Absent in the wild, Tahitian vanilla (V. tahitensis) is a gourmet spice restricted in distribution to cultivated and feral stands in French Polynesia and Papua New Guinea. Its origins have been elusive. Our objective was to test the purported hybrid derivation and parentage of V. tahitensis from aromatic, neotropical progenitors. Nucleotide sequences from V. tahitensis and neotropical Vanilla were assayed for phylogenetic relatedness in two independently inherited genomic regions, the nuclear ITS region, and the trnH-psbA noncoding region of chloroplast DNA. As predicted to occur for early generation hybrids, placement of V. tahitensis was nonconcordant. All V. tahitensis clustered with V. planifolia from analysis of cpDNA sequences, suggesting V. planifolia as the maternal genome contributor. Phylogenetic reconstruction of ITS sequences showed that most V. tahitensis nested incongruently with V. odorata, but others remained sister to V. planifolia. Recovery of ITS clones in V. tahitensis related to both V. planifolia and V. odorata also supports its biphyletic origin from these two taxa. We interpret the high percentage (95%) of additive polymorphic sites in V. tahitensis relative to its parents as indication of a recent, and probably human-mediated, evolutionary origin.

DNA remodeling during endoreplication appears to be a strong developmental characteristic in orchids. In this study, we analyzed DNA content and nuclei in 41 species of orchids to further map the genome evolution in this plant family. We demonstrate that the DNA remodeling observed in 36 out of 41 orchids studied corresponds to strict partial endoreplication. Such process is developmentally regulated in each wild species studied. Cytometry data analyses allowed us to propose a model where nuclear states 2C, 4E, 8E, etc. form a series comprising a fixed proportion, the euploid genome 2C, plus 2–32 additional copies of a complementary part of the genome. The fixed proportion ranged from 89% of the genome in Vanilla mexicana down to 19% in V. pompona, the lowest value for all 148 orchids reported. Insterspecific hybridization did not suppress this phenomenon. Interestingly, this process was not observed in mass-produced epiphytes. Nucleolar volumes grow with the number of endocopies present, coherent with high transcription activity in endoreplicated nuclei. Our analyses suggest species-specific chromatin rearrangement. Towards understanding endoreplication, V. planifolia constitutes a tractable system for isolating the genomic sequences that confer an advantage via endoreplication from those that apparently suffice at diploid level.

Genome irregularities may be transmitted not only during vegetative propagation but also by sexual reproduction in Vanilla. However, there must be a complex regulation of genome size and organization between the aneuploidy in somatic tissues and subsequently euploid gametic tissue. This is a novel example of polysomaty with developmentally regulated partial endoreplication.

The first vanilla genetic linkage map was constructed by analyzing the progeny of an interspecific cross between Vanilla xtahitensis J. W. Moore (pro sp.) and Vanilla pompona Schiede. The two-way pseudotestcross mapping strategy was used and a total of 225 amplified fragment length polymorphism (AFLP) markers were mapped on 18 linkage groups covering 1035.85 cM. Thirteen tahitian vanilla morphotypes, one Vanilla planifolia Andrews and recent hybrids were compared by measuring seven morphological traits and by genotyping, with 539 AFLP fragments. The morphotypes studied showed relatively homogenous stem traits but differed in their bean and leaf traits as in their AFLP pattern. Genetic variability and AFLP genotyping comparison suggest a diversification in French Polynesia based on sexual reproduction and are consistent with the hypothesis of a single introduction event. These results are the first step for vanilla breeding program and will be also useful for tahitian vanilla resource preservation.

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.