Patching gaps in plant genomes results in gene movement and erosion of colinearity.

Colinearity of genes in plant genomes generally decreases with increasing evolutionary distance while the actual number of genes remains more or less constant. To characterize the molecular mechanisms of this "gene movement," we identified non-colinear genes by three-way comparison of the genomes of Brachypodium, rice, and sorghum. We found that genomic fragments of up to 50 kb containing the non-colinear genes are duplicated to acceptor sites elsewhere in the genome. Apparent movement of genes may usually be the result of subsequent deletions of genes in the donor region. Often, the duplicated fragments are precisely bordered by transposable elements (TEs) at the acceptor site. Highly diagnostic sequence motifs at these borders strongly suggest that these gene movements were the result of double-strand break (DSB) repair through synthesis-dependent strand annealing. In these cases, a copy of the foreign DNA fragment is used as filler DNA to repair the DSB linked with the transposition of TEs. Interestingly, most TEs we found associated with gene movement have a very low copy number in the genome and for several we did not find autonomous copies. This suggests that some of these elements spontaneously arose from unspecific interaction with TE proteins that are encoded by autonomous elements. Additionally, we found evidence that gene movements can also be caused when DSBs are repaired after template slippage or unequal crossing-over events. The observed frequency of gene movements can explain the erosion of gene colinearity between plant genomes during evolution.

[1]  G. Gloor,et al.  Efficient copying of nonhomologous sequences from ectopic sites via P-element-induced gap repair , 1994, Molecular and cellular biology.

[2]  J. Jurka,et al.  Helitrons on a roll: eukaryotic rolling-circle transposons. , 2007, Trends in genetics : TIG.

[3]  Jianxin Ma,et al.  Rapid recent growth and divergence of rice nuclear genomes. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[4]  D. Leister.  Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance gene. , 2004, Trends in genetics : TIG.

[5]  Joachim Messing,et al.  Gene movement by Helitron transposons contributes to the haplotype variability of maize. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Dawn H. Nagel,et al.  The B73 Maize Genome: Complexity, Diversity, and Dynamics , 2009, Science.

[7]  Joachim Messing,et al.  Reconstruction of monocotelydoneous proto-chromosomes reveals faster evolution in plants than in animals , 2009, Proceedings of the National Academy of Sciences.

[8]  S. Lovett.  Encoded errors: mutations and rearrangements mediated by misalignment at repetitive DNA sequences , 2004, Molecular microbiology.

[9]  V. Gorbunova,et al.  How plants make ends meet: DNA double-strand break repair. , 1999, Trends in plant science.

[10]  Contrasting Rates of Evolution in Pm3 Loci From Three Wheat Species and Rice , 2007, Genetics.

[11]  J. Bennetzen,et al.  Transposable elements, genes and recombination in a 215-kb contig from wheat chromosome 5Am , 2002, Functional & Integrative Genomics.

[12]  Beat Keller,et al.  CACTA Transposons in Triticeae. A Diverse Family of High-Copy Repetitive Elements1 , 2003, Plant Physiology.

[13]  M. Gouy,et al.  Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[14]  D. Petrov.  Evolution of genome size: new approaches to an old problem. , 2001, Trends in genetics : TIG.

[15]  Sai Guna Ranjan Gurazada,et al.  Genome sequencing and analysis of the model grass Brachypodium distachyon , 2010, Nature.

[16]  N. Vinckenbosch,et al.  RNA-based gene duplication: mechanistic and evolutionary insights , 2009, Nature Reviews Genetics.

[17]  Charaf Benarafa,et al.  The ovalbumin serpins revisited: perspective from the chicken genome of clade B serpin evolution in vertebrates. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Pavel A Pevzner,et al.  Mammalian phylogenomics comes of age. , 2004, Trends in genetics : TIG.

[19]  T. Wicker,et al.  Rapid Genome Divergence at Orthologous Low Molecular Weight Glutenin Loci of the A and A m Genomes of Wheat , 2003 .

[20]  M. Morgante,et al.  Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize , 2005, Nature Genetics.

[21]  A. Nicolas,et al.  Meiotic instability of human minisatellite CEB1 in yeast requires DNA double-strand breaks , 1999, Nature Genetics.

[22]  R. Durbin,et al.  A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. , 1995, Gene.

[23]  Mihaela M. Martis,et al.  The Sorghum bicolor genome and the diversification of grasses , 2009, Nature.

[24]  James K. M. Brown,et al.  Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. , 2002, Genome research.

[25]  Sean R. Eddy,et al.  Pack-MULE transposable elements mediate gene evolution in plants , 2004, Nature.

[26]  J. Bennetzen,et al.  Integration and nonrandom mutation of a plasma membrane proton ATPase gene fragment within the Bs1 retroelement of maize. , 1994, The Plant cell.

[27]  K. Devos,et al.  Comparative genetics in the grasses. , 1998, Plant molecular biology.

[28]  M. Kupiec,et al.  Analysis of repair mechanism choice during homologous recombination , 2009, Nucleic acids research.

[29]  Ralph Scully,et al.  Mechanisms of double-strand break repair in somatic mammalian cells. , 2009, The Biochemical journal.

[30]  H. Puchta.  The repair of double-strand breaks in plants: mechanisms and consequences for genome evolution. , 2004, Journal of experimental botany.

[31]  W. Goedecke,et al.  Mechanisms of DNA double-strand break repair and their potential to induce chromosomal aberrations. , 2000, Mutagenesis.

[32]  Phillip SanMiguel,et al.  The paleontology of intergene retrotransposons of maize , 1998, Nature Genetics.

[33]  Wen-Hsiung Li,et al.  Rates of Nucleotide Substitution in Angiosperm Mitochondrial DNA Sequences and Dates of Divergence Between Brassica and Other Angiosperm Lineages , 1999, Journal of Molecular Evolution.

[34]  Haibao Tang,et al.  Angiosperm genome comparisons reveal early polyploidy in the monocot lineage , 2009, Proceedings of the National Academy of Sciences.

[35]  H. Puchta,et al.  Species‐specific double‐strand break repair and genome evolution in plants , 2000, The EMBO journal.

[36]  Takuji Sasaki,et al.  The map-based sequence of the rice genome , 2005, Nature.