Kelly Swarts

Comprehensive genotyping of the USA national maize inbred seed bank

BackgroundGenotyping by sequencing, a new low-cost, high-throughput sequencing technology was used to genotype 2,815 maize inbred accessions, preserved mostly at the National Plant Germplasm System in the USA. The collection includes inbred lines from breeding programs all over the world.ResultsThe method produced 681,257 single-nucleotide polymorphism (SNP) markers distributed across the entire genome, with the ability to detect rare alleles at high confidence levels. More than half of the SNPs in the collection are rare. Although most rare alleles have been incorporated into public temperate breeding programs, only a modest amount of the available diversity is present in the commercial germplasm. Analysis of genetic distances shows population stratification, including a small number of large clusters centered on key lines. Nevertheless, an average fixation index of 0.06 indicates moderate differentiation between the three major maize subpopulations. Linkage disequilibrium (LD) decays very rapidly, but the extent of LD is highly dependent on the particular group of germplasm and region of the genome. The utility of these data for performing genome-wide association studies was tested with two simply inherited traits and one complex trait. We identified trait associations at SNPs very close to known candidate genes for kernel color, sweet corn, and flowering time; however, results suggest that more SNPs are needed to better explore the genetic architecture of complex traits.ConclusionsThe genotypic information described here allows this publicly available panel to be exploited by researchers facing the challenges of sustainable agriculture through better knowledge of the nature of genetic diversity.

Novel Methods to Optimize Genotypic Imputation for Low-Coverage, Next-Generation Sequence Data in Crop Plants

Next‐generation sequencing technology such as genotyping‐by‐sequencing (GBS) made low‐cost, but often low‐coverage, whole‐genome sequencing widely available. Extensive inbreeding in crop plants provides an untapped, high quality source of phased haplotypes for imputing missing genotypes. We introduce Full‐Sib Family Haplotype Imputation (FSFHap), optimized for full‐sib populations, and a generalized method, Fast Inbred Line Library ImputatioN (FILLIN), to rapidly and accurately impute missing genotypes in GBS‐type data with ordered markers. FSFHap and FILLIN impute missing genotypes with high accuracy in GBS‐genotyped maize (Zea mays L.) inbred lines and breeding populations, while Beagle v. 4 is still preferable for diverse heterozygous populations. FILLIN and FSFHap are implemented in TASSEL 5.0.

A study of allelic diversity underlying flowering-time adaptation in maize landraces

Landraces (traditional varieties) of domesticated species preserve useful genetic variation, yet they remain untapped due to the genetic linkage between the few useful alleles and hundreds of undesirable alleles. We integrated two approaches to characterize the diversity of 4,471 maize landraces. First, we mapped genomic regions controlling latitudinal and altitudinal adaptation and identified 1,498 genes. Second, we used F-one association mapping (FOAM) to map the genes that control flowering time, across 22 environments, and identified 1,005 genes. In total, we found that 61.4% of the single-nucleotide polymorphisms (SNPs) associated with altitude were also associated with flowering time. More than half of the SNPs associated with altitude were within large structural variants (inversions, centromeres and pericentromeric regions). The combined mapping results indicate that although floral regulatory network genes contribute substantially to field variation, over 90% of the contributing genes probably have indirect effects. Our dual strategy can be used to harness the landrace diversity of plants and animals.

Independent Molecular Basis of Convergent Highland Adaptation in Maize

Convergent evolution is the independent evolution of similar traits in different species or lineages of the same species; this often is a result of adaptation to similar environments, a process referred to as convergent adaptation. We investigate here the molecular basis of convergent adaptation in maize to highland climates in Mesoamerica and South America, using genome-wide SNP data. Taking advantage of archaeological data on the arrival of maize to the highlands, we infer demographic models for both populations, identifying evidence of a strong bottleneck and rapid expansion in South America. We use these models to then identify loci showing an excess of differentiation as a means of identifying putative targets of natural selection and compare our results to expectations from recently developed theory on convergent adaptation. Consistent with predictions across a wide parameter space, we see limited evidence for convergent evolution at the nucleotide level in spite of strong similarities in overall phenotypes. Instead, we show that selection appears to have predominantly acted on standing genetic variation and that introgression from wild teosinte populations appears to have played a role in highland adaptation in Mexican maize.

Genomic estimation of complex traits reveals ancient maize adaptation to temperate North America

Estimating temperate adaptation in ancient maize Maize as a staple food crop in temperate North America required adaptation to a shorter growing season. On its first introduction in the southwestern United States ∼4000 years ago, maize was extensively grown in the lowlands. Cultivation in the temperate uplands did not occur for another 2000 years. Swarts et al. used ancient DNA data from 1900-year-old maize cobs found in a temperate cave in the southwestern United States and mapped the ancient flowering phenotype. The ancient maize samples were marginally adapted to temperate regions as a result of selection on standing variation. Science, this issue p. 512 Archaeological maize found in ancient turkey pens was adapted to temperate environments by 1900 years ago. By 4000 years ago, people had introduced maize to the southwestern United States; full agriculture was established quickly in the lowland deserts but delayed in the temperate highlands for 2000 years. We test if the earliest upland maize was adapted for early flowering, a characteristic of modern temperate maize. We sequenced fifteen 1900-year-old maize cobs from Turkey Pen Shelter in the temperate Southwest. Indirectly validated genomic models predicted that Turkey Pen maize was marginally adapted with respect to flowering, as well as short, tillering, and segregating for yellow kernel color. Temperate adaptation drove modern population differentiation and was selected in situ from ancient standing variation. Validated prediction of polygenic traits improves our understanding of ancient phenotypes and the dynamics of environmental adaptation.

Dysregulation of expression correlates with rare-allele burden and fitness loss in maize

Here we report a multi-tissue gene expression resource that represents the genotypic and phenotypic diversity of modern inbred maize, and includes transcriptomes in an average of 255 lines in seven tissues. We mapped expression quantitative trait loci and characterized the contribution of rare genetic variants to extremes in gene expression. Some of the new mutations that arise in the maize genome can be deleterious; although selection acts to keep deleterious variants rare, their complete removal is impeded by genetic linkage to favourable loci and by finite population size. Modern maize breeders have systematically reduced the effects of this constant mutational pressure through artificial selection and self-fertilization, which have exposed rare recessive variants in elite inbred lines. However, the ongoing effect of these rare alleles on modern inbred maize is unknown. By analysing this gene expression resource and exploiting the extreme diversity and rapid linkage disequilibrium decay of maize, we characterize the effect of rare alleles and evolutionary history on the regulation of expression. Rare alleles are associated with the dysregulation of expression, and we correlate this dysregulation to seed-weight fitness. We find enrichment of ancestral rare variants among expression quantitative trait loci mapped in modern inbred lines, which suggests that historic bottlenecks have shaped regulation. Our results suggest that one path for further genetic improvement in agricultural species lies in purging the rare deleterious variants that have been associated with crop fitness.

Corrigendum: A study of allelic diversity underlying flowering-time adaptation in maize landraces

Nat. Genet.; 10.1038/ng.3784; corrected online 20 February 2017 In the version of this article initially published online, the name of author Martha Willcox was misspelled as Martha Wilcox. The error has been corrected in the print, PDF and HTML versions of this article.

A large scale joint analysis of flowering time reveals independent temperate adaptations in maize

Modulating days to flowering is a key mechanism in plants for adapting to new environments, and variation in days to flowering drives population structure by limiting mating. To elucidate the genetic architecture of flowering across maize, a quantitative trait, we mapped flowering in five global populations, a diversity panel (Ames) and four half-sib mapping designs, Chinese (CNNAM), US (USNAM), and European Dent (EUNAM-Dent) and Flint (EUNAM-Flint). Using whole-genome projected SNPs, we tested for joint association using GWAS, resampling GWAS and two regional approaches; Regional Heritability Mapping (RHM) (1, 2) and a novel method, Boosted Regional Heritability Mapping (BRHM). Direct overlap in significant regions detected between populations and flowering candidate genes was limited, but whole-genome cross-population predictive abilities were ≤0.78. Poor predictive ability correlated with increased population differentiation (r = 0.41), unless the parents were broadly sampled from across the North American temperate-tropical germplasm gradient; uncorrected GWAS results from populations with broadly sampled parents were well predicted by temperate-tropical FSTs in machine learning. Machine learning between GWAS results also suggested shared architecture between the American panels and, more distantly, the European panels, but not the Chinese panel. Machine learning approaches can reconcile non-linear relationships, but the combined predictive ability of all of the populations did not significantly enhance prediction of physiological candidates. While the North American-European temperate adaption is well studied, this study suggest independent temperate adaptation evolved in the Chinese panel, most likely in China after 1500, a finding supported by differential gene ontology term enrichment between populations.

Identifying the diamond in the rough: a study of allelic diversity underlying flowering time adaptation in maize landraces

Landraces (traditional varieties) of crop species are a reservoir of useful genetic diversity, yet remain untapped due to the genetic linkage between the few useful alleles with hundreds of undesirable alleles1. We integrated two approaches to characterize the genetic diversity of over 3000 maize landraces from across the Americas. First, we mapped the genomic regions controlling latitudinal and altitudinal adaptation, identifying 1498 genes. Second, we developed and used F-One Association Mapping (FOAM) to directly map genes controlling flowering time across 22 environments, identifying 1,005 genes. In total 65% of the SNPs associated with altitude were also associated with flowering time. In particular, we observed many of the significant SNPs were contained in large structural variants (inversions, centromeres, and pericentromeric regions): 29.4% for flowering time, 58.4% for altitude and 13.1% for latitude. The combined mapping results indicate that while floral regulatory network genes contribute substantially to field variation, over 90% of contributing genes likely have indirect effects. Our strategy can be used to harness the diversity of maize and other plant and animal species.