Abstract

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.

Highlights

  • Expansion of species to conditions that differ from their native range depends on their abilities to adapt to new environments

  • Such lines are less heterozygous than landraces and more amenable for high-throughput sequencing (HTS) genotype calls

  • On chromosome 6, for example, we found a segment of extended heterozygosity bearing 37 genes (S11A Fig), 6 of which are reported as part of the highest read depth variants in maize [20], signaling a structural variant recently confirmed by PCR assays in a collection of lines [39]

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Summary

Introduction

Expansion of species to conditions that differ from their native range depends on their abilities to adapt to new environments. Despite loss of diversity associated with population bottlenecks during their domestication [1], domesticated species offer repeated examples of shifts in geographic range. Niche modeling of primitive maize landraces and cotton cultivars has demonstrated that their range rapidly exceeds that of their wild relatives [3,4]. Such rapid expansion is facilitated along east-west axes sharing more similar day-length characteristics and climates than along north-south axes [2]. Data suggest that the evolution of vernalization or photoperiod-neutral requirements has delayed expansion of wheat and barley to Northern latitudes by hundreds of years [5]

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