Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2023 Mar;33(3):359-370.
doi: 10.1101/gr.276705.122. Epub 2023 Feb 28.

Large haplotypes highlight a complex age structure within the maize pan-genome

Jianing Liu  1 , R Kelly Dawe  2   3
Affiliations

Large haplotypes highlight a complex age structure within the maize pan-genome

Jianing Liu et al. Genome Res. 2023 Mar.

Abstract

The genomes of maize and other eukaryotes contain stable haplotypes in regions of low recombination. These regions, including centromeres, long heterochromatic blocks, and rDNA arrays, have been difficult to analyze with respect to their diversity and origin. Greatly improved genome assemblies are now available that enable comparative genomics over these and other nongenic spaces. Using 26 complete maize genomes, we developed methods to align intergenic sequences while excluding genes and regulatory regions. The centromere haplotypes (cenhaps) extend for megabases on either side of the functional centromere regions and appear as evolutionary strata, with haplotype divergence/coalescence times dating as far back as 450 thousand years ago (kya). Application of the same methods to other low recombination regions (heterochromatic knobs and rDNA) and all intergenic spaces revealed that deep coalescence times are ubiquitous across the maize pan-genome. Divergence estimates vary over a broad timescale with peaks at ∼16 and 300 kya, reflecting a complex history of gene flow among diverging populations and changes in population size associated with domestication. Cenhaps and other long haplotypes provide vivid displays of this ancient diversity.

PubMed Disclaimer

Figures

Figure 1.
Figure 1.
Cenhaps on Chromosome 8. (A) Alignments between NAM lines and B73 over Chromosome 8. Syntenic aligned regions (gray) and inverted segments (red) are shown. Blue arrows show the cenhap region with exceptional divergence. (B) Alignments between NAM lines and P39 over Chromosome 8. Annotation is the same as A. (C) Pairwise alignments and TE comparisons between CML322, CML52, and B73 over an ∼1 Mb region of Chromosome 8. Total kb of major TE families are shown below, in colors that match the annotation in the main panel (see Supplemental Fig. S9 for a more detailed view of TE subfamilies). This region does not include the CENH3 or CentC domains. (D) Pairwise alignments between NAM lines and B73 over CentC arrays on Chromosome 8. x- and y-axes show CentC monomers, and color intensity reflects the Jaccard index (JI) between each monomer pair. The non-B73 haplotypes are shaded in olive. (E) Clustering of CentC arrays on centromere 8. The colors over inbred names indicate varieties of corn: northern flint (pink), temperate (blue), mixed (red), and tropical (green).
Figure 2.
Figure 2.
Divergence times of cenhaps. (A) Divergence times between NAM lines and B73 over pericentromeric regions. Dots represent estimated divergence times over 20-kb windows. The cenhap regions are highlighted in blue. (B) Cenhaps outlined in A. The divergence times over CentC regions (orange bars) are not reliable because of inaccurate alignment over CentC arrays and embedded retrotransposons within the arrays.
Figure 3.
Figure 3.
Ancient haplotypes in the 9S knob and NOR. (A) Dot-matrix alignments between 21 NAM lines and B73 over the knob180 array on Chromosome 9S (only 21 have the 9S knob). x- and y-axes show knob180 monomers, and color intensity reflects the Jaccard index between each monomer pair. (B) Clustering of 9S knobs based on repeat array alignments. Divergence times from B73 (kya) were calculated using syntenic SNPs in TEs that lie within the arrays. In panel A the non-B73 haplotypes are indicated in olive and green, and the corresponding clusters in B are circled in matching colors. (C) Dot-matrix alignments between 25 NAM lines and B73 over the NOR. x- and y-axes show 18S rDNA monomers, and color intensity reflects the Jaccard index (JI) between each monomer pair. (D) Clustering of the 6S knob180 array that is about 10 Mb from the NOR on Chromosome 6. The TEs in the knob were dated using syntenic SNPs. In B and D, the colors over individual inbred names indicate varieties of corn: northern flint (pink), temperate (blue), mixed (red), and tropical (green).
Figure 4.
Figure 4.
Whole-genome age distributions. (A) Hierarchical clustering of cenhaps from three chromosomes showing that most cenhap diversity dates to 10–30 kya. (B) Divergence times of intergenic spaces estimated from 20-kb windows represented in a density plot. (C) Density plot of all divergence times displayed in B. The x-axis shows probability densities, where the total area under the curve is 1. Local maxima are highlighted as red dots. When the B73 haplotype is compared to similar haplotypes, there is good alignment and few SNPs, giving discrete young peaks on the right of the curve (at ∼2.4, 1.6, and 0.8 kya, representing windows with 3, 2, or 1 SNP). When B73 is compared to more divergent haplotypes, there are more SNPs and the aligned regions may be smaller due to the presence of SVs (such as a deletion). In these cases, the denominators change to the size of the alignable sequence, causing the age distribution to become more continuous at older ages. (D) Density plot of cenhap divergence times only, annotated as in C. The two large peaks at older age represent cases where the B73 cenhap is in the minority group and diverged from most other cenhaps ∼220 kya (Chr 2) or ∼60 kya (Chr 7). (E) Effective population size (Ne) of maize over the past 0.5 million yr.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

References

    1. Abouelhoda MI, Ohlebusch E. 2005. Chaining algorithms for multiple genome comparison. J Discrete Algorithms 3: 321–341. 10.1016/j.jda.2004.08.011 - DOI
    1. Albert PS, Gao Z, Danilova TV, Birchler JA. 2010. Diversity of chromosomal karyotypes in maize and its relatives. Cytogenet Genome Res 129: 6–16. 10.1159/000314342 - DOI - PubMed
    1. Altemose N, Logsdon GA, Bzikadze AV, Sidhwani P, Langley SA, Caldas GV, Hoyt SJ, Uralsky L, Ryabov FD, Shew CJ, et al. 2022. Complete genomic and epigenetic maps of human centromeres. Science 376: eabl4178. 10.1126/science.abl4178 - DOI - PMC - PubMed
    1. Andorf C, Beavis WD, Hufford M, Smith S, Suza WP, Wang K, Woodhouse M, Yu J, Lübberstedt T. 2019. Technological advances in maize breeding: past, present and future. Theor Appl Genet 132: 817–849. 10.1007/s00122-019-03306-3 - DOI - PubMed
    1. Ardelean CF, Becerra-Valdivia L, Pedersen MW, Schwenninger J-L, Oviatt CG, Macías-Quintero JI, Arroyo-Cabrales J, Sikora M, Ocampo-Díaz YZE, Rubio-Cisneros II, et al. 2020. Evidence of human occupation in Mexico around the last glacial maximum. Nature 584: 87–92. 10.1038/s41586-020-2509-0 - DOI - PubMed

Publication types

LinkOut - more resources