GmERFVII transcription factors upregulate PATHOGENESIS-RELATED10 and contribute to soybean cyst nematode resistance

Abstract Low oxygen availability within plant cells arises during plant development but is exacerbated under environmental stress conditions. The group VII ETHYLENE RESPONSE FACTOR (ERFVII) transcription factors have been identified as pivotal regulators in the hypoxia response to abiotic stress. However, their roles in transcriptional regulation during biotic stresses remain less defined. In this study, we investigated the biological function and regulatory mechanism of soybean (Glycine max) ERFVII transcription factors during soybean cyst nematode (Heterodera glycines Ichinohe) infection. We provide evidence that soybean cyst nematode infection induces responses at the infection sites similar to those induced by hypoxia, characterized by the stabilization of ERFVII proteins and increased expression of hypoxia-responsive genes. Hypoxia pretreatment of soybeans enhances their resistance to nematode infection. We demonstrate that ERFVII members GmRAP2.12 and GmRAP2.3 act as transcriptional activators to drive the expression of GmPR10-09g, a member of the PR10 gene family highly induced by soybean cyst nematode and positively impacting nematode resistance. Transgenic hairy root analysis of nematode infection for either GmRAP2.12 or N-end rule pathway components (GmATE or GmPRT6) indicates a positive role of ERFVIIs in soybean defense responses against cyst nematode. The results of our study emphasize the important functions of GmERFVIIs in strengthening soybean’s immune responses against cyst nematode by transcriptional activation of GmPR10.