An antiviral jacalin‐like lectin gene contributes to nonhost resistance and host determination of potexviruses among Brassicaceae

Plant resistance influences the host range of pathogens; however, the mechanism driving this influence remains poorly understood. Brassicaceae species are not natural hosts of potexviruses, for reasons that have not yet been determined. This study investigated the molecular basis of nonhost resistance (NHR) to potexviruses in the Brassicaceae, focusing on the non-nucleotide-binding leucine-rich repeat (NLR) resistance gene JACALIN-TYPE LECTIN REQUIRED FOR POTEXVIRUS RESISTANCE1 (JAX1). We found that JAX1 is a Brassicaceae-specific conserved gene that has been lost or pseudogenized in some species, and duplicated in others. Most JAX1 orthologs from diverse Brassicaceae species effectively inhibit plantago asiatica mosaic virus (PlAMV) accumulation, indicating that antiviral activity is conserved among the Brassicaceae. However, we demonstrated that some Brassicaceae plants in which JAX1 expression was not detected allow local or systemic viral infection. Quadruple knockout of JAX1 genes via gene editing in Sisymbrium irio, a nonhost of PlAMV, led to loss of resistance and potexvirus susceptibility in this species. These results clearly indicate that JAX1 represents one layer of multi-layer NHR against potexviruses in the Brassicaceae, shedding light on the pivotal role of non-NLR antiviral resistance in shaping the host range of these plant viruses.