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

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.