A highly diversified NLR cluster in melon contains homologs that confer powdery mildew and aphid resistance

Podosphaera xanthii is the main causal agent of powdery mildew (PM) on Cucurbitaceae. In Cucumis melo, the Pm-w resistance gene, which confers resistance to P. xanthii, is located on chromosome 5 in a cluster of nucleotide-binding leucine-rich repeat receptors (NLRs). We used positional cloning and transgenesis, to isolate the Pm-wWMR 29 gene encoding a coiled-coil NLR (CC-NLR). Pm-wWMR 29 conferred high level of resistance to race 1 of PM and intermediate level of resistance to race 3 of PM. Pm-wWMR 29 turned out to be a homolog of the Aphis gossypii resistance gene Vat-1PI 161375. We confirmed that Pm-wWMR 29 did not confer resistance to aphids, while Vat-1PI 161375 did not confer resistance to PM. We showed that both homologs were included in a highly diversified cluster of NLRs, the Vat cluster. Specific Vat-1PI 161375 and Pm-wWMR 29 markers were present in 10% to 13% of 678 accessions representative of wild and cultivated melon types worldwide. Phylogenic reconstruction of 34 protein homologs of Vat-1PI 161375 and Pm-wWMR 29 identified in 24 melon accessions revealed an ancestor with four R65aa-a specific motif in the LRR domain, evolved towards aphid and virus resistance, while an ancestor with five R65aa evolved towards PM resistance. The complexity of the cluster comprising the Vat/Pm-w genes and its diversity in melon suggest that Vat homologs may contribute to the recognition of a broad range of yet to be identified pests and pathogens.