Beet cyst nematode HsSNARE1 interacts with both AtSNAP2 and AtPR1 and promotes disease in Arabidopsis

[Display omitted] •A t-SNARE domain-containing effector HsSNARE1 was identified from beet cyst nematode (BCN).•Protein structure modeling analysis found that three mutations (E141D, A143T and −148S) altered regional structure of HsSNARE1 from random coils to α-helixes.•Expression of HsSNARE1 significantly enhanced while expression of its highly homologous soybean cyst nematode (SCN) HgSNARE1 and its mutant HsSNARE1-M1, both of which carry those above-mentioned three mutations, remarkably suppressed BCN susceptibility of Arabidopsis.•HsSNARE1 promotes cyst nematode disease by interaction with both AtSNAP2 and AtPR1 via its t-SNARE domain and N-terminal uncharacterized fragment, respectively, and significant suppression of both AtSHMT4 and AtPR1.•This work pinpoints a new molecular mode of action of the t-SNARE-domain containing cyst nematode effectors. Plant parasitic cyst nematodes secrete a number of effectors into hosts to initiate formation of syncytia and infection causing huge yield losses. The identified cyst nematode effectors are still limited, and the cyst nematode effectors-involved interaction mechanisms between cyst nematodes and plants remain largely unknown. The t-SNARE domain-containing effector in beet cyst nematode (BCN) was identified by In situ hybridization and immunohistochemistry analyses. The mutant of effector gene was designed by protein structure modeling analysis. The functions of effector gene and its mutant were analyzed by genetic transformation in Arabidopsis and infection by BCN. The protein–protein interaction was analyzed by yeast two hybrid, BiFC and pulldown assays. Gene expression was assayed by quantitative real-time PCR. A t-SNARE domain-containing BCN HsSNARE1 was identified as an effector, and its mutant HsSNARE1-M1 carrying three mutations (E141D, A143T and −148S) that altered regional structure from random coils to α-helixes was designed and constructed. Transgenic analyses indicated that expression of HsSNARE1 significantly enhanced while expression of HsSNARE1-M1 and highly homologous HgSNARE1 remarkably suppressed BCN susceptibility of Arabidopsis. HsSNARE1 interacted with AtSNAP2 and AtPR1 via its t-SNARE domain and N-terminal, respectively, while HsSNARE1-M1/HgSNARE1 could not interact with AtPR1 but bound AtSNAP2. AtSNAP2, AtSHMT4 and AtPR1 interacted pairwise, but neither HsSNARE1 nor HsSNARE1-M1/HgSNARE1 could interact with AtSHMT4. Expression of HsSNARE1 significantly suppressed while expression of HsSNAR