Hidden Root Wars: How Tiny Nematodes Sabotage Legumes and What Breeding Can Do About It

Legumes are the quiet workhorses of global agriculture. Soybean, chickpea, pea, lentil, common bean, cowpea and faba bean fix atmospheric nitrogen through their symbiosis with rhizobial bacteria, enriching soils, cutting the need for synthetic fertilizers and underpinning sustainable rotations across the world. Yet beneath the soil surface, an almost invisible enemy is quietly draining their productivity. Plant-parasitic nematodes, microscopic roundworms that feed on roots, are estimated to cost legume growers roughly 10 to 14 percent of their yields every year. A comprehensive new review published in the Journal of Agriculture and Food Research by María Córdoba-Sánchez, Diego Rubiales, Pablo Castillo and Juan E. Palomares-Rius synthesises decades of research on the three most damaging nematode groups attacking legumes, and argues that plant breeding, from classical selection to CRISPR gene editing, is the most sustainable weapon available against them.

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