Uneven chromosome contraction and expansion in the maize genome.

Maize (Zea mays or corn), both a major food source and an important cytogenetic model, evolved from a tetraploid that arose about 4.8 million years ago (Mya). As a result, maize has extensive duplicated regions within its genome. We have sequenced the two copies of one such region, generating 7.8 Mb of sequence spanning 17.4 cM of the short arm of chromosome 1 and 6.6 Mb (25.6 cM) from the long arm of chromosome 9. Rice, which did not undergo a similar whole genome duplication event, has only one orthologous region (4.9 Mb) on the short arm of chromosome 3, and can be used as reference for the maize homoeologous regions. Alignment of the three regions allowed identification of syntenic blocks, and indicated that the maize regions have undergone differential contraction in genic and intergenic regions and expansion by the insertion of retrotransposable elements. Approximately 9% of the predicted genes in each duplicated region are completely missing in the rice genome, and almost 20% have moved to other genomic locations. Predicted genes within these regions tend to be larger in maize than in rice, primarily because of the presence of predicted genes in maize with larger introns. Interestingly, the general gene methylation patterns in the maize homoeologous regions do not appear to have changed with contraction or expansion of their chromosomes. In addition, no differences in methylation of single genes and tandemly repeated gene copies have been detected. These results, therefore, provide new insights into the diploidization of polyploid species.

[1]  C. Town.  Annotating the genome of Medicago truncatula. , 2006, Current opinion in plant biology.

[2]  B. Gaut,et al.  Uneven distribution of expressed sequence tag loci on maize pachytene chromosomes. , 2005, Genome research.

[3]  B. Birren,et al.  Structure and Architecture of the Maize Genome1[W] , 2005, Plant Physiology.

[4]  Gordon Gremme,et al.  Engineering a software tool for gene structure prediction in higher organisms , 2005, Inf. Softw. Technol..

[5]  David J. Chen,et al.  Homologous recombination and nonhomologous end-joining repair pathways regulate fragile site stability. , 2005, Genes & development.

[6]  Rod A Wing,et al.  Sequence, annotation, and analysis of synteny between rice chromosome 3 and diverged grass species. , 2005, Genome research.

[7]  Galina Fuks,et al.  Whole-Genome Validation of High-Information-Content Fingerprinting1 , 2005, Plant Physiology.

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

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

[10]  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.

[11]  Xiaohong Wang,et al.  Databases and Information Integration for the Medicago truncatula Genome and Transcriptome1 , 2005, Plant Physiology.

[12]  B. Roe,et al.  Sequencing the Genespaces of Medicago truncatula and Lotus japonicus1 , 2005, Plant Physiology.

[13]  Andy Pereira,et al.  Faculty Opinions recommendation of Evolution of DNA sequence nonhomologies among maize inbreds. , 2005 .

[14]  J. Bennetzen,et al.  Mechanisms of recent genome size variation in flowering plants. , 2005, Annals of botany.

[15]  Jianxin Ma,et al.  Consistent over-estimation of gene number in complex plant genomes. , 2004, Current opinion in plant biology.

[16]  E. Lander,et al.  Finishing the euchromatic sequence of the human genome , 2004 .

[17]  J. Bonfield,et al.  Finishing the euchromatic sequence of the human genome , 2004, Nature.

[18]  R. Wing,et al.  Sequence composition and genome organization of maize. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Nathan M. Springer,et al.  Utility of Different Gene Enrichment Approaches Toward Identifying and Sequencing the Maize Gene Space1[w] , 2004, Plant Physiology.

[20]  Jianxin Ma,et al.  Close split of sorghum and maize genome progenitors. , 2004, Genome research.

[21]  B. Larkins,et al.  Characterization of the maize endosperm transcriptome and its comparison to the rice genome. , 2004, Genome research.

[22]  J. Bennetzen,et al.  Gene loss and movement in the maize genome. , 2004, Genome research.

[23]  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.

[24]  P. Schnable,et al.  Types and Frequencies of Sequencing Errors in Methyl-Filtered and High C0t Maize Genome Survey Sequences1[w] , 2004, Plant Physiology.

[25]  Jianxin Ma,et al.  Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. , 2004, Genome research.

[26]  B. Birren,et al.  Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae , 2004, Nature.

[27]  Steven G. Schroeder,et al.  Anchoring 9,371 Maize Expressed Sequence Tagged Unigenes to the Bacterial Artificial Chromosome Contig Map by Two-Dimensional Overgo Hybridization1 , 2004, Plant Physiology.

[28]  Joachim Messing,et al.  Pattern of diversity in the genomic region near the maize domestication gene tb1. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[29]  D. Grant,et al.  Expanding the genetic map of maize with the intermated B73 × Mo17 (IBM) population , 2002, Plant Molecular Biology.

[30]  J. Messing,et al.  Endosperm-specific demethylation and activation of specific alleles of α-tubulin genes of Zea mays L. , 1995, Molecular and General Genetics MGG.

[31]  J. Bennetzen,et al.  Structure and evolution of the r/b chromosomal regions in rice, maize, and sorghum , 2004 .

[32]  J Quackenbush,et al.  Enrichment of Gene-Coding Sequences in Maize by Genome Filtration , 2003, Science.

[33]  S. Dike,et al.  Maize Genome Sequencing by Methylation Filtration , 2003, Science.

[34]  J. Bennetzen,et al.  A complex history of rearrangement in an orthologous region of the maize, sorghum, and rice genomes , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Junhua Peng,et al.  Comparative DNA sequence analysis of wheat and rice genomes. , 2003, Genome research.

[36]  Joachim Messing,et al.  Gene expression of a gene family in maize based on noncollinear haplotypes , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Junhua Peng,et al.  The organization and rate of evolution of wheat genomes are correlated with recombination rates along chromosome arms. , 2003, Genome research.

[38]  Ilia J. Leitch,et al.  Comparisons with Caenorhabditis (∼100 Mb) and Drosophila (∼175 Mb) Using Flow Cytometry Show Genome Size in Arabidopsis to be ∼157 Mb and thus ∼25 % Larger than the Arabidopsis Genome Initiative Estimate of ∼125 Mb , 2003 .

[39]  Yinan Yuan,et al.  High-Cot sequence analysis of the maize genome. , 2003, The Plant journal : for cell and molecular biology.

[40]  Volker Brendel,et al.  The Maize Genome Contains a Helitron Insertion Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.008375. , 2003, The Plant Cell Online.

[41]  Ilia J Leitch,et al.  Comparisons with Caenorhabditis (approximately 100 Mb) and Drosophila (approximately 175 Mb) using flow cytometry show genome size in Arabidopsis to be approximately 157 Mb and thus approximately 25% larger than the Arabidopsis genome initiative estimate of approximately 125 Mb. , 2003, Annals of botany.

[42]  E. Mauceli,et al.  Whole-genome sequence assembly for mammalian genomes: Arachne 2. , 2003, Genome research.

[43]  Ngozi A. Duru,et al.  Characterization of Three Maize Bacterial Artificial Chromosome Libraries toward Anchoring of the Physical Map to the Genetic Map Using High-Density Bacterial Artificial Chromosome Filter Hybridization1 , 2002, Plant Physiology.

[44]  J. Messing,et al.  Mosaic organization of orthologous sequences in grass genomes. , 2002, Genome research.

[45]  J. Bennetzen,et al.  The regulatory regions required for B' paramutation and expression are located far upstream of the maize b1 transcribed sequences. , 2002, Genetics.

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

[47]  H. Fu,et al.  Intraspecific violation of genetic colinearity and its implications in maize , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[48]  Guang R. Gao,et al.  TROLL-Tandem Repeat Occurrence Locator , 2002, Bioinform..

[49]  H. Kotani,et al.  Physical map-based sizes of the centromeric regions of Arabidopsis thaliana chromosomes 1, 2, and 3. , 2002, DNA research : an international journal for rapid publication of reports on genes and genomes.

[50]  B. Berger,et al.  ARACHNE: a whole-genome shotgun assembler. , 2002, Genome research.

[51]  Joachim Messing,et al.  Sequence, Regulation, and Evolution of the Maize 22-kD α Zein Gene Family , 2001 .

[52]  M. Morgante,et al.  Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome. , 2001, Genome research.

[53]  J. Jurka,et al.  Rolling-circle transposons in eukaryotes , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[54]  K. H. Wolfe.  Yesterday's polyploids and the mystery of diploidization , 2001, Nature Reviews Genetics.

[55]  The Arabidopsis Genome Initiative.  Analysis of the genome sequence of the flowering plant Arabidopsis thaliana , 2000, Nature.

[56]  V. Solovyev,et al.  Ab initio gene finding in Drosophila genomic DNA. , 2000, Genome research.

[57]  S. Wessler,et al.  Recent, extensive, and preferential insertion of members of the miniature inverted-repeat transposable element family Heartbreaker into genic regions of maize. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[58]  Robert A. Martienssen,et al.  Differential methylation of genes and retrotransposons facilitates shotgun sequencing of the maize genome , 1999, Nature Genetics.

[59]  J. Bennetzen,et al.  Colinearity and its exceptions in orthologous adh regions of maize and sorghum. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

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

[61]  M. Borodovsky,et al.  GeneMark.hmm: new solutions for gene finding. , 1998, Nucleic acids research.

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

[63]  S. Wessler,et al.  LTR-retrotransposons and MITEs: important players in the evolution of plant genomes. , 1995, Current opinion in genetics & development.

[64]  J. Messing,et al.  Tissue-specific DNase l-sensitive sites of the maize P gene and their changes upon epimutation. , 1995, The Plant Journal.

[65]  J. Bennetzen,et al.  Active maize genes are unmodified and flanked by diverse classes of modified, highly repetitive DNA. , 1994, Genome.

[66]  J. Messing,et al.  Variegated phenotype and developmental methylation changes of a maize allele originating from epimutation. , 1994, Genetics.

[67]  D. Bullock,et al.  Nuclear DNA content in F1 hybrids of maize , 1993, Heredity.

[68]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[69]  B. Burr,et al.  Gene mapping with recombinant inbreds in maize. , 1988, Genetics.

[70]  S. Wessler,et al.  Inactivation of the maize transposable element Activator (Ac) is associated with its DNA modification. , 1987, The EMBO journal.

[71]  V. Pirrotta,et al.  Two adjacent genomic zein sequences: structure, organization and tissue-specific restriction pattern. , 1983, Journal of molecular biology.

[72]  J. Vieira,et al.  The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. , 1982, Gene.

[73]  P. Thuriaux.  Is recombination confined to structural genes on the eukaryotic genome? , 1977, Nature.

[74]  C. A. Thomas.  The genetic organization of chromosomes. , 1971, Annual review of genetics.

[75]  M. Rhoades.  Duplicate Genes in Maize , 1951, The American Naturalist.

[76]  B. Mcclintock.  A CYTOLOGICAL DEMONSTRATION OF THE LOCATION OF AN INTERCHANGE BETWEEN TWO NON-HOMOLOGOUS CHROMOSOMES OF ZEA MAYS. , 1930, Proceedings of the National Academy of Sciences of the United States of America.