Brandenburg, Jean-Tristan, Mary-Huard, Tristan, Rigaill, Guillem, Hearne, Sarah J., Corti, Hélène, Joets, Johann, Vitte, Clémentine, Charcosset, Alain, Nicolas, Stéphane D., Tenaillon, Maud I., Génétique Quantitative et Evolution - Le Moulon (Génétique Végétale) (GQE-Le Moulon), Institut National de la Recherche Agronomique (INRA)-Université Paris-Sud - Paris 11 (UP11)-AgroParisTech-Centre National de la Recherche Scientifique (CNRS), AgroParisTech, Université Paris Sud (Paris 11), Université Paris-Saclay, Centre National de la Recherche Scientifique (CNRS), Mathématiques et Informatique Appliquées (MIA-Paris), AgroParisTech-Institut National de la Recherche Agronomique (INRA), Institut des Sciences des Plantes de Paris-Saclay (IPS2 (UMR_9213 / UMR_1403)), Institut National de la Recherche Agronomique (INRA)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS)-Université Paris Diderot - Paris 7 (UPD7)-Université Paris-Saclay-Université Paris-Sud - Paris 11 (UP11), International Maize and Wheat Improvement Centre, CIMMYT, French National Research Agency (ANR) [ANR-10-BTBR-03], Investissementsd'Avenir'Programme, the LabEx, Centre National de la Recherche Scientifique (CNRS)-AgroParisTech-Université Paris-Sud - Paris 11 (UP11)-Institut National de la Recherche Agronomique (INRA), Institut National de la Recherche Agronomique (INRA)-Université Paris-Sud - Paris 11 (UP11)-Université Paris Diderot - Paris 7 (UPD7)-Université d'Évry-Val-d'Essonne (UEVE)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Institut National de la Recherche Agronomique (INRA)-Université Paris-Sud - Paris 11 (UP11)-Université Paris Diderot - Paris 7 (UPD7)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS), International Maize and Wheat Improvement Center (CIMMYT), Consultative Group on International Agricultural Research [CGIAR] (CGIAR)-Consultative Group on International Agricultural Research [CGIAR] (CGIAR), Génétique Quantitative et Evolution - Le Moulon (Génétique Végétale) ( GQE-Le Moulon ), Institut National de la Recherche Agronomique ( INRA ) -Université Paris-Sud - Paris 11 ( UP11 ) -AgroParisTech-Centre National de la Recherche Scientifique ( CNRS ), Centre National de la Recherche Scientifique ( CNRS ), UMR 518, UMR 1403 Institut des Sciences des Plantes de Paris Saclay, Institut National de la Recherche Agronomique ( INRA ) -Université Paris Diderot - Paris 7 ( UPD7 ), and Institut National de la Recherche Agronomique (INRA)-AgroParisTech
Through the local selection of landraces, humans have guided the adaptation of crops to a vast range of climatic and ecological conditions. This is particularly true of maize, which was domesticated in a restricted area of Mexico but now displays one of the broadest cultivated ranges worldwide. Here, we sequenced 67 genomes with an average sequencing depth of 18x to document routes of introduction, admixture and selective history of European maize and its American counterparts. To avoid the confounding effects of recent breeding, we targeted germplasm (lines) directly derived from landraces. Among our lines, we discovered 22,294,769 SNPs and between 0.9% to 4.1% residual heterozygosity. Using a segmentation method, we identified 6,978 segments of unexpectedly high rate of heterozygosity. These segments point to genes potentially involved in inbreeding depression, and to a lesser extent to the presence of structural variants. Genetic structuring and inferences of historical splits revealed 5 genetic groups and two independent European introductions, with modest bottleneck signatures. Our results further revealed admixtures between distinct sources that have contributed to the establishment of 3 groups at intermediate latitudes in North America and Europe. We combined differentiation- and diversity-based statistics to identify both genes and gene networks displaying strong signals of selection. These include genes/gene networks involved in flowering time, drought and cold tolerance, plant defense and starch properties. Overall, our results provide novel insights into the evolutionary history of European maize and highlight a major role of admixture in environmental adaptation, paralleling recent findings in humans., Author summary The spread of a species outside its native range depends on its ability to face new environmental challenges. Despite a loss of diversity associated with recurrent introductions, domesticated species offer excellent examples of rapid expansion and adaptation to new climatic and ecological conditions. This is exemplified in maize, which was first domesticated in a restricted area of Central Mexico but now displays one of the broadest cultivated ranges of all crops. Here, we focused on the largely overlooked history of European maize, which was introduced from American sources. We sequenced 67 genomes from both continents. The data suggest two independent European introductions and also the admixed origin of three groups: maize from the US Corn Belt, European Flints and Italian material. We found modest genetic footprints of bottlenecks from European introduction. We detected signs of past selection at genes and gene pathways involved in adaptation to abiotic (drought/cold) and biotic (pathogens/herbivores) challenges. Our results provide novel insights into the evolutionary history of European maize and highlight a major role of admixture in environmental adaptation.