Ancestral grass karyotype reconstruction unravels new mechanisms of genome shuffling as a source of plant evolution.

The comparison of the chromosome numbers of today's species with common reconstructed paleo-ancestors has led to intense speculation of how chromosomes have been rearranged over time in mammals. However, similar studies in plants with respect to genome evolution as well as molecular mechanisms leading to mosaic synteny blocks have been lacking due to relevant examples of evolutionary zooms from genomic sequences. Such studies require genomes of species that belong to the same family but are diverged to fall into different subfamilies. Our most important crops belong to the family of the grasses, where a number of genomes have now been sequenced. Based on detailed paleogenomics, using inference from n = 5-12 grass ancestral karyotypes (AGKs) in terms of gene content and order, we delineated sequence intervals comprising a complete set of junction break points of orthologous regions from rice, maize, sorghum, and Brachypodium genomes, representing three different subfamilies and different polyploidization events. By focusing on these sequence intervals, we could show that the chromosome number variation/reduction from the n = 12 common paleo-ancestor was driven by nonrandom centric double-strand break repair events. It appeared that the centromeric/telomeric illegitimate recombination between nonhomologous chromosomes led to nested chromosome fusions (NCFs) and synteny break points (SBPs). When intervals comprising NCFs were compared in their structure, we concluded that SBPs (1) were meiotic recombination hotspots, (2) corresponded to high sequence turnover loci through repeat invasion, and (3) might be considered as hotspots of evolutionary novelty that could act as a reservoir for producing adaptive phenotypes.

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

[2]  Francesca Antonacci,et al.  Evolutionary Formation of New Centromeres in Macaque , 2007, Science.

[3]  Martin Charles Golumbic,et al.  Complexity and Algorithms for Graph and Hypergraph Sandwich Problems , 1998, Graphs Comb..

[4]  F. Han,et al.  High frequency of centromere inactivation resulting in stable dicentric chromosomes of maize. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[5]  George W. Bell,et al.  Mapping of Meiotic Single-Stranded DNA Reveals Double-Strand-Break Hotspots near Centromeres and Telomeres , 2007, Current Biology.

[6]  Shreedhar Natarajan,et al.  A 1463 gene cattle-human comparative map with anchor points defined by human genome sequence coordinates. , 2004, Genome research.

[7]  Jérôme Gouzy,et al.  Narcisse: a mirror view of conserved syntenies , 2007, Nucleic Acids Res..

[8]  Miftahudin,et al.  A Chromosome Bin Map of 16,000 Expressed Sequence Tag Loci and Distribution of Genes Among the Three Genomes of Polyploid Wheat , 2004, Genetics.

[9]  M. Lysak,et al.  Chromosomal Phylogeny and Karyotype Evolution in x=7 Crucifer Species (Brassicaceae)[W] , 2008, The Plant Cell Online.

[10]  Haibao Tang,et al.  Unraveling ancient hexaploidy through multiply-aligned angiosperm gene maps. , 2008, Genome research.

[11]  Jan P. Buchmann,et al.  Patching gaps in plant genomes results in gene movement and erosion of colinearity. , 2010, Genome research.

[12]  Brandon S. Gaut,et al.  Evolutionary dynamics of grass genomes , 2002 .

[13]  A. Baldini,et al.  Improved telomere detection using a telomere repeat probe (TTAGGG)n generated by PCR. , 1991, Nucleic acids research.

[14]  Phil Trinh,et al.  Genomic features in the breakpoint regions between syntenic blocks , 2004, ISMB/ECCB.

[15]  A. Paterson,et al.  Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Eric Tannier.  Yeast Ancestral Genome Reconstructions: The Possibilities of Computational Methods , 2009, RECOMB-CG.

[17]  J. Messing,et al.  Diverged copies of the seed regulatory Opaque-2 gene by a segmental duplication in the progenitor genome of rice, sorghum, and maize. , 2008, Molecular plant.

[18]  E. Kellogg,et al.  Evolutionary history of the grasses. , 2001, Plant physiology.

[19]  G. Marais,et al.  Biased gene conversion: implications for genome and sex evolution. , 2003, Trends in genetics : TIG.

[20]  K. McBreen,et al.  Mechanisms of chromosome number reduction in Arabidopsis thaliana and related Brassicaceae species. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[21]  J. Bennetzen,et al.  Evolutionary History and Positional Shift of a Rice Centromere , 2007, Genetics.

[22]  R. Bicknell,et al.  Understanding Apomixis: Recent Advances and Remaining Conundrums , 2004, The Plant Cell Online.

[23]  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.

[24]  B. Mcclintock.  The Behavior in Successive Nuclear Divisions of a Chromosome Broken at Meiosis. , 1939, Proceedings of the National Academy of Sciences of the United States of America.

[25]  W. Jin,et al.  Centromere repositioning in cucurbit species: Implication of the genomic impact from centromere activation and inactivation , 2009, Proceedings of the National Academy of Sciences.

[26]  S. Hiscock,et al.  Polyploidy: Doubling up for Evolutionary Success , 2007, Current Biology.

[27]  J. Messing,et al.  The 'inner circle' of the cereal genomes. , 2009, Current opinion in plant biology.

[28]  J. Messing,et al.  Amplification of prolamin storage protein genes in different subfamilies of the Poaceae , 2009, Theoretical and Applied Genetics.

[29]  D. Hoisington,et al.  Comparative Map and Trait Viewer (CMTV): an integrated bioinformatic tool to construct consensus maps and compare QTL and functional genomics data across genomes and experiments , 2004, Plant Molecular Biology.

[30]  Jaroslav Opatrny,et al.  Total Ordering Problem , 1979, SIAM J. Comput..

[31]  Agnes P Chan,et al.  Uneven chromosome contraction and expansion in the maize genome. , 2006, Genome research.

[32]  F. Piras,et al.  Uncoupling of Satellite DNA and Centromeric Function in the Genus Equus , 2010, PLoS genetics.

[33]  J. Salse,et al.  Identification and Characterization of Shared Duplications between Rice and Wheat Provide New Insight into Grass Genome Evolution[W] , 2008, The Plant Cell Online.

[34]  Hélène Hayes,et al.  High-resolution comparative mapping among man, cattle and mouse suggests a role for repeat sequences in mammalian genome evolution , 2006, BMC Genomics.

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

[36]  Cédric Chauve,et al.  A Methodological Framework for the Reconstruction of Contiguous Regions of Ancestral Genomes and Its Application to Mammalian Genomes , 2008, PLoS Comput. Biol..

[37]  Joachim Messing,et al.  Change of Gene Structure and Function by Non-Homologous End-Joining, Homologous Recombination, and Transposition of DNA , 2009, PLoS genetics.

[38]  J. Messing,et al.  Organization of the prolamin gene family provides insight into the evolution of the maize genome and gene duplications in grass species , 2008, Proceedings of the National Academy of Sciences.

[39]  Jérôme Salse,et al.  Improved criteria and comparative genomics tool provide new insights into grass paleogenomics , 2009, Briefings Bioinform..

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

[41]  Marie-France Sagot,et al.  Analysis of fine-scale mammalian evolutionary breakpoints provides new insight into their relation to genome organisation , 2009 .

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

[43]  M T Clegg,et al.  Genome comparisons reveal a dominant mechanism of chromosome number reduction in grasses and accelerated genome evolution in Triticeae , 2009, Proceedings of the National Academy of Sciences.

[44]  Owen J. Marshall,et al.  Neocentromeres: new insights into centromere structure, disease development, and karyotype evolution. , 2008, American journal of human genetics.

[45]  Pierre Sourdille,et al.  Molecular Basis of Evolutionary Events That Shaped the Hardness Locus in Diploid and Polyploid Wheat Species (Triticum and Aegilops)w⃞ , 2005, The Plant Cell Online.

[46]  A. Meyer,et al.  The evolutionary significance of ancient genome duplications , 2009, Nature Reviews Genetics.

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

[48]  J. Salse,et al.  Structure and expression analysis of rice paleo duplications , 2008, Nucleic acids research.

[49]  Ryan A. Rapp,et al.  Evolutionary genetics of genome merger and doubling in plants. , 2008, Annual review of genetics.

[50]  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.

[51]  P. Pevzner,et al.  Dynamics of Mammalian Chromosome Evolution Inferred from Multispecies Comparative Maps , 2005, Science.

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

[53]  Loretta Auvil,et al.  Breakpoint regions and homologous synteny blocks in chromosomes have different evolutionary histories. , 2009, Genome research.

[54]  R. O’Neill,et al.  Species-specific shifts in centromere sequence composition are coincident with breakpoint reuse in karyotypically divergent lineages , 2007, Genome Biology.

[55]  K. Choo,et al.  Human centromere repositioning "in progress". , 2004, Proceedings of the National Academy of Sciences of the United States of America.

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

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