The AP2/ERF transcription factor GmTINY mediates ethylene regulation of Rhg1-conferred resistance against soybean cyst nematode

The soybean complex resistance locus Rhg1 is a primary contributor to the control of soybean cyst nematode (Heterodera glycines; SCN), a major threat to soybean production worldwide. Two genes within this locus, GmAAT_Rhg1 and GmSNAP18, are upregulated during SCN infection. In this study, we found that SCN-resistant soybean varieties exhibit elevated ethylene (ETH) production upon infection. Exogenous ETH application further increased GmAAT_Rhg1 and GmSNAP18 transcript levels and enhanced the SCN-resistance response. These genes are divergently transcribed from a shared promoter containing three ERELEE4 ethylene-responsive elements (AATTCAAA). Using yeast one-hybrid screening, we identified the AP2/ERF transcription factor GmTINY (Glyma.01G147600) as an ERELEE4-binding protein. GmTINY is localized to the nucleus, and its expression is induced by both ETH treatment and SCN infection. Molecular, biochemical, and genetic analyses showed that GmTINY binds to the Rhg1 ERELEE4 elements and regulates the expression of GmAAT_Rhg1 and GmSNAP18, thereby enhancing SCN resistance. Additionally, overexpression of GmTINY induced several xyloglucan endotransglycosylase/hydrolase (XTH) genes, particularly GmXTH2, which is implicated in cell wall remodeling and restricts nematode development beyond the J2 stage. Together, these findings reveal an ETH-GmTINY signaling axis that regulates both Rhg1-mediated and cell wall-related resistance pathways, providing new insights for engineering durable SCN resistance in soybean.