Inbreeding drives maize centromere evolution

Abstract

Functional centromeres, the chromosomal sites of spindle attachment during cell division, are marked epigenetically by the centromerespecific histone H3 variant cenH3 and typically contain long stretches of centromere-specific tandem DNA repeats (∼1.8 Mb in maize). In 23 inbreds of domesticated maize chosen to represent the genetic diversity of maize germplasm, partial or nearly complete loss of the tandem DNA repeat CentC precedes 57 independent cenH3 relocation events that result in neocentromere formation. Chromosomal regions with newly acquired cenH3 are colonized by the centromere-specific retrotransposon CR2 at a rate that would result in centromere-sized CR2 clusters in 20,000-95,000 y. Three lines of evidence indicate that CentC loss is linked to inbreeding, including (i) CEN10 of temperate lineages, presumed to have experienced a genetic bottleneck, contain less CentC than their tropical relatives; (ii) strong selection for centromere-linked genes in domesticated maize reduced diversity at seven of the ten maize centromeres to only one or two postdomestication haplotypes; and (iii) the centromere with the largest number of haplotypes in domesticated maize (CEN7) has the highest CentC levels in nearly all domesticated lines. Rare recombinations introduced one (CEN2) or more (CEN5) alternate CEN haplotypes while retaining a single haplotype at domestication loci linked to these centromeres. Taken together, this evidence strongly suggests that inbreeding, favored by postdomestication selection for centromere-linked genes affecting key domestication or agricultural traits, drives replacement of the tandem centromere repeats in maize and other crop plants. Similar forces may act during speciation in natural systems.centromere drive | centromere paradox | founder effect | hemicentric inversion | linkage disequilibrium C entromere-specific tandemly arranged DNA repeats vary in length and nucleotide sequence between species. The puzzling observation that centromeres can consist of highly variable sequences despite being involved in an essential cellular function (i.e., chromosome segregation) has been coined the "centromere paradox" (1). "Centromere drive" has been proposed to preferentially segregate the "favored" centromere into the female gamete and thereby provide the selective force that acts on centromere DNA sequences and interacting proteins (2).Maize (Zea mays ssp. mays) was domesticated between 7.5 and 10 thousand years ago (ka) from wind-pollinated outcrossing wild teosinte (Z. mays ssp. parviglumis) (3, 4) in a process that dramatically changed its morphology. Several quantitative trait loci (QTLs) responsible for these morphological changes were identified in pioneering work (5-8), and a large number of additional genetic loci involved in maize domestication and improvement were subsequently identified in genome-wide scans (9). Gene (and centromere) flow between the fully interfertile maize and teosinte subspecies has been documented (10, 11). Functional centromeres of maize consist of 1-2 Mb of DN...

Centromere location in Arabidopsis is unaltered by extreme divergence in CENH3 protein sequence

“…Although this result may not be so surprising in the case of a close relative such as L. oleraceum CENH3, it is remarkable for Z. mays CENH3. The association between CENH3 nucleosomes and maize DNA is variable, as multiple relocation events have been characterized in the domesticated population (Schneider et al 2016). There is no sequence similarity between centromeric sequences of the monocot Z. mays and dicot A. thaliana.…”

Improved maize reference genome with single-molecule technologies

“…Alignment of chromatin immunoprecipitation followed by sequencing (ChIP-seq) data for the centromere specific histone H3 (CENH3) 14 revealed that centromeres are accurately placed and largely intact. Several previously identified 15 megabase sized mis oriented pericentromeric regions were also corrected (Extended Data Fig. 3a, b).…”

“…7). The high density of alignments across and near many of the exceedingly retrotransposon rich centromeres reflects the comparatively low genetic diversity of most centromeres in domesticated maize 15 and illustrates the ability of the combined optical mapping/single molecule sequencing methodology to traverse large repeat rich regions. Within the aligned regions, approximately 32% of the Ki11 and 26% of the W22 optical maps exhibited clear evidence of structural variation, including 3,408 insertions and 3,298 deletions ( Table 2).…”

Remarkable Evolutionary Plasticity of Centromeric Chromatin

“…The domestication of selfish elements appears to be responsible for the most remarkable example of centromere evolution, the partial or complete replacement of the satellite centromeres of the wild ancestor of maize by a selfish element in maize inbred lines (Schneider et al 2016). During domestication of maize from teosinte over the past ∼9000 years, selection for agronomic traits was accompanied by dense insertion of CR2 centromerespecific retrotransposons and frequent loss by small inversions and deletions of the ancestral 155-bp CentC satellite in all 10 maize centromeres, 57 times independently in 26 inbred lines.…”