The Evolution of a High Copy Gene Array in Arabidopsis

Kane, Joshua; Freeling, Michael; Lyons, Eric

doi:10.1007/s00239-010-9350-2

The Evolution of a High Copy Gene Array in Arabidopsis

Journal Article · Sat May 22 00:00:00 EDT 2010 · Journal of Molecular Evolution

DOI:https://doi.org/10.1007/s00239-010-9350-2· OSTI ID:1816152

Kane, Joshua ^[1]; Freeling, Michael ^[2]; Lyons, Eric ^[2]

Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology; OSTI
Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology

Local gene duplication is a prominent mechanism of gene copy number expansion. Elucidating the mechanisms by which local duplicates arise is necessary in understanding the evolution of genomes and their host organisms. Chromosome one of Arabidopsis thaliana contains an 81-gene array subdivided into 27 triplet units (t-units), with each t-unit containing three pre-transfer RNA genes. We utilized phylogenetic tree reconstructions and comparative genomics to order the events leading to the array’s formation, and propose a model using unequal crossing-over as the primary mechanism of array formation. The model is supported by additional phylogenetic information from intergenic spacer sequences separating each t-unit, comparative analysis to an orthologous array of 12 t-units in the sister taxa Arabidopsis lyrata, and additional modeling using a stochastic simulation of orthologous array divergence. Lastly, comparative phylogenetic analysis demonstrates that the two orthologous t-unit arrays undergo concerted evolution within each taxa and are likely fluctuating in copy number under neutral evolutionary drift. These findings hold larger implications for future research concerning gene and genome evolution.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of California, Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC); National Science Foundation (NSF)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1816152

Journal Information:: Journal of Molecular Evolution, Journal Name: Journal of Molecular Evolution Journal Issue: 6 Vol. 70; ISSN 0022-2844

Publisher:: Springer NatureCopyright Statement

Country of Publication:: United States

Language:: English

References (51)

Expression of nuclear tRNATyr genes from Arabidopsis thaliana in HeLa cell and wheat germ extracts Stange, Nicole; Beier, Dagmar; Beier, Hildburg Plant Molecular Biology, Vol. 16, Issue 5 https://doi.org/10.1007/bf00015078	journal	May 1991
Nuclear tRNATyr genes are highly amplified at a single chromosomal site in the genome of Arabidopsis thaliana Beier, Dagmar; Stange, Nicole; Gross, Hans J. Molecular and General Genetics MGG, Vol. 225, Issue 1 https://doi.org/10.1007/bf00282644	journal	January 1991
Rates of Nucleotide Substitution in Angiosperm Mitochondrial DNA Sequences and Dates of Divergence Between Brassica and Other Angiosperm Lineages Yang, Yau-Wen; Lai, Kun-Nan; Tai, Pon-Yean Journal of Molecular Evolution, Vol. 48, Issue 5 https://doi.org/10.1007/pl00006502	journal	May 1999
Molecular and biological characterization of an isolate of the potyvirus passiflora virus Y naturally infecting soybean (Glycine max) in Brazil Ribeiro-Junior, Marcos Roberto; Barreto da Silva, Felipe; Marubayashi, Julio Massaharu Archives of Virology, Vol. 167, Issue 12 https://doi.org/10.1007/s00705-022-05605-5	journal	September 2022
A comparison of the ribosomal DNA's of Xenopus laevis and Xenopus mulleri: the evolution of tandem genes Brown, Donald D.; Wensink, Pieter C.; Jordan, Eddie Journal of Molecular Biology, Vol. 63, Issue 1 https://doi.org/10.1016/0022-2836(72)90521-9	journal	January 1972
A split promoter for a eucaryotic tRNA gene Hofstetter, Hans; Kressmann, Armin; Birnstiel, Max L. Cell, Vol. 24, Issue 2 https://doi.org/10.1016/0092-8674(81)90348-2	journal	May 1981
Isolation and properties of bacteria capable of high rates of β-galactosidase synthesis Horiuchi, Tadao; Tomizawa, Jun-Ichi; Novick, Aaron Biochimica et Biophysica Acta (BBA) - Specialized Section on Nucleic Acids and Related Subjects, Vol. 55, Issue 1-2 https://doi.org/10.1016/0926-6550(62)90226-8	journal	January 1962
The dual nature of homologous recombination in plants Schuermann, D.; Molinier, J.; Fritsch, O. Trends in Genetics, Vol. 21, Issue 3 https://doi.org/10.1016/j.tig.2005.01.002	journal	March 2005
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/s0022-2836(05)80360-2	journal	October 1990
Recent duplication, domain accretion and the dynamic mutation of the human genome Eichler, Evan E. Trends in Genetics, Vol. 17, Issue 11 https://doi.org/10.1016/s0168-9525(01)02492-1	journal	November 2001
A Relationship between Dominance, Phenotypic Stability and Variability, and a Theory of Alternative Genetic Pathways Lewis, D. Nature, Vol. 172, Issue 4390 https://doi.org/10.1038/1721136a0	journal	December 1953
The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla No authors listed Nature, Vol. 449, Issue 7161, p. 463-467 https://doi.org/10.1038/nature06148	journal	August 2007
Recombination: an underappreciated factor in the evolution of plant genomes Gaut, Brandon S.; Wright, Stephen I.; Rizzon, Carène Nature Reviews Genetics, Vol. 8, Issue 1 https://doi.org/10.1038/nrg1970	journal	January 2007
Rapid duplication and loss of genes coding for the alpha chains of hemoglobin. Zimmer, E. A.; Martin, S. L.; Beverley, S. M. Proceedings of the National Academy of Sciences, Vol. 77, Issue 4 https://doi.org/10.1073/pnas.77.4.2158	journal	April 1980
Time for acquiring a new gene by duplication. Ohta, T. Proceedings of the National Academy of Sciences, Vol. 85, Issue 10 https://doi.org/10.1073/pnas.85.10.3509	journal	May 1988
Unequal crossing over then and now. Tartof, K. D. Genetics, Vol. 120, Issue 1 https://doi.org/10.1093/genetics/120.1.1	journal	September 1988
Meiotic Recombination Between Paralogous RBCSB Genes on Sister Chromatids of Arabidopsis thaliana Jelesko, John G.; Carter, Kristy; Thompson, Whitney Genetics, Vol. 166, Issue 2 https://doi.org/10.1093/genetics/166.2.947	journal	February 2004
Molecular Evolution of Minisatellites in Hemiascomycetous Yeasts Richard, Guy-Franck; Dujon, Bernard Molecular Biology and Evolution, Vol. 23, Issue 1 https://doi.org/10.1093/molbev/msj022	journal	September 2005
tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence Lowe, Todd M.; Eddy, Sean R. Nucleic Acids Research, Vol. 25, Issue 5 https://doi.org/10.1093/nar/25.5.955	journal	March 1997
Analysis of Intrachromosomal Duplications in Yeast Saccharomyces cerevisiae: A Possible Model for Their Origin Achaz, Guillaume; Coissac, Eric; Viari, Alain Molecular Biology and Evolution, Vol. 17, Issue 8 https://doi.org/10.1093/oxfordjournals.molbev.a026410	journal	August 2000
Highly efficient concerted evolution in the ribosomal DNA repeats: Total rDNA repeat variation revealed by whole-genome shotgun sequence data Ganley, A. R. D.; Kobayashi, T. Genome Research, Vol. 17, Issue 2 https://doi.org/10.1101/gr.5457707	journal	January 2007
Human-Mouse Alignments with BLASTZ Schwartz, S. Genome Research, Vol. 13, Issue 1 https://doi.org/10.1101/gr.809403	journal	January 2003
Finding and Comparing Syntenic Regions among Arabidopsis and the Outgroups Papaya, Poplar, and Grape: CoGe with Rosids Lyons, Eric; Pedersen, Brent; Kane, Josh Plant Physiology, Vol. 148, Issue 4 https://doi.org/10.1104/pp.108.124867	journal	October 2008
Very Low Gene Duplication Rate in the Yeast Genome Gao, Li-zhi; Innan, Hideki Science, Vol. 306, Issue 5700 https://doi.org/10.1126/science.1102033	journal	November 2004
The Evolutionary Fate and Consequences of Duplicate Genes Lynch, M. Science, Vol. 290, Issue 5494 https://doi.org/10.1126/science.290.5494.1151	journal	November 2000
Bias in Plant Gene Content Following Different Sorts of Duplication: Tandem, Whole-Genome, Segmental, or by Transposition Freeling, Michael Annual Review of Plant Biology, Vol. 60, Issue 1 https://doi.org/10.1146/annurev.arplant.043008.092122	journal	June 2009
Concerted and Birth-and-Death Evolution of Multigene Families Nei, Masatoshi; Rooney, Alejandro P. Annual Review of Genetics, Vol. 39, Issue 1 https://doi.org/10.1146/annurev.genet.39.073003.112240	journal	December 2005
Tandem gene arrays in Trypanosoma brucei: Comparative phylogenomic analysis of duplicate sequence variation Jackson, Andrew P. BMC Evolutionary Biology, Vol. 7, Issue 1 https://doi.org/10.1186/1471-2148-7-54	journal	January 2007
Gene Duplication: The Genomic Trade in Spare Parts Hurles, Matthew PLoS Biology, Vol. 2, Issue 7 https://doi.org/10.1371/journal.pbio.0020206	journal	July 2004
Evolution by Gene Duplication Ohno, Susumu Springer Berlin, Heidelberg https://doi.org/10.1007/978-3-642-86659-3	book	January 1970
Expression of nuclear tRNATyr genes from Arabidopsis thaliana in HeLa cell and wheat germ extracts Stange, Nicole; Beier, Dagmar; Beier, Hildburg Plant Molecular Biology, Vol. 16, Issue 5 https://doi.org/10.1007/BF00015078	journal	May 1991
Nuclear tRNATyr genes are highly amplified at a single chromosomal site in the genome of Arabidopsis thaliana Beier, Dagmar; Stange, Nicole; Gross, Hans J. Molecular and General Genetics MGG, Vol. 225, Issue 1 https://doi.org/10.1007/BF00282644	journal	January 1991
Expression of variant nuclearArabidopsis tRNASer genes and pre-tRNA maturation differ in HeLa, yeast and wheat germ extracts Beier, Dagmar; Beier, Hildburg Molecular and General Genetics MGG, Vol. 233, Issue 1-2 https://doi.org/10.1007/BF00587580	journal	May 1992
Rates of Nucleotide Substitution in Angiosperm Mitochondrial DNA Sequences and Dates of Divergence Between Brassica and Other Angiosperm Lineages Yang, Yau-Wen; Lai, Kun-Nan; Tai, Pon-Yean Journal of Molecular Evolution, Vol. 48, Issue 5 https://doi.org/10.1007/PL00006502	journal	May 1999
Isolation and properties of bacteria capable of high rates of β-galactosidase synthesis Horiuchi, Tadao; Tomizawa, Jun-Ichi; Novick, Aaron Biochimica et Biophysica Acta, Vol. 55, Issue 1-2 https://doi.org/10.1016/0006-3002(62)90941-1	journal	January 1962
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Recent duplication, domain accretion and the dynamic mutation of the human genome Eichler, Evan E. Trends in Genetics, Vol. 17, Issue 11 https://doi.org/10.1016/S0168-9525(01)02492-1	journal	November 2001
Evolution by gene duplication: an update Zhang, Jianzhi Trends in Ecology & Evolution, Vol. 18, Issue 6 https://doi.org/10.1016/S0169-5347(03)00033-8	journal	June 2003
Consequences of genome duplication Sémon, Marie; Wolfe, Kenneth H. Current Opinion in Genetics & Development, Vol. 17, Issue 6 https://doi.org/10.1016/j.gde.2007.09.007	journal	December 2007
Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events Bowers, John E.; Chapman, Brad A.; Rong, Junkang Nature, Vol. 422, Issue 6930 https://doi.org/10.1038/nature01521	journal	March 2003
The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus) Ming, Ray; Hou, Shaobin; Feng, Yun Nature, Vol. 452, Issue 7190 https://doi.org/10.1038/nature06856	journal	April 2008
Nucleotide sequence of a mutant eukaryotic gene: the yeast tyrosine-inserting ochre suppressor SUP4-o. Goodman, H. M.; Olson, M. V.; Hall, B. D. Proceedings of the National Academy of Sciences, Vol. 74, Issue 12 https://doi.org/10.1073/pnas.74.12.5453	journal	December 1977
MODELTEST: testing the model of DNA substitution Posada, D.; Crandall, K. A. Bioinformatics, Vol. 14, Issue 9 https://doi.org/10.1093/bioinformatics/14.9.817	journal	October 1998
MrBayes 3: Bayesian phylogenetic inference under mixed models Ronquist, Fredrik; Huelsenbeck, John P. Bioinformatics, Vol. 19, Issue 12, p. 1572-1574 https://doi.org/10.1093/bioinformatics/btg180	journal	August 2003
Preservation of Duplicate Genes by Complementary, Degenerative Mutations Force, Allan; Lynch, Michael; Pickett, F. Bryan Genetics, Vol. 151, Issue 4 https://doi.org/10.1093/genetics/151.4.1531	journal	April 1999
Genome-Level Evolution of Resistance Genes in Arabidopsis thaliana Baumgarten, Andrew; Cannon, Steven; Spangler, Russ Genetics, Vol. 165, Issue 1 https://doi.org/10.1093/genetics/165.1.309	journal	September 2003
CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Thompson, Julie D.; Higgins, Desmond G.; Gibson, Toby J. Nucleic Acids Research, Vol. 22, Issue 22, p. 4673-4680 https://doi.org/10.1093/nar/22.22.4673	journal	January 1994
How to usefully compare homologous plant genes and chromosomes as DNA sequences: How to usefully compare plant genomes Lyons, Eric; Freeling, Michael The Plant Journal, Vol. 53, Issue 4 https://doi.org/10.1111/j.1365-313X.2007.03326.x	journal	February 2008
Evolution of repeated DNA sequences by unequal crossover Smith, G. Science, Vol. 191, Issue 4227 https://doi.org/10.1126/science.1251186	journal	February 1976
Meiotic Recombination Between Paralogous RBCSB Genes on Sister Chromatids of Arabidopsis thaliana Jelesko, John G.; Carter, Kristy; Thompson, Whitney Genetics, Vol. 166, Issue 2 https://doi.org/10.1534/genetics.166.2.947	journal	February 2004
Genome evolution among cruciferous plants: a lecture from the comparison of the genetic maps of three diploid species--Capsella rubella, Arabidopsis lyrata subsp. petraea, and A. thaliana Koch, M. A.; Kiefer, M. American Journal of Botany, Vol. 92, Issue 4 https://doi.org/10.3732/ajb.92.4.761	journal	April 2005

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Whole Genome and Tandem Duplicate Retention Facilitated Glucosinolate Pathway Diversification in the Mustard Family Hofberger, Johannes A.; Lyons, Eric; Edger, Patrick P. Genome Biology and Evolution, Vol. 5, Issue 11 https://doi.org/10.1093/gbe/evt162	journal	October 2013
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