Root-knot-nematode-derived mimics of RGF peptides hijack host signalling to orchestrate feeding site formation

Root-knot nematodes establish long-term parasitic relationships with diverse hosts by inducing specialized feeding cells. However, the molecular mechanisms by which nematodes manipulate this developmental reprogramming process remain largely unknown. Here we identify a class of ROOT MERISTEM GROWTH FACTOR (RGF)-like peptide effectors conserved in root-knot nematodes. MgRGF from Meloidogyne graminicola and MiRGF1 from M. incognita are expressed in subventral gland cells during early infection and secreted into the host apoplast. Functional analysis reveals that nematode RGFs are critical for feeding site development. Intriguingly, these peptides elicit host-specific outcomes in Arabidopsis and rice, involving both cell proliferation and expansion-two processes essential for establishing feeding cell identity. Further genetic and biochemical evidence demonstrates that nematode RGF peptides functionally mimic plant endogenous RGFs by hijacking the host RGI-receptor-mediated signalling pathway to regulate root growth and promote parasitism. Beyond PLT transcription factors, PSY peptide genes were identified as key downstream components of this RGF signalling cascade in rice. Functional characterization of OsPSY5 suggests its positive role in promoting cell elongation and facilitating nematode parasitism. Our findings unveil a cross-kingdom mimicry strategy whereby root-knot nematode-secreted RGF peptides co-opt host RGF signalling to orchestrate feeding cell formation, highlighting potential targets for engineering nematode resistance in crops.