Natural Allelic Variations in IbCHYR1–IbZnFR Complex Regulate Fusarium Root Rot Resistance in Sweet Potato

Abstract Sweet potato ( Ipomoea batatas ) is a globally important autohexaploid root and tuber crop. Fusarium root rot threatens its entire growth, harvest, and storage period, thereby reducing yield and quality. Therefore, a deeper understanding of Fusarium pathogenicity and sweet potato defense is urgently required. Here, two single nucleotide polymorphisms are identified within the promoter region of the I. batatas CHY zinc‐finger and ring protein1 ( IbCHYR1 ) gene that encode an E3 ubiquitin ligase linked to root rot resistance. In susceptible varieties, the high dosage allele Pro :: IbCHYR1 Hap1 leads to increased expression of IbCHYR1 . Overexpression of IbCHYR1 increases susceptibility to root rot and Fusarium wilt. IbCHYR1 interacts with the I. batatas CCCH‐type zinc‐finger protein ( IbZnFR ) to promote its degradation. IbZnFR confers resistance to root rot and Fusarium wilt and improves yield by more than 10%. The high dosage Pro :: IbZnFR Hap2 allele is associated with resistance to root rot disease. Moreover, FfRlpA2 , a conserved Fusarium effector, is identified as a protease inhibitor that stabilizes and hijacks IbCHYR1 to degrade IbZnFR , thereby inhibiting multiple defense pathways. These findings provide insights into Fusarium pathogenicity and a genetic basis for root rot research and improvement of disease‐resistant sweet potato varieties.