The Vanilla genus is a complex taxonomic group characterized by a vegetative reproduction mode combined with intra- and inter-specific hybridizations, and polyploidy events. These factors strongly impact the diversification of the genus and complicate the delimitation of taxa. Among the hundred Vanilla species, Vanilla planifolia Jacks. ex Andrews and Vanilla × tahitensis J. W. Moore are the main cultivated aromatic species. We applied Genotyping-by-Sequencing to explore the genetic diversity of these two cultivated vanilla species, seven closely related species and nineteen interspecific hybrids. The inter- and intra-specific relationships of 133 vanilla accessions were examined based on 2004 filtered SNPs. Our results showed a strong genetic structuring between the nine species studied, with wild species showing much lower heterozygosity levels than cultivated ones. Moreover, using Bayesian clustering analyses, the kinship of several hybrids could be verified. We evidenced in particular that Vanilla sotoarenasii and Vanilla odorata C.Presl may be the parental species of V. x tahitensis. The analysis of 1129 SNPs for 84 V. planifolia accessions showed a clear genetic demarcation between the vegetatively propagated traditional vanilla cultivars compared to the accessions derived from sexual reproduction, and a higher genetic diversity and lower heterozygosity of the latter (Ho = 0.206) compared to the former (Ho = 0.362). Our data are consistent with a single-step domestication for V. planifolia in accordance with the recent history of its cultivation. It also opens avenues to breed new V. planifolia varieties adapted to biotic and abiotic constraints and to reduce mutational load induced by clonal propagation.

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Fusarium oxysporum f. sp radicis-vanillae (Forv), the causal agent of Root and Stem Rot disease, is the main pathogen affecting vanilla production. Sources of resistance have been reported in Vanilla planifolia G. Jackson ex Andrews, the main cultivated vanilla species. Here we developed the first high-density genetic map in this species with 1,804 GBS-generated single nucleotide polymorphism (SNP) markers using 125 selfed progenies of the CR0040 traditional vanilla cultivar. Sixteen linkage groups (LG) were successfully constructed, with a mean of 113 SNPs and an average length of 207 cM per LG. The map had a high density with an average of 5.45 SNP every 10 cM and an average distance of 1.85 cM between adjacent markers. The first 3 LG were aligned against the first assembled chromosome of CR0040 and the other 13 LG were correctly associated with the other 13 assembled chromosomes. The population was challenged with the highly pathogenic Forv strain Fo072 using the root-dip inoculation method. Five traits were mapped and 20 QTLs were associated with resistance to Fo072. Among genes retrieved in the CR0040 physical regions associated with QTLs, genes potentially involved in biotic resistance mechanisms have been highlighted, coding for kinases, E3 ubiquitin ligases, pentatricopeptide repeat-containing proteins, and one leucine-rich repeat receptor underlying the qFo72_08.1 QTL. This study should provide useful resources for marker-assisted selection in V. planifolia.