Soybean resistance locus Rhg1 confers resistance to multiple cyst nematodes in diverse plant species

Authors: BUTLER, KATELYN - University Of Wisconsin; CHEN, SHIYAN - Cornell University; SMITH, JOHN - University Of Wisconsin; Wang, Xiaohong; BENT, ANDREW - University Of Wisconsin

Submitted to: Phytopathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/23/2019
Publication Date: 11/4/2019
Citation: Butler, K.J., Chen, S., Smith, J.M., Wang, X., Bent, A.F. 2019. Soybean resistance locus Rhg1 confers resistance to multiple cyst nematodes in diverse plant species. Phytopathology. https://doi.org/10.1094/PHYTO-07-19-0225-R.
DOI: https://doi.org/10.1094/PHYTO-07-19-0225-R

Interpretive Summary: Plant-parasitic cyst nematodes are agriculturally important pests, causing substantial crop losses annually. Using host resistance is the most economical and environmentally sound method for nematode control. Rhg1 (Resistance to Heterodera glycines 1), a resistance locus in soybean, is the most popular resistance source used against the soybean cyst nematode (Heterodera glycines). In this study, we studied if the Rhg1 resistance locus could function in different plant species and confer resistance to their respective cyst nematode species. To this end, we generated transgenic Arabidopsis and potato lines overexpressing Rhg1 and tested them for infection with the beet cyst nematode (BCN; Heterodera schachtii) and potato cyst nematodes (PCN; Globodera rostochiensis and G. pallida), respectively. BCN can infect a wide range of crops including sugar beet and many cruciferous vegetables as well as Arabidopsis and PCN are the most devastating pests of potatoes. Excitingly, transgenic Arabidopsis and potato lines expressing Rhg1 showed enhanced resistance to BCN and PCN, respectively. The results demonstrated that soybean Rhg1 can function across plant species, suggesting a utility of this resistance locus in developing engineered nematode resistance in other crops.

Technical Abstract: Cyst nematodes consistently threaten agricultural production, causing billions of dollars of loss globally. The Rhg1 (Resistance to Heterodera glycines 1) resistance locus of soybean (Glycine max) is the most popular resistance source used against soybean cyst nematode (Heterodera glycines). We investigated if this resistance locus could function in different plant families, conferring resistance to their respective cyst nematode parasites. Transgenic Arabidopsis thaliana and potato (Solanum tuberosum) plants were generated that express the three soybean genes of the complex Rhg1 locus. The recipient Brassicaceae and Solanaceae plant species exhibited elevated resistance, respectively, to Heterodera schachtii and to Globodera rostochiensis and G. pallida. The transgenic plants were subjected to additional molecular and phenotypic characterization. While root length was slightly reduced in Arabidopsis Rhg1+ lines, equal numbers of nematodes penetrated wild-type and Rhg1+ roots and resistance was manifested later in nematode development. Greenhouse studies showed that the overall potato tuber weight per plant was moderately reduced in Rhg1-expressing lines in comparison with control lines. Native Arabidopsis and potato alpha-SNAPs (Soluble NSF [N-ethylamine sensitive factor] attachment protein) were shown to be able to compensate for toxic soybean Rhg1 alpha-SNAP proteins, but some negative consequences of heterologous Rhg1 expression remained, which may be explained by the absence of other Rhg1-associated factors from the soybean genome. The multi-species efficacy of soybean Rhg1 demonstrates that the encoded mechanisms can function across plant families and against multiple genera of the cyst nematode subfamily Heteroderidae.