Unlocking the Barley Genome by Chromosomal and Comparative Genomics[W][OA]

Survey sequence and array hybridization data from flow-sorted barley chromosomes were integrated using a comparative genomics model to define an ordered gene map of the barley genome that contains approximately two-thirds of its estimated 32000 genes. The resulting high-resolution framework facilitated a genome-wide structural analysis of the barley genome and a detailed comparative analysis with wheat. We used a novel approach that incorporated chromosome sorting, next-generation sequencing, array hybridization, and systematic exploitation of conserved synteny with model grasses to assign ~86% of the estimated ~32,000 barley (Hordeum vulgare) genes to individual chromosome arms. Using a series of bioinformatically constructed genome zippers that integrate gene indices of rice (Oryza sativa), sorghum (Sorghum bicolor), and Brachypodium distachyon in a conserved synteny model, we were able to assemble 21,766 barley genes in a putative linear order. We show that the barley (H) genome displays a mosaic of structural similarity to hexaploid bread wheat (Triticum aestivum) A, B, and D subgenomes and that orthologous genes in different grasses exhibit signatures of positive selection in different lineages. We present an ordered, information-rich scaffold of the barley genome that provides a valuable and robust framework for the development of novel strategies in cereal breeding.

[1]  Miftahudin,et al.  Analysis of Expressed Sequence Tag Loci on Wheat Chromosome Group 4 , 2004, Genetics.

[2]  Joachim Messing,et al.  Ancestral grass karyotype reconstruction unravels new mechanisms of genome shuffling as a source of plant evolution. , 2010, Genome research.

[3]  P. Schulze-Lefert,et al.  Cell-Autonomous Expression of Barley Mla1 Confers Race-Specific Resistance to the Powdery Mildew Fungus via a Rar1-Independent Signaling Pathway , 2001, Plant Cell.

[4]  M T Clegg,et al.  Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[5]  R. Haselkorn,et al.  Genes encoding plastid acetyl-CoA carboxylase and 3-phosphoglycerate kinase of the Triticum/Aegilops complex and the evolutionary history of polyploid wheat , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[6]  J. Doležel,et al.  High-resolution flow karyotyping and chromosome sorting in Vicia faba lines with standard and reconstructed karyotypes , 1995, Theoretical and Applied Genetics.

[7]  M. Nei,et al.  Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. , 1986, Molecular biology and evolution.

[8]  Andreas Graner,et al.  454 sequencing put to the test using the complex genome of barley , 2006, BMC Genomics.

[9]  D. Laurie,et al.  The Pseudo-Response Regulator Ppd-H1 Provides Adaptation to Photoperiod in Barley , 2005, Science.

[10]  Robbie Waugh,et al.  Gene expression quantitative trait locus analysis of 16 000 barley genes reveals a complex pattern of genome-wide transcriptional regulation. , 2008, The Plant journal : for cell and molecular biology.

[11]  Grégoire M. Hummel,et al.  NaRALF, a peptide signal essential for the regulation of root hair tip apoplastic pH in Nicotiana attenuata, is required for root hair development and plant growth in native soils. , 2007, The Plant journal : for cell and molecular biology.

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

[13]  K. Takeda,et al.  A high-density transcript linkage map of barley derived from a single population , 2009, Heredity.

[14]  Detlef Weigel,et al.  SHOREmap: simultaneous mapping and mutation identification by deep sequencing , 2009, Nature Methods.

[15]  M. Platzer,et al.  A whole-genome snapshot of 454 sequences exposes the composition of the barley genome and provides evidence for parallel evolution of genome size in wheat and barley. , 2009, The Plant journal : for cell and molecular biology.

[16]  H. Germain,et al.  Characterization of five RALF-like genes from Solanum chacoense provides support for a developmental role in plants , 2004, Planta.

[17]  G. Kahl,et al.  Development of flow cytogenetics and physical genome mapping in chickpea (Cicer arietinum L.) , 2004, Chromosome Research.

[18]  S. Dudoit,et al.  Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. , 2002, Nucleic acids research.

[19]  E. Lander,et al.  Genomic mapping by fingerprinting random clones: a mathematical analysis. , 1988, Genomics.

[20]  Uwe Scholz,et al.  Gene Content and Virtual Gene Order of Barley Chromosome 1H1[C][W][OA] , 2009, Plant Physiology.

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

[22]  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.

[23]  L. Qi,et al.  Complex genome rearrangements reveal evolutionary dynamics of pericentromeric regions in the Triticeae. , 2006, Genome.

[24]  Jean-Luc Jannink,et al.  The emergence of whole genome association scans in barley. , 2009, Current opinion in plant biology.

[25]  Joachim Messing,et al.  Palaeogenomics of plants: synteny-based modelling of extinct ancestors. , 2010, Trends in plant science.

[26]  Xiaowu Wang,et al.  Cloning and expression analysis of a pollen preferential rapid alkalinization factor gene, BoRALF1, from broccoli flowers , 2010, Molecular Biology Reports.

[27]  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.

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

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

[30]  Ruben P. Jolie,et al.  Pectin methylesterase and its proteinaceous inhibitor: a review. , 2010, Carbohydrate research.

[31]  I. Somssich,et al.  The wheat Mla homologue TmMla1 exhibits an evolutionarily conserved function against powdery mildew in both wheat and barley. , 2011, The Plant journal : for cell and molecular biology.

[32]  I. Leitch,et al.  Nuclear DNA Amounts in Angiosperms , 1995 .

[33]  Hiroaki Sakai,et al.  Comprehensive Sequence Analysis of 24,783 Barley Full-Length cDNAs Derived from 12 Clone Libraries1[W][OA] , 2011, Plant Physiology.

[34]  Ute Baumann,et al.  An atlas of gene expression from seed to seed through barley development , 2006, Functional & Integrative Genomics.

[35]  R. Haselkorn,et al.  Phylogenetic analysis of the acetyl-CoA carboxylase and 3-phosphoglycerate kinase loci in wheat and other grasses , 2002, Plant Molecular Biology.

[36]  M. Morgante,et al.  Genetic Dissection of Barley Morphology and Development1[W][OA] , 2010, Plant Physiology.

[37]  J. Doležel,et al.  Analysis and sorting of rye (Secale cereale L.) chromosomes using flow cytometry. , 2003, Genome.

[38]  J. Macas,et al.  Chromosome Sorting and PCR-Based Physical Mapping in Pea (Pisum Sativum L.) , 2004, Chromosome Research.

[39]  K. Devos Updating the 'crop circle'. , 2005, Current opinion in plant biology.

[40]  L. Xiong,et al.  A genome-wide survey of HD-Zip genes in rice and analysis of drought-responsive family members , 2007, Plant Molecular Biology.

[41]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[42]  I. Grosse,et al.  A 1,000-loci transcript map of the barley genome: new anchoring points for integrative grass genomics , 2007, Theoretical and Applied Genetics.

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

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

[45]  L. Yan,et al.  The wheat and barley vernalization gene VRN3 is an orthologue of FT , 2006, Proceedings of the National Academy of Sciences.

[46]  G. Segal,et al.  Rapid elimination of low-copy DNA sequences in polyploid wheat: a possible mechanism for differentiation of homoeologous chromosomes. , 1997, Genetics.

[47]  L Nardi,et al.  Plant Genome Size Estimation by Flow Cytometry: Inter-laboratory Comparison , 1998 .

[48]  Dawei Li,et al.  The sequence and de novo assembly of the giant panda genome , 2010, Nature.

[49]  Francois Sabot,et al.  Low-pass shotgun sequencing of the barley genome facilitates rapid identification of genes, conserved non-coding sequences and novel repeats , 2008, BMC Genomics.

[50]  J. Doležel,et al.  Dissection of the nuclear genome of barley by chromosome flow sorting , 2006, Theoretical and Applied Genetics.

[51]  Ziheng Yang PAML 4: phylogenetic analysis by maximum likelihood. , 2007, Molecular biology and evolution.

[52]  A. Meister,et al.  Cytologically integrated physical restriction fragment length polymorphism maps for the barley genome based on translocation breakpoints. , 2000, Genetics.

[53]  Hikmet Budak,et al.  Megabase Level Sequencing Reveals Contrasted Organization and Evolution Patterns of the Wheat Gene and Transposable Element Spaces[W] , 2010, Plant Cell.

[54]  D. Laurie,et al.  A Pseudo-Response Regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat (Triticum aestivum L.) , 2007, Theoretical and Applied Genetics.

[55]  Kazuo Shinozaki,et al.  Development of 5006 Full-Length CDNAs in Barley: A Tool for Accessing Cereal Genomics Resources , 2009, DNA research : an international journal for rapid publication of reports on genes and genomes.

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

[57]  Rod A Wing,et al.  A New Resource for Cereal Genomics: 22K Barley GeneChip Comes of Age1 , 2004, Plant Physiology.

[58]  P. Langridge,et al.  The International Barley Sequencing Consortium—At the Threshold of Efficient Access to the Barley Genome1[W] , 2009, Plant Physiology.

[59]  I. Grosse,et al.  Evidence and evolutionary analysis of ancient whole-genome duplication in barley predating the divergence from rice , 2009, BMC Evolutionary Biology.

[60]  J. Doležel,et al.  Flow karyotyping and chromosome sorting in bread wheat (Triticum aestivum L.) , 2002, Theoretical and Applied Genetics.

[61]  M. Feldman,et al.  Sequence Elimination and Cytosine Methylation Are Rapid and Reproducible Responses of the Genome to Wide Hybridization and Allopolyploidy in Wheat , 2001, The Plant Cell Online.

[62]  G. Moore,et al.  Cereal Genome Evolution: Grasses, line up and form a circle , 1995, Current Biology.

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

[64]  B. Gill,et al.  A cytogenetic ladder-map of the wheat homoeologous group-4 chromosomes , 1995, Theoretical and Applied Genetics.

[65]  Pascal Condamine,et al.  Coupling amplified DNA from flow-sorted chromosomes to high-density SNP mapping in barley , 2008, BMC Genomics.

[66]  J. Anderson,et al.  Molecular mapping of wheat: major genes and rearrangements in homoeologous groups 4, 5, and 7. , 1995, Genetics.

[67]  Z. Chen,et al.  Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. , 2007, Annual review of plant biology.

[68]  Faye M. Rosin,et al.  Old dogs , new tricks : Regulatory evolution in conserved genetic modules leads to novel morphologies in plants , 2009 .

[69]  P. Hayes,et al.  Large deletions within the first intron in VRN-1 are associated with spring growth habit in barley and wheat , 2005, Molecular Genetics and Genomics.

[70]  Uwe Scholz,et al.  De novo 454 sequencing of barcoded BAC pools for comprehensive gene survey and genome analysis in the complex genome of barley , 2009 .

[71]  Stefano Lonardi,et al.  Development and implementation of high-throughput SNP genotyping in barley , 2009, BMC Genomics.

[72]  M. Feldman,et al.  Allopolyploidy-Induced Rapid Genome Evolution in the Wheat (Aegilops–Triticum) Group , 2001, The Plant Cell Online.