Eucaryotic Genome Evolution Through the Spontaneous Duplication of Large Chromosomal Segments

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 2003 Dec 20

PMID 14685272

Citations 96

Authors

Romain Koszul

Sandrine Caburet

Bernard Dujon

Gilles Fischer

Affiliations

Soon will be listed here.

Abstract

There is growing evidence that duplications have played a major role in eucaryotic genome evolution. Sequencing data revealed the presence of large duplicated regions in the genomes of many eucaryotic organisms, and comparative studies have suggested that duplication of large DNA segments has been a continuing process during evolution. However, little experimental data have been produced regarding this issue. Using a gene dosage assay for growth recovery in Saccharomyces cerevisiae, we demonstrate that a majority of the revertant strains (58%) resulted from the spontaneous duplication of large DNA segments, either intra- or interchromosomally, ranging from 41 to 655 kb in size. These events result in the concomitant duplication of dozens of genes and in some cases in the formation of chimeric open reading frames at the junction of the duplicated blocks. The types of sequences at the breakpoints as well as their superposition with the replication map suggest that spontaneous large segmental duplications result from replication accidents. Aneuploidization events or suppressor mutations that do not involve large-scale rearrangements accounted for the rest of the reversion events (in 26 and 16% of the strains, respectively).

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References

Robinson-Rechavi M, Marchand O, Escriva H, Laudet V . An ancestral whole-genome duplication may not have been responsible for the abundance of duplicated fish genes. Curr Biol. 2001; 11(12):R458-9. DOI: 10.1016/s0960-9822(01)00280-9. View

Cha R, Kleckner N . ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones. Science. 2002; 297(5581):602-6. DOI: 10.1126/science.1071398. View

Bailey J, Gu Z, Clark R, Reinert K, Samonte R, Schwartz S . Recent segmental duplications in the human genome. Science. 2002; 297(5583):1003-7. DOI: 10.1126/science.1072047. View

Lupski J . Genomic disorders: structural features of the genome can lead to DNA rearrangements and human disease traits. Trends Genet. 1998; 14(10):417-22. DOI: 10.1016/s0168-9525(98)01555-8. View

Pelletier R, Krasilnikova M, Samadashwily G, Lahue R, Mirkin S . Replication and expansion of trinucleotide repeats in yeast. Mol Cell Biol. 2003; 23(4):1349-57. PMC: 141142. DOI: 10.1128/MCB.23.4.1349-1357.2003. View

Malkova A, Ivanov E, Haber J . Double-strand break repair in the absence of RAD51 in yeast: a possible role for break-induced DNA replication. Proc Natl Acad Sci U S A. 1996; 93(14):7131-6. PMC: 38948. DOI: 10.1073/pnas.93.14.7131. View

Winzeler E, Shoemaker D, Astromoff A, Liang H, Anderson K, Andre B . Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science. 1999; 285(5429):901-6. DOI: 10.1126/science.285.5429.901. View

Morrow D, Connelly C, Hieter P . "Break copy" duplication: a model for chromosome fragment formation in Saccharomyces cerevisiae. Genetics. 1997; 147(2):371-82. PMC: 1208164. DOI: 10.1093/genetics/147.2.371. View

Wong S, Butler G, Wolfe K . Gene order evolution and paleopolyploidy in hemiascomycete yeasts. Proc Natl Acad Sci U S A. 2002; 99(14):9272-7. PMC: 123130. DOI: 10.1073/pnas.142101099. View

10.

Abdel-Rahman W, Katsura K, Rens W, GORMAN P, Sheer D, Bicknell D . Spectral karyotyping suggests additional subsets of colorectal cancers characterized by pattern of chromosome rearrangement. Proc Natl Acad Sci U S A. 2001; 98(5):2538-43. PMC: 30173. DOI: 10.1073/pnas.041603298. View

11.

Spector L, Fogel S . Mitotic hyperploidy for chromosomes VIII and III in Saccharomyces cerevisiae. Curr Genet. 1992; 21(4-5):309-18. DOI: 10.1007/BF00351688. View

12.

Wach A, Brachat A, Pohlmann R, Philippsen P . New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast. 1994; 10(13):1793-808. DOI: 10.1002/yea.320101310. View

13.

Myung K, Datta A, Kolodner R . Suppression of spontaneous chromosomal rearrangements by S phase checkpoint functions in Saccharomyces cerevisiae. Cell. 2001; 104(3):397-408. DOI: 10.1016/s0092-8674(01)00227-6. View

14.

Roelants F, Potier S, Souciet J, De Montigny J . Reactivation of the ATCase domain of the URA2 gene complex: a positive selection method for Ty insertions and chromosomal rearrangements in Saccharomyces cerevisiae. Mol Gen Genet. 1995; 246(6):767-73. DOI: 10.1007/BF00290725. View

15.

Llorente B, Malpertuy A, Neuveglise C, De Montigny J, Aigle M, Artiguenave F . Genomic exploration of the hemiascomycetous yeasts: 18. Comparative analysis of chromosome maps and synteny with Saccharomyces cerevisiae. FEBS Lett. 2001; 487(1):101-12. DOI: 10.1016/s0014-5793(00)02289-4. View

16.

Courseaux A, Richard F, Grosgeorge J, Ortola C, Viale A, Turc-Carel C . Segmental duplications in euchromatic regions of human chromosome 5: a source of evolutionary instability and transcriptional innovation. Genome Res. 2003; 13(3):369-81. PMC: 430257. DOI: 10.1101/gr.490303. View

17.

Llorente B, Durrens P, Malpertuy A, Aigle M, Artiguenave F, Blandin G . Genomic exploration of the hemiascomycetous yeasts: 20. Evolution of gene redundancy compared to Saccharomyces cerevisiae. FEBS Lett. 2001; 487(1):122-33. DOI: 10.1016/s0014-5793(00)02291-2. View

18.

Bach M, Roelants F, De Montigny J, Huang M, Potier S, Souciet J . Recovery of gene function by gene duplication in Saccharomyces cerevisiae. Yeast. 1995; 11(2):169-77. DOI: 10.1002/yea.320110208. View

19.

Whittaker S, Rockmill B, Blechl A, Maloney D, Resnick M, Fogel S . The detection of mitotic and meiotic aneuploidy in yeast using a gene dosage selection system. Mol Gen Genet. 1988; 215(1):10-8. DOI: 10.1007/BF00331296. View

20.

Locke D, Segraves R, Carbone L, Archidiacono N, Albertson D, Pinkel D . Large-scale variation among human and great ape genomes determined by array comparative genomic hybridization. Genome Res. 2003; 13(3):347-57. PMC: 430292. DOI: 10.1101/gr.1003303. View