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Genome-wide footprints in the carob tree (Ceratonia siliqua) unveil a new domestication pattern of a fruit tree in the Mediterranean

Baumel A., Feliner G.N., Médail F., La Malfa S., Di Guardo M., Bou Dagher Kharrat M., Lakhal-Mirleau F., Frelon V., Ouahmane L., Diadema K., Sanguin H., Viruel J.. 2022. Molecular Ecology, 31 (15) : p. 4095-4111.

DOI: 10.1111/mec.16563

Intense research efforts over the last two decades renewed our understanding of plant phylogeography and domestication in the Mediterranean basin. We aim to investigate the evolutionary history and the origin of domestication of the carob tree (Ceratonia siliqua), which has been cultivated for millennia for food and fodder. We used >1000 microsatellite genotypes to delimit seven carob evolutionary units (CEUs). We investigated genome-wide diversity and evolutionary patterns of the CEUs with 3557 SNPs generated by restriction-site associated DNA sequencing (RADseq). To address the complex wild vs. cultivated status of sampled trees, we classified 56 sampled populations across the Mediterranean basin as wild, semi-natural or cultivated. Nuclear and cytoplasmic loci were identified from RADseq data and separated for analyses. Phylogenetic analyses of these genomic-wide data allowed us to resolve west-to-east expansions from a single long-term refugium likely located in the foothills of the High Atlas Mountains near the Atlantic coast. Our findings support multiple origins of domestication with a low impact on the genetic diversity at range wide level. The carob was mostly domesticated from locally selected wild genotypes and scattered long-distance westward dispersals of domesticated varieties by humans, concomitant with major historical migrations by Romans, Greeks and Arabs. Ex-situ efforts to preserve carob genetic resources should prioritize accessions from both western and eastern populations, with emphasis on the most differentiated CEUs situated in Southwest Morocco, South Spain and Eastern Mediterranean. Our study highlights the relevance of wild and seminatural habitats in the conservation of genetic resources for cultivated trees.

Mots-clés : domestication des plantes; génome; ceratonia siliqua; biogéographie; variation génétique; microsatellite; phytogénétique; ressource génétique végétale; région méditerranéenne

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