A natural variation in rice susceptibility factor Rsf1 confers resistance to root-knot nematode

Rice root-knot nematode (RRKN, Meloidogyne graminicola) is a destructive nematodes threatening global rice production. Few RRKN-resistant resources have been reported and their natural variations remain largely unknown. Here, we identify RRKN susceptibility factor 1 (Rsf1), encoding a cysteine-rich protein, via Genome-Wide Association Study (GWAS), multi-omics analysis, and functional validation. A natural variation in the TATA-box of OsRsf1 is observed, wherein RRKN-susceptible rice accessions contain haplotype (Hap) A while resistant accessions contain HapG. OsRsf1 with HapA is highly expressed and induced by RRKN infection, while HapG OsRsf1 shows low expression, conferring enhanced RRKN resistance. We further demonstrate that transcription factor Myb44 promotes OsRsf1 expression. Knockouts of OsRsf1 in rice and its ortholog AtRsf1 in Arabidopsis significantly enhanced nematode resistance, indicating that functional conservation. Mutations in OsRsf1 trigger a general defence response during RRKN infection. Our finding reveals a conserved Rsf1-mediated susceptibility mechanism underlying RRKN infection and provides a promising target for breeding nematode-resistant crops.