise choreography of effectors, hormones, transcription factors, and epigenetic marks, the authors conclude, is not merely an academic exercise but a prerequisite for engineering crops that refuse to build the parasite’s dining room, a goal with enormous implications for global food security as biotic pressures on agriculture intensify.

Subject of Research: Molecular mechanisms of feeding site formation and transcriptional reprogramming in plant-parasitic nematode interactions

Article Title: Cellular plasticity and transcriptional reprogramming in plant-nematode interactions: insights into feeding site formation and plant defense

Article References: Yusuf, A. G., & Bello, T. T. (2025). Cellular plasticity and transcriptional reprogramming in plant-nematode interactions: insights into feeding site formation and plant defense. Crop Health, 3(1), Article 16. https://doi.org/10.1007/s44297-025-00056-1

Image Credits: AI Generated

DOI: 10.1007/s44297-025-00056-1

Keywords: plant-parasitic nematodes, root-knot nematode, cyst nematode, giant cells, syncytium, transcription factors, effector proteins, auxin signaling, cytokinin, plant immunity, CRISPR, RNA interference

The review, authored by Abdulmujib Gboyega Yusuf, Tesleem Taye Bello and Saheed O. Anifiwoshe, focuses on a family of effector proteins produced in the nematode’s esophageal glands and injected directly into host cells through a hollow, retractable stylet. Effectors are pathogen-derived molecules that modify host cellular processes to the parasite’s advantage. In sedentary nematodes, they are indispensable: without them, the nematode cannot induce the permanent feeding sites, known as giant cells or syncytia, upon which its entire life cycle depends. If feeding site formation fails, the life cycle aborts or the parasite develops into mobile males that abandon the root tissue altogether.

The infection process itself is a carefully staged operation. Second-stage juveniles hatch in the soil, are attracted to host roots, and penetrate the epidermis using both mechanical force and an arsenal of cell wall-degrading enzymes. Genomic analysis of Meloidogyne incognita has revealed more than 81 genes encoding such enzymes, including pectate lyases, beta-1,4-endoglucanases and xylanases. During this early invasive phase, the nematode’s subventral esophageal glands are most active, secreting effectors that facilitate penetration, migration and the suppression of initial immune responses. As the worm settles into its sedentary lifestyle, these glands degenerate and the dorsal gland takes over, producing the effectors that reprogram host development and sustain the long-term biotrophic interface.

It is among these dorsal gland effectors that the peptide hormone mimics reside. The review highlights five major families: CLE-like peptides that mimic CLAVATA3/EMBRYO SURROUNDING REGION-related signals controlling stem cell identity and meristem activity; CEP-like peptides that co-opt nutrient signaling and root architecture pathways; IDA-like peptides that exploit cell separation programs; RALF-like peptides that manipulate cell wall integrity and immunity; and PSY-like peptides that imitate sulfated growth-regulating peptides. Each of these families engages specific host receptor-like kinases, allowing the parasite to plug directly into conserved plant signaling modules that govern growth, cell identity and defense.

The CLE mimics were the first to be characterized, emerging from motif-based database searches that revealed sequence similarities between plant CLE peptides and gland-secreted peptides of the soybean cyst nematode Heterodera glycines. Plant CLE peptides are produced as prepropeptides bearing a signal peptide, a variable domain and a conserved twelve-amino-acid CLE motif, and they act through leucine-rich repeat receptor-like kinases such as CLAVATA1. Cyst nematode CLE-like effectors, secreted from the dorsal gland during sedentary stages, replicate this architecture and function as ligands that promote the cellular reprogramming of the developing syncytium. B-type CLE peptides in H. glycines show homology to the Tracheary Element Differentiation Inhibitory Factor, suggesting the mimics may also promote the vascularization of feeding sites and integrate with auxin signaling through HD-ZIP III transcription factors. Intriguingly, the host’s own CLE peptides are upregulated during root-knot nematode infection, and reduced gall formation in the Arabidopsis cle3 mutant indicates that endogenous CLE signaling is co-opted to reinforce gall development, meaning nematode and plant peptides may converge on shared receptor hubs.

CEP-like peptides represent an even more striking case of cross-kingdom deception, because plant-parasitic nematodes are the only known non-plant organisms that biosynthesize CEPs. The well-studied MhCEP11 from Meloidogyne hapla shows striking sequence homology to CEP peptides of Medicago truncatula and Arabidopsis. Root-knot nematode CEPs are short peptides of roughly fifteen amino acids that lack a pro-domain, a simplification that may streamline processing and permit rapid apoplastic delivery to host receptors. Even a single amino acid substitution can alter peptide activity, indicating considerable plasticity in host-specific virulence, and comparative analyses suggest these peptides evolved independently within Meloidogyne species, potentially contributing to their extraordinarily broad host ranges.

The RALF mimics illustrate how the parasites target the interface between development and immunity. MiRALF1, secreted by M. incognita, binds FERONIA, a malectin-like receptor kinase that senses cell wall integrity and modulates immune responses. Nematode development is significantly impaired in fer mutants of Arabidopsis, underscoring the receptor’s importance for virulence. A search of the M. incognita genome uncovered eighteen RALF-like peptides, many retaining the conserved YISY and RGC motifs of plant RALFs, yet lacking the pro-domains, canonical dibasic cleavage sites and certain cysteine residues found in their plant counterparts. These structural simplifications likely allow rapid secretion of the bioactive peptide directly into the apoplast. In soybean, a nematode RALF-like peptide interacts with the FER-like receptor GmLMM1, and a corresponding mutant line displays increased resistance to root-knot infection, confirming the pathway as a susceptibility factor.

Perhaps the most technically fascinating aspect of these effectors is their dependence on precise post-translational modification and trafficking. The cyst nematode effector GrCLE1 from Globodera rostochiensis is processed into a twelve-amino-acid glycopeptide carrying hydroxylated and tri-arabinosylated proline residues, modifications that enhance receptor affinity and shield the peptide from proteolytic degradation in the apoplast. Incomplete modification yields intermediate forms with reduced activity. MhCEP11 requires hydroxylation at two proline positions for full functionality, and PSY-like effectors depend on tyrosine sulfation, likely catalyzed by a nematode-encoded sulfotransferase, to engage the PSY1 receptor. Delivery routes also differ: RALF and IDA mimics act apoplastically, whereas the cyst nematode effector HgCLE2 is first delivered into the host cytoplasm and then trafficked to distal apoplastic targets, a route governed by its N-terminal variable domain. Secretion is tightly coordinated with developmental stage, with most peptide effectors expressed specifically in the dorsal gland during sedentary periods, and some, such as the CLE effectors of H. glycines, timed to coincide with peaks of host root meristem activity.

The review also addresses the evolutionary origins of this molecular deception, attributing it to a convergence of horizontal gene transfer, gene duplication with neofunctionalization, and adaptive sequence evolution. Certain CLE-like genes in cyst nematodes lack clear phylogenetic continuity within the nematode lineage and may have originated from rhizosphere microbes, while roughly 54 percent of effector families in H. schachtii show no detectable homology outside sedentary nematodes, consistent with recent acquisition or rapid divergence under host-imposed selection. Transposable elements frequently cluster near effector loci, potentially shuffling promoter regions and secretion motifs. Comparative genomics reveals a broader evolutionary trade-off: migratory nematodes rely on peptidases and pectin-degrading enzymes for mechanical invasion, whereas sedentary species shifted toward effectors that mimic developmental signals, enabling long-term modulation of host transcriptional programs. Notably, the bacterium Xanthomonas oryzae independently evolved the sulfated peptide RaxX, which mimics plant PSY peptides to bind the rice XA21 receptor, a striking example of convergent evolution toward the same peptide-receptor modules.

The authors identify several critical research gaps and translational opportunities. Structure-based prediction tools, including deep-learning models trained on AlphaFold-derived features, could illuminate effector-receptor interfaces, while advanced proteomics may map the full landscape of effector modifications. Live-cell imaging with minimal fluorescent tags and proximity-labeling techniques such as TurboID could reveal how host machinery is co-opted for effector maturation and delivery. On the applied side, CRISPR-Cas9 editing could modify host receptor kinases to evade effector binding without disrupting normal signaling, while host-induced gene silencing, synthetic decoy receptors and effector-based diagnostics offer further routes to durable resistance. As the review concludes, targeting the mimicry interface itself, rather than the whole parasite, may prove the most precise and ecologically compatible strategy for protecting crops from these masterful molecular impostors.

Subject of Research: Peptide hormone mimicry and effector trafficking in sedentary plant-parasitic nematodes

Article Title: Molecular mimicry and trafficking of peptide effectors in sedentary nematodes: emerging drivers of feeding site formation and host signaling hijack

Article References: Yusuf, A. G., Bello, T. T., & Anifiwoshe, S. O. (2026). Molecular mimicry and trafficking of peptide effectors in sedentary nematodes: emerging drivers of feeding site formation and host signaling hijack. Crop Health, 4(1), Article 1. https://doi.org/10.1007/s44297-025-00063-2

Image Credits: AI Generated

DOI: 10.1007/s44297-025-00063-2

Keywords: plant-parasitic nematodes, molecular mimicry, peptide effectors, CLE peptides, RALF, CEP, PSY, feeding site formation, receptor-like kinases, horizontal gene transfer, post-translational modification, crop protection