The cyst nematode resistance gene Hs4 from a wild relative of sugar beet confers resistance in an unrelated species

Abstract Plant-parasitic nematodes are major global pests in important crops. The beet cyst nematode (BCN, Heterodera schachtii ) is the most severe pest in sugar beet ( Beta vulgaris L.) production. It induces a specific feeding site within the roots, known as a syncytium. The Hs4 gene from Patellifolia procumbens , a distant relative of sugar beet, confers complete BCN resistance in beet. It encodes an endoplasmic reticulum (ER)-bound rhomboid protease. We expressed Hs4 in the unrelated species Arabidopsis thaliana . Transgenic lines exhibited BCN resistance in correlation with the Hs4 expression level. Histological analysis identified initial syncytia also in resistant plants. The ultrastructural analysis revealed an abundance of small ER-derived vesicles in syncytia of susceptible plants. In contrast, in resistant plants, ER membranes formed compact membrane aggregations. In line with the highest Hs4 expression, syncytia were destroyed by necrosis. Our observations are consistent with previous studies on beet roots, underscoring the ER's crucial role in nematode infection. In Arabidopsis, as in beet, the expression of Hs4 can mediate the collapse of the nematode feeding site. Our study also demonstrates that Hs4 has the potential to provide cyst nematode resistance to distantly related crops.