WI12 (Rhg1) interacts with DELLAs and mediates soybean cyst nematode resistance through hormone pathways

The soybean cyst nematode (SCN) is one of the most important causes of soybean yield loss. The major source of genetic resistance to SCN is the Rhg1 repeat, a tandem copy number polymorphism of three genes. The roles of these genes are only partially understood. Moreover, nematode populations virulent on Rhg1‐carrying soybeans are becoming more common, increasing the need to understand the most successful genetic resistance mechanism. Here, we show that a Rhg1‐locus gene (Glyma.18G02270) encoding a wound‐inducible protein (WI12 (Rhg1) ) is needed for SCN resistance. Furthermore, knockout of WI12(Rhg1) reduces the expression of DELLA18, and the expression of WI12(Rhg1) is itself induced by either JA, SA or GA. The content of the defence hormone SA is significantly lower whilst GA(12) and GA(53) are increased in WI12(Rhg1) knockout roots compared with unedited hairy roots. We find that WI12 (Rhg1) directly interacts with DELLA18 (Glyma.18G040000) in yeast and plants and that double knockout of DELLA18 and its homeolog DELLA11 (Glyma.11G216500) significantly reduces SCN resistance and alters the root morphology. As DELLA proteins are implicated in hormone signalling, we explored the content of defence hormones (JA and SA) in DELLA knockout and unedited roots, finding reduced levels of JA and SA after the knockout of DELLA. Additionally, the treatment of DELLA‐knockout roots with JA or SA rescues SCN resistance lost by the knockout. Meanwhile, the SCN resistance of unedited roots decreases after the treatment with GA, but increases with JA or SA. Our findings highlight the critical roles of WI12 (Rhg1) and DELLA proteins in SCN resistance through interconnection with hormone signalling.