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

A Corrigendum to this article was published on 26 May 2017

This article has been updated

Abstract

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 alleles1. 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.

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Figure 1: Experimental design.
Figure 2: Geographic coordinates of original sampling sites of landrace accessions.
Figure 3: Minor allele frequency distributions.
Figure 4: Significance for flowering time, and overlap between flowering time and latitude- and altitude-associated SNPs.
Figure 5: Flowering-time pathway, showing the genes involved in flowering time at the leaf and shoot apical meristem (SAM).

Change history

  • 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.

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Acknowledgements

J.A.R.N., M.W., J.B., S.T., E.P., A.T., H.V.D., V.V., A.O., A.E.B., N.O.G.M., I.O.-M., F.S.V., A.G.E., G.A., P.W. and S.H. were supported by La Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación (SAGARPA), Mexico under the MasAgro (Sustainable Modernization of Traditional Agriculture) initiative. J.A.R.N., C.R., K.S. and E.S.B. were supported by the US National Science Foundation (grant no. 1238014 and 0922493), and the USDA–ARS. We would like to thank ICAMEX and DuPont Pioneer Mexico for assistance in establishing the phenotypic trials.

Author information

Authors and Affiliations

Authors

Contributions

J.A.R.N. conducted the GWAS analyses; M.W. coordinated the execution of the phenotypic trials, and the collection and curation of the phenotypic data; J.B. developed the phenotypic experimental designs, formulated models and determined landrace parent–environment estimates; C.R. assisted with the GWAS analysis and data interpretation; K.S. performed genotype imputation; S.T., E.P., A.T., H.V.D.,V.V., A.O., A.E.B., N.O.G.M., I.O.-M. and A.G.E. conducted the phenotypic trials; F.S.V. and A.G.E. developed the test-cross germplasm; G.A., P.W. and E.S.B. developed the project concept; S.H. coordinated the genotypic data collection, meta-data creation and passport data curation; and J.A.R.N., S.H. and E.S.B. wrote the manuscript.

Corresponding authors

Correspondence to Sarah Hearne or Edward S Buckler.

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Competing interests

The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 Maize landrace FOAM design with crossing and evaluation nested within adaptation class.

Supplementary Figure 2 First two principal coordinates from multidimensional scaling of the genetic distance among accessions.

Colors correspond to country of origin according to passport information of the accession.

Supplementary Figure 3 Landrace adaptation classes in MDS space.

LT corresponds to lowland tropical, ST to subtropical and HL to highland. Highland landraces span most of the first principal coordinate, displaying incomplete differentiation from middle- and low-elevation populations. Those landraces appear admixed with subtropical and low-elevation landraces and are almost entirely exclusive to Mexican material. In contrast, subtropical and tropical landraces are present admixed across both axes.

Supplementary Figure 4 Genome-wide view of the LD empirical threshold.

Red shaded areas represent the centromeres. In general, for all chromosomes, centromeres and the pericentromeric regions display higher LD than the rest of the genome. Two additional regions, shaded in gray, are the inversions on chromosomes 3 and 4. The dashed horizontal line represents the empirical LD threshold used to define the set of high-LD regions.

Supplementary Figure 5 Overlap rate with flowering time.

Overlap rate is estimated for the top associating SNPs of altitude and latitude at various P-value thresholds.

Supplementary Figure 6 MDS of the centromere of chromosome 5.

MDS for FOAM landrace accessions (blue) and the NAM founders (red). Most NAM founders cluster together, sharing one allele, with the other alleles corresponding to Il14H (top right), P39 (bottom) and CML333 (middle).

Supplementary Figure 7 Frequency of INV4m according to each accession’s adaptation class.

Supplementary Figure 8 Genomic prediction accuracy across trials by trait (days to anthesis or days to silking) and marker density.

Supplementary Figure 9 Replication of accessions across trials

Supplementary Figure 10 GBS distribution of missing data.

Proportion missing before imputation by site and by individual for the GBS genotypes on the FOAM landrace parents.

Supplementary Figure 11 Distribution of depth of coverage across all sites and samples.

Supplementary Figure 12 Median LD across windows for FOAM landrace parents.

The LD threshold was chosen based on change in slope and corresponds to the red line.

Supplementary Figure 13 QQ plot for the flowering time GWAS.

Supplementary Figure 14 QQ plot for the altitude GWAS across models.

Models correspond to the generalized linear model (GLM), a model with a population structure covariate in the from of 10 PCs (GLM + Q), a mixed model with a relatedness matrix (MLM + K) and a mixed model with relatedness and population structure (MLM Q + K).

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–14 (PDF 1557 kb)

Supplementary Table 1

Phenotypic evaluation information. Lists years of evaluation, trial name, location, adaptation class, number of accessions evaluated, row length in meters, number of plants per row, and broad sense heritability estimates from variance partitioning model (XLSX 10 kb)

Supplementary Table 2

Top genes associated with female flowering (XLSX 61 kb)

Supplementary Table 3

Top genes associated with male flowering (XLSX 61 kb)

Supplementary Table 4

Gene Ontology enrichment for flowering time candidate genes (XLSX 12 kb)

Supplementary Table 5

Gene Ontology enrichment for genes associated with male and female flowering time in FOAM landrace panel (XLSX 10 kb)

Supplementary Table 6

Top SNPs associated with altitude (XLSX 117 kb)

Supplementary Table 7

Top SNPs associated with latitude (XLSX 248 kb)

Supplementary Table 8

CIMMYT inbred lines homozygous for the chromosome 4 inversion (XLSX 8 kb)

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Romero Navarro, J., Willcox, M., Burgueño, J. et al. A study of allelic diversity underlying flowering-time adaptation in maize landraces. Nat Genet 49, 476–480 (2017). https://doi.org/10.1038/ng.3784

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