Retroelement Genome Painting: Cytological Visualization of Retroelement Expansions in the Genera Zea and Tripsacum

Lamb, Jonathan C.; Birchler, James A.

doi:10.1534/genetics.105.053165

Cited by 63 publications

(49 citation statements)

References 46 publications

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“…To investigate whether recombination between retrotransposons extends beyond the CRM family, we performed a preliminary analysis of full-length Opie elements that revealed recombination sites in both the LTR and polyprotein regions (Figs. S5 and S6), indicating that retrotransposon recombination is not limited to the centromere-specific CRM family, which belongs to the Ty3/gypsy group of retrotransposons, but also occurs in this Ty1/copia element that is broadly distributed along Zea chromosome arms (6). However, the high frequency of recombinations among Opie elements, combined with the efficient removal of full-length elements from their chromosomal arm locations, provides a very spotty record of Opie element evolution and makes it difficult to reconstruct the history of these elements, let alone measure the effects on retrotransposition rate for individual recombination events.…”

Section: Resultsmentioning

confidence: 99%

“…Lineage-specific retrotransposon amplification has been documented in several plant genomes (4)(5)(6), and appears to result from temporary relief of otherwise tight suppression of transcription. Retrotransposon transcription has been shown to be induced by tissue culture (7), microbial elicitors of plant defense responses (8), and polyploidization (9), but this temporary increase in retrotransposon transcription has not been shown to effect genome expansion of the magnitude observed in many crop plants.…”

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confidence: 99%

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Sustained retrotransposition is mediated by nucleotide deletions and interelement recombinations

Sharma

Schneider

Presting

2008

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

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The term ''C-value paradox'' was coined by C. A. Thomas, Jr. in 1971 [Thomas CA (1971) Ann Rev Genetics 5:237-256] to describe the initially puzzling lack of correlation between an organism's genome size and its morphological complexity. Polyploidy and the expansion of repetitive DNA, primarily transposable elements, are two mechanisms that have since been found to account for this differential. While the inactivation of retrotransposons by methylation and their removal from the genome by illegitimate recombination have been well documented, the cause of the apparently periodic bursts of retrotranposon expansion is as yet unknown. We show that the expansion of the CRM1 retrotransposon subfamily in the ancient allotetraploid crop plant corn is linked to the repeated formation of novel recombinant elements derived from two parental retrotransposon genotypes, which may have been brought together during the hybridization of two sympatric species that make up the present day corn genome, thus revealing a unique mechanism linking polyploidy and retrotransposition.centromere ͉ corn ͉ genome expansion ͉ chromodomain ͉ polyploidy M any of the world's crop plants are polyploids. Corn, the most widely grown food crop in the United States, is known to have an allotetraploid origin not later than 4.8 million years ago (MYA) (1, 2) from two parental genomes that had diverged from each other Ϸ11.9 MYA (2). This tetraploidization event was followed by a major genome expansion mediated by retrotransposons (3), the cause of which is unknown.Lineage-specific retrotransposon amplification has been documented in several plant genomes (4-6), and appears to result from temporary relief of otherwise tight suppression of transcription. Retrotransposon transcription has been shown to be induced by tissue culture (7), microbial elicitors of plant defense responses (8), and polyploidization (9), but this temporary increase in retrotransposon transcription has not been shown to effect genome expansion of the magnitude observed in many crop plants.In contrast, the forces counteracting genome expansion are fairly well understood and documented, and are known to include recombination between long terminal repeats (LTRs) of a single element (10, 11) or adjacent elements (10, 12), leading to solo LTRs or complex hybrid retrotransposon arrangements, and illegitimate recombinations, which result in deletions between very short regions of sequence homology on the same DNA strand (10). These factors contribute to element inactivation and removal and limit the estimated half-life of rice retrotransposons to Ͻ6 million years (13). Genome expansion requires that retrotransposition rates be sustained at levels higher than element removal rates. How retrotransposons accomplish this has thus far been completely unknown (14).Centromeric retrotransposons (CR) comprise a family of elements that show strong preference for integration at active centromeres (15,16). Two CR subfamilies have been recognized in maize (CRM1 and CRM2) and rice (CRR1 and CRR2) for so...

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Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

Sustained retrotransposition is mediated by nucleotide deletions and interelement recombinations

Sharma

Schneider

Presting

2008

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

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“…Functional centromeres of maize consist of 1-2 Mb of DNA enriched for the tandemly arranged CentC repeat and members of the centromeric retrotransposon (CR) family (12), which are widely distributed in seed plants and have been extensively characterized (13)(14)(15)(16)(17)(18). Elements belonging to the maize CR1, CR2, and CR3 subfamilies have the remarkable ability to target their integration to centromeres and thus mark the historic centromere positions (12).FISH analysis has revealed that most centromeres of teosinte, and all centromeres of other Zea species and the more distantly related genus Tripsacum, contain large amounts of CentC (19,20), suggesting that CentC-rich centromeres represent the ancestral state. In contrast, centromeres of domesticated maize display a remarkable variation of CentC content in different inbreds (19).…”

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“…FISH analysis has revealed that most centromeres of teosinte, and all centromeres of other Zea species and the more distantly related genus Tripsacum, contain large amounts of CentC (19,20), suggesting that CentC-rich centromeres represent the ancestral state. In contrast, centromeres of domesticated maize display a remarkable variation of CentC content in different inbreds (19).…”

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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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“…Although effective in all tested inbred lines, the application of the repetitive element cocktail for somatic karyotyping has some limitations. The presence and copy number of repetitive elements varies among maize lines (Rivin et al 1986;Kato et al 2004;Lamb and Birchler 2006) and related species . Therefore, the hybridization pattern must be determined for each line.…”

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Single-Gene Detection and Karyotyping Using Small-Target Fluorescence in Situ Hybridization on Maize Somatic Chromosomes

et al. 2007

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Combined with a system for identifying each of the chromosomes in a genome, visualizing the location of individual genetic loci by fluorescence in situ hybridization (FISH) would aid in assembling physical and genetic maps. Previously, large genomic clones have been successfully used as FISH probes onto somatic chromosomes but this approach is complicated in species with abundant repetitive elements. In this study, repeat-free portions of sequences that were anchored to particular chromosomes including genes, gene clusters, large cDNAs, and portions of BACs obtained from public databases were used to label the corresponding physical location using FISH. A collection of probes that includes at least one marker on each chromosome in the maize complement was assembled, allowing a small-target karyotyping system to be developed. This set provides the foundation onto which additional loci could be added to strengthen further the ability to perform chromosomal identification in maize and its relatives. The probes were demonstrated to produce signals in several wild relatives of maize, including Zea luxurians, Z. diploperennis, and Tripsacum dactyloides.

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Retroelement Genome Painting: Cytological Visualization of Retroelement Expansions in the Genera Zea and Tripsacum

Cited by 63 publications

References 46 publications

Sustained retrotransposition is mediated by nucleotide deletions and interelement recombinations

Sustained retrotransposition is mediated by nucleotide deletions and interelement recombinations

Inbreeding drives maize centromere evolution

Single-Gene Detection and Karyotyping Using Small-Target Fluorescence in Situ Hybridization on Maize Somatic Chromosomes

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