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.

Aphis gossypii/Aphis frangulae collected worldwide: Microsatellite markers data and genetic cluster assignment.

Aphis gossypii is a cosmopolitan aphid species able to colonize hundreds of plant species from various families [1]. It causes serious damage to a wide range of crops and it is considered a major pest of cucurbits and cotton [2]. It reproduces clonally, by obligate parthenogenesis, on secondary hosts present throughout the year in the intertropical area. At higher latitude, some lineages clonally overwinter but part of the population may have a sexual reproduction in autumn on primary host such as Hibiscus syriacus, to generate cold resistant overwintering eggs [3]. It is highly challenging to distinguish A. gossypii from its sister species Aphis frangulae as both are colonizing solanaceous plants as secondary hosts but the primary host of A. frangulae is Frangula alnus[4]. This paper describes a worldwide collection of both species from December 1989 to September 2019. Aphids were collected individually on plants (19 families) or in traps. The location, the morph type and the botanical family of the host plant were registered. DNA was extracted from each aphid and amplified at 8 microsatellite loci [5]. Amplicons were analysed with ABI technology and their size was defined with Genemapper software. We named each unique combination of alleles, called a multilocus genotype (MLG), and then each individual was given its MLG. The matrix of alleles of all MLGs was run for a Bayesian analysis to describe the genetic structure of the diversity collected and then each MLG had a probability to belong to a genetic group [6,7]. Probability of assignation to each genetic group revealed by the analysis was reported to each individual according to its MLG. This dataset can be used to analyze host plant specificities in A. gossypii, genetic diversity in A. gossypii and relative incidence of variants in diverse geographical regions, admixture between two sister species (Aphis gossypii and Aphis frangulae).

Insight into the durability of plant resistance to aphids from a demo-genetic study of Aphis gossypii in melon crops.

Resistance breakdown has been observed following the deployment of plant cultivars resistant to pests. Assessing the durability of a resistance requires long-term experiments at least at a regional scale. We collected such data for melon resistance conferred by the Vat gene cluster to melon aphids. We examined landscape-level populations of Aphis gossypii collected in 2004-2015, from melon-producing regions with and without the deployment of Vat resistance and with different climates. We conducted demo-genetic analyses of the aphid populations on Vat and non-Vat plants during the cropping seasons. The Vat resistance decreased the density of aphid populations in all areas and changed the genetic structure and composition of these populations. Two bottlenecks were identified in the dynamics of adapted clones, due to the low levels of production of dispersal morphs and winter extinction. Our results suggest that (i) Vat resistance will not be durable in the Lesser Antilles, where no bottleneck affected the dynamics of adapted clones, (ii) Vat resistance will be durable in south-west France, where both bottlenecks affected the dynamics of adapted clones and (iii) Vat resistance will be less durable in south-east France, where only one of the two bottlenecks was observed.