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The origins and adaptation of European potatoes reconstructed from historical genomes

Abstract

Potato, one of the most important staple crops, originates from the highlands of the equatorial Andes. There, potatoes propagate vegetatively via tubers under short days, constant throughout the year. After their introduction to Europe in the sixteenth century, potatoes adapted to a shorter growing season and to tuber formation under long days. Here, we traced the demographic and adaptive history of potato introduction to Europe. To this end, we sequenced 88 individuals that comprise landraces, modern cultivars and historical herbarium samples, including specimens collected by Darwin during the voyage of the Beagle. Our findings show that European potatoes collected during the period 1650–1750 were closely related to Andean landraces. After their introduction to Europe, potatoes admixed with Chilean genotypes. We identified candidate genes putatively involved in long-day pre-adaptation, and showed that the 1650–1750 European individuals were not long-day adapted through previously described allelic variants of the CYCLING DOF FACTOR1 gene. Such allelic variants were detected in Europe during the nineteenth century. Our study highlights the power of combining contemporary and historical genomes to understand the complex evolutionary history of crop adaptation to new environments.

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Data availability

Sequencing data generated in this study are available in the European Nucleotide Archive (ENA) under project Nos. PRJEB31013 and PRJEB31171 for UDG-treated and non-UDG-treated libraries, respectively.

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Acknowledgements

We thank D. Weigel for initial discussions during the conception of this project; B. Glover and C. Bartram (Cambridge University Herbarium), M. Graniszewska and H. Leśniewska (University of Warsaw) for granting access to historic herbarium samples; J. Krause (MPI for the Science of Human History), V. Schuenemann and E. Reiter (University of Tuebingen) for access to clean-room facilities and technical support; M. Neumann and S. Latorre for laboratory assistance; L. Shannon (University of Minnesota) for input on potato diversity; C. Bachem, H. van Eck and J. Willemsen (Wageningen University) for input on array design; N. Arciniegas (National University of Colombia) for collection assistance; T. Karasov, M. Zaidem and members of the Burbano laboratory for comments on the manuscript; and M. Purugganan (New York University) for supporting R. Gutaker during the final stages of the project. We thank the Spanish National Research Council (CSIC) and the Ministry of Economy and Competitiveness for financing the project No. CGL 2010–19747, which facilitated the visits to Colombia and access to the collections of the Real Jardin Botanico Herbarium (MA). This study was funded by the Max Planck Society and its Presidential Innovation Fund (H.A.B).

Author information

R.M.G and H.A.B. conceived and designed the study with input from S.P. D.E., N.L.A., S.K., J.L.F.-A. and S.P curated, identified, pre-selected and contributed contemporary and historic potato samples. R.M.G carried out DNA extractions, hybridization captures and library preparations. R.M.G. performed the bioinformatic processing of sequencing data with input from C.L.W and H.A.B. C.L.W. carried out ploidy estimation of samples. R.M.G. performed the phylogeographic and population genomics analyses with input from H.A.B. R.M.G., S.P. and H.A.B. contributed to the interpretation of the data. R.M.G and H.A.B wrote the manuscript with input from all authors. All authors read and approved the manuscript.

Correspondence to Hernán A. Burbano.

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The authors declare no competing interests.

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Supplementary information

Supplementary Information

Supplementary Methods and Supplementary Figs. 1–15

Reporting Summary

Supplementary Tables 1

Provenance and meta-information of historical samples.

Supplementary Tables 2

Provenance and meta-information of modern samples.

Supplementary Tables 3

Sequenced loci nuclear.

Supplementary Tables 4

Characteristics of sequenced libraries.

Supplementary Tables 5

Read support for different StCDF1 alleles.

Supplementary Tables 6

Loss of heterozygosity and Tajima’s D-statistics.

Supplementary Tables 7

Description: evaluation of the 100 best admixture graph models.

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Fig. 1: Relationship of the oldest European potatoes (collected 1650–1750) to historical and contemporary South American potatoes.
Fig. 2: Genetic differentiation and admixture of potato populations in Europe.
Fig. 3: Geographic and temporal distribution of stabilizing insertions in the StCDF1 gene.
Fig. 4: Potential signatures of selection in genes linked to photoperiod.