Light-Signalling Regulators GmSTF3/4 Enhance Soybean Susceptibility to Cyst Nematodes via Activation of Sugar Transporters

Abstract

Soybean cyst nematode (SCN; Heterodera glycines Ichinohe) is a plant-parasitic nematode that causes substantial yield losses in soybean production. Light signalling is a critical environmental factor that influences photomorphogenesis and carbohydrate metabolism. However, its transcriptional regulation under pathogen-induced stress remains unclear. In this study, the biological function and regulatory mechanism of TGACG-motif binding factor 3/4 (GmSTF3/4), a shoot-to-root mobile protein in soybean (Glycine max), were investigated during H. glycines infection. Evidence was provided that light signalling modulated soybean susceptibility to cyst nematode, marked by light-enhanced nematode infection and upregulation of photoreceptor gene expression post-infection. GmSTF3/4 interacted with CONSTITUTIVE PHOTOMORPHOGENIC1a (GmCOP1a) and mediated its degradation. The nematode was identified to accelerate the shoot-to-root translocation of GmSTF3/4. Phenotypic analysis revealed that GmSTF3/4 promoted nematode development, whereas GmCOP1a exerted an antagonistic effect. Furthermore, the integrated analyses of Cleavage Under Targets and Tagmentation (CUT&Tag) and RNA sequencing (RNA-seq) indicated that GmSTF3/4 bound to the promoters of multiple sugar transporter genes, including GmSWEET8, GmSWEET10b, GmSWEET13d, GmSUC8, and GmERD6-like. The subcellular localization confirmed their plasma membrane targeting, and functional validation in yeast demonstrated the sucrose transport activity of four of these genes. Transient expression assays of five candidate genes during nematode infection supported the positive regulatory role of GmSWEET10b in facilitating nematode infection and development, a result further supported by the Gmsweet10b mutant. Collectively, this study revealed that GmSTF3/4 enhanced soybean susceptibility to cyst nematodes by transcriptionally activating sugar transporter genes, offering a new avenue for SCN-resistance research.