How Parasitic Nematodes Hijack Plant Cells to Build Their Own Feeding Machines

Plant-parasitic nematodes are among the most destructive agricultural pests on the planet, and a new review published in the journal Crop Health lays bare just how sophisticated their attack really is. Rather than simply feeding on plant tissue, sedentary endoparasitic nematodes such as root-knot nematodes (Meloidogyne spp.) and cyst nematodes (Globodera and Heterodera spp.) perform a kind of biological sorcery: they force differentiated root cells to abandon their normal identity, re-enter the cell cycle, and rebuild themselves into dedicated nutrient factories. The review, authored by Abdulmujib Gboyega Yusuf and Tesleem Taye Bello, synthesizes decades of molecular work to explain how these microscopic worms exploit cellular plasticity and transcriptional reprogramming to construct specialized feeding sites, and how plants fight back.

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