Maize centromeres expand and adopt a uniform size in the genetic background of oat

Wang, Kai; Wu, Yufeng; Zhang, Wenli; Dawe, R. Kelly; Jiang, Jiming

doi:10.1101/gr.160887.113

Cited by 79 publications

(108 citation statements)

References 60 publications

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“…S7) that allow phylogenetic reconstruction of CEN5 in the 28 maize inbreds examined. confirms previous reports of active genes in functional centromeres (24,25). The fact that CEN5 is retained in almost its entirety in all maize and teosinte inbreds (SI Appendix, Fig.…”

Section: Significancesupporting

confidence: 77%

Inbreeding drives maize centromere evolution

Schneider

Xie

Wolfgruber

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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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...

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Section: Significancesupporting

confidence: 77%

Inbreeding drives maize centromere evolution

Schneider

Xie

Wolfgruber

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Most newly formed neocentromeres are associated with gene "desert" regions and do not contain satellite repeats (Marshall et al, 2008;K. Wang et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Boom-Bust Turnovers of Megabase-Sized Centromeric DNA inSolanumSpecies: Rapid Evolution of DNA Sequences Associated with Centromeres

et al. 2014

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Centromeres are composed of long arrays of satellite repeats in most multicellular eukaryotes investigated to date. The satellite repeat-based centromeres are believed to have evolved from "neocentromeres" that originally contained only single-or low-copy sequences. However, the emergence and evolution of the satellite repeats in centromeres has been elusive. Potato (Solanum tuberosum) provides a model system for studying centromere evolution because each of its 12 centromeres contains distinct DNA sequences, allowing comparative analysis of homoeologous centromeres from related species. We conducted genome-wide analysis of the centromeric sequences in Solanum verrucosum, a wild species closely related to potato. Unambiguous homoeologous centromeric sequences were detected in only a single centromere (Cen9) between the two species. Four centromeres (Cen2, Cen4, Cen7, and Cen10) in S. verrucosum contained distinct satellite repeats that were amplified from retrotransposon-related sequences. Strikingly, the same four centromeres in potato contain either different satellite repeats (Cen2 and Cen7) or exclusively single-and low-copy sequences (Cen4 and Cen10). Our sequence comparison of five homoeologous centromeres in two Solanum species reveals rapid divergence of centromeric sequences among closely related species. We propose that centromeric satellite repeats undergo boom-bust cycles before a favorable repeat is fixed in the population.

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“…Neocentromere activation is usually associated with the loss of the original centromere (duSart et al 1997), or with inactivation but retention of the original centromere on the same chromosome (Amor et al 2004;Wang et al 2014). The vast majority of neocentromeres, including several plant neocentromeres (Nasuda et al 2005;Fu et al 2013;Wang et al 2014;Zhang et al 2013a), do not contain long arrays of satellite repeats that are typically associated with centromeres. The neocentromeric DNA sequences are generally deficient in genes, but otherwise not distinct from average genome sequences (Marshall et al 2008;Wang et al 2014).…”

mentioning

confidence: 99%

“…The vast majority of neocentromeres, including several plant neocentromeres (Nasuda et al 2005;Fu et al 2013;Wang et al 2014;Zhang et al 2013a), do not contain long arrays of satellite repeats that are typically associated with centromeres. The neocentromeric DNA sequences are generally deficient in genes, but otherwise not distinct from average genome sequences (Marshall et al 2008;Wang et al 2014). A centromere can also "move" to a different position along the chromosome during evolution (Ventura et al 2001;Han et al 2009).…”

mentioning

confidence: 99%