Widespread Gene Conversion in Centromere Cores

Overview

Journal PLoS Biol

Specialty Biology

Date 2010 Mar 17

PMID 20231874

Citations 76

Authors

Jinghua Shi

Sarah E Wolf

John M Burke

Gernot G Presting

Jeffrey Ross-Ibarra

R Kelly Dawe

Affiliations

Soon will be listed here.

Abstract

Centromeres are the most dynamic regions of the genome, yet they are typified by little or no crossing over, making it difficult to explain the origin of this diversity. To address this question, we developed a novel CENH3 ChIP display method that maps kinetochore footprints over transposon-rich areas of centromere cores. A high level of polymorphism made it possible to map a total of 238 within-centromere markers using maize recombinant inbred lines. Over half of the markers were shown to interact directly with kinetochores (CENH3) by chromatin immunoprecipitation. Although classical crossing over is fully suppressed across CENH3 domains, two gene conversion events (i.e., non-crossover marker exchanges) were identified in a mapping population. A population genetic analysis of 53 diverse inbreds suggests that historical gene conversion is widespread in maize centromeres, occurring at a rate >1x10(-5)/marker/generation. We conclude that gene conversion accelerates centromere evolution by facilitating sequence exchange among chromosomes.

Citing Articles

The recombination landscape of introgression in yeast.

Schwarzkopf E, Brandt N, Smukowski Heil C PLoS Genet. 2025; 21(2):e1011585.

PMID: 39937775 PMC: 11845044. DOI: 10.1371/journal.pgen.1011585.

The recombination landscape of introgression in yeast.

Schwarzkopf E, Brandt N, Smukowski Heil C bioRxiv. 2024; .

PMID: 39026729 PMC: 11257466. DOI: 10.1101/2024.01.04.574263.

The structure, function, and evolution of plant centromeres.

Naish M, Henderson I Genome Res. 2024; 34(2):161-178.

PMID: 38485193 PMC: 10984392. DOI: 10.1101/gr.278409.123.

Three near-complete genome assemblies reveal substantial centromere dynamics from diploid to tetraploid in Brachypodium genus.

Chen C, Wu S, Sun Y, Zhou J, Chen Y, Zhang J Genome Biol. 2024; 25(1):63.

PMID: 38439049 PMC: 10910784. DOI: 10.1186/s13059-024-03206-w.

Dicentric chromosomes are resolved through breakage and repair at their centromeres.

Cook D, Kozmin S, Yeh E, Petes T, Bloom K Chromosoma. 2024; 133(2):117-134.

PMID: 38165460 PMC: 11180013. DOI: 10.1007/s00412-023-00814-6.

References

Murphy W, Larkin D, Everts-van der Wind A, Bourque G, Tesler G, Auvil L . Dynamics of mammalian chromosome evolution inferred from multispecies comparative maps. Science. 2005; 309(5734):613-7. DOI: 10.1126/science.1111387. View

Remington D, Thornsberry J, Matsuoka Y, Wilson L, Whitt S, Doebley J . Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci U S A. 2001; 98(20):11479-84. PMC: 58755. DOI: 10.1073/pnas.201394398. View

Lambie E, Roeder G . Repression of meiotic crossing over by a centromere (CEN3) in Saccharomyces cerevisiae. Genetics. 1986; 114(3):769-89. PMC: 1203013. DOI: 10.1093/genetics/114.3.769. View

Schindelhauer D, Schwarz T . Evidence for a fast, intrachromosomal conversion mechanism from mapping of nucleotide variants within a homogeneous alpha-satellite DNA array. Genome Res. 2002; 12(12):1815-26. PMC: 187568. DOI: 10.1101/gr.451502. View

Lee H, Zhang W, Langdon T, Jin W, Yan H, Cheng Z . Chromatin immunoprecipitation cloning reveals rapid evolutionary patterns of centromeric DNA in Oryza species. Proc Natl Acad Sci U S A. 2005; 102(33):11793-8. PMC: 1187982. DOI: 10.1073/pnas.0503863102. View

Wright S, Vroh Bi I, Schroeder S, Yamasaki M, Doebley J, McMullen M . The effects of artificial selection on the maize genome. Science. 2005; 308(5726):1310-4. DOI: 10.1126/science.1107891. View

Luce A, Sharma A, Mollere O, Wolfgruber T, Nagaki K, Jiang J . Precise centromere mapping using a combination of repeat junction markers and chromatin immunoprecipitation-polymerase chain reaction. Genetics. 2006; 174(2):1057-61. PMC: 1602074. DOI: 10.1534/genetics.106.060467. View

SanMiguel P, Gaut B, Tikhonov A, Nakajima Y, Bennetzen J . The paleontology of intergene retrotransposons of maize. Nat Genet. 1998; 20(1):43-5. DOI: 10.1038/1695. View

Jiang J, Birchler J, Parrott W, Dawe R . A molecular view of plant centromeres. Trends Plant Sci. 2003; 8(12):570-5. DOI: 10.1016/j.tplants.2003.10.011. View

10.

Fu Y, Wen T, Ronin Y, Chen H, Guo L, Mester D . Genetic dissection of intermated recombinant inbred lines using a new genetic map of maize. Genetics. 2006; 174(3):1671-83. PMC: 1667089. DOI: 10.1534/genetics.106.060376. View

11.

Copenhaver G, Nickel K, Kuromori T, Benito M, Kaul S, Lin X . Genetic definition and sequence analysis of Arabidopsis centromeres. Science. 2000; 286(5449):2468-74. DOI: 10.1126/science.286.5449.2468. View

12.

Wolfgruber T, Sharma A, Schneider K, Albert P, Koo D, Shi J . Maize centromere structure and evolution: sequence analysis of centromeres 2 and 5 reveals dynamic Loci shaped primarily by retrotransposons. PLoS Genet. 2009; 5(11):e1000743. PMC: 2776974. DOI: 10.1371/journal.pgen.1000743. View

13.

Kato A, Lamb J, Birchler J . Chromosome painting using repetitive DNA sequences as probes for somatic chromosome identification in maize. Proc Natl Acad Sci U S A. 2004; 101(37):13554-9. PMC: 518793. DOI: 10.1073/pnas.0403659101. View

14.

Hudson R, Kaplan N . Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics. 1985; 111(1):147-64. PMC: 1202594. DOI: 10.1093/genetics/111.1.147. View

15.

BEADLE G . A Possible Influence of the Spindle Fibre on Crossing-Over in Drosophila. Proc Natl Acad Sci U S A. 1932; 18(2):160-5. PMC: 1076180. DOI: 10.1073/pnas.18.2.160. View

16.

Lander E, Green P, ABRAHAMSON J, Barlow A, Daly M, Lincoln S . MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics. 1987; 1(2):174-81. DOI: 10.1016/0888-7543(87)90010-3. View

17.

Lee M, Sharopova N, Beavis W, Grant D, Katt M, Blair D . Expanding the genetic map of maize with the intermated B73 x Mo17 (IBM) population. Plant Mol Biol. 2002; 48(5-6):453-61. DOI: 10.1023/a:1014893521186. View

18.

Hudson R . Two-locus sampling distributions and their application. Genetics. 2002; 159(4):1805-17. PMC: 1461925. DOI: 10.1093/genetics/159.4.1805. View

19.

Hill W, Weir B . Variances and covariances of squared linkage disequilibria in finite populations. Theor Popul Biol. 1988; 33(1):54-78. DOI: 10.1016/0040-5809(88)90004-4. View

20.

Smith G . Evolution of repeated DNA sequences by unequal crossover. Science. 1976; 191(4227):528-35. DOI: 10.1126/science.1251186. View