The genome of the recently domesticated crop plant sugar beet (Beta vulgaris)

Sugar beet (Beta vulgaris ssp. vulgaris) is an important crop of temperate climates which provides nearly 30% of the world’s annual sugar production and is a source for bioethanol and animal feed. The species belongs to the order of Caryophylalles, is diploid with 2n = 18 chromosomes, has an estimated genome size of 714–758 megabases and shares an ancient genome triplication with other eudicot plants. Leafy beets have been cultivated since Roman times, but sugar beet is one of the most recently domesticated crops. It arose in the late eighteenth century when lines accumulating sugar in the storage root were selected from crosses made with chard and fodder beet. Here we present a reference genome sequence for sugar beet as the first non-rosid, non-asterid eudicot genome, advancing comparative genomics and phylogenetic reconstructions. The genome sequence comprises 567 megabases, of which 85% could be assigned to chromosomes. The assembly covers a large proportion of the repetitive sequence content that was estimated to be 63%. We predicted 27,421 protein-coding genes supported by transcript data and annotated them on the basis of sequence homology. Phylogenetic analyses provided evidence for the separation of Caryophyllales before the split of asterids and rosids, and revealed lineage-specific gene family expansions and losses. We sequenced spinach (Spinacia oleracea), another Caryophyllales species, and validated features that separate this clade from rosids and asterids. Intraspecific genomic variation was analysed based on the genome sequences of sea beet (Beta vulgaris ssp. maritima; progenitor of all beet crops) and four additional sugar beet accessions. We identified seven million variant positions in the reference genome, and also large regions of low variability, indicating artificial selection. The sugar beet genome sequence enables the identification of genes affecting agronomically relevant traits, supports molecular breeding and maximizes the plant’s potential in energy biotechnology.

[1]  Richard Durbin,et al.  Sequence analysis Fast and accurate short read alignment with Burrows – Wheeler transform , 2009 .

[2]  T. Schmidt,et al.  A sugar beet (Beta vulgaris L.) reference FISH karyotype for chromosome and chromosome-arm identification, integration of genetic linkage groups and analysis of major repeat family distribution. , 2012, The Plant journal : for cell and molecular biology.

[3]  Bernd Weisshaar,et al.  Construction and characterization of a sugar beet (Beta vulgaris) fosmid library. , 2008, Genome.

[4]  Robert D. Finn,et al.  InterPro in 2011: new developments in the family and domain prediction database , 2011, Nucleic acids research.

[5]  E. Biancardi,et al.  Beta maritima: The Origin of Beets , 2011 .

[6]  Sang-Keun Oh,et al.  A genome-wide comparison of NB-LRR type of resistance gene analogs (RGA) in the plant kingdom , 2012, Molecules and cells.

[7]  Christian Jung,et al.  The Absence of TIR-Type Resistance Gene Analogues in the Sugar Beet (Beta vulgaris L.) Genome , 2003, Journal of Molecular Evolution.

[8]  Oliver Eulenstein,et al.  DupTree: a program for large-scale phylogenetic analyses using gene tree parsimony , 2008, Bioinform..

[9]  Alvaro J. González,et al.  The Medicago Genome Provides Insight into the Evolution of Rhizobial Symbioses , 2011, Nature.

[10]  Nathan M. Springer,et al.  Progress toward understanding heterosis in crop plants. , 2013, Annual review of plant biology.

[11]  S. Eddy,et al.  Automated de novo identification of repeat sequence families in sequenced genomes. , 2002, Genome research.

[12]  David Haussler,et al.  Using native and syntenically mapped cDNA alignments to improve de novo gene finding , 2008, Bioinform..

[13]  J. Lundberg,et al.  An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants : APG II THE ANGIOSPERM PHYLOGENY GROUP * , 2003 .

[14]  Christopher P. L. Grof,et al.  Sucrose transporters of higher plants. , 2010, Current opinion in plant biology.

[15]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[16]  E. D. Earle,et al.  Nuclear DNA content of some important plant species , 1991, Plant Molecular Biology Reporter.

[17]  Christian Jung,et al.  Analysis of DNA polymorphisms in sugar beet (Beta vulgaris L.) and development of an SNP-based map of expressed genes , 2007, Theoretical and Applied Genetics.

[18]  R. Soejono,et al.  Root & tuber crops , 1981 .

[19]  J. Dopazo,et al.  The human phylome , 2007, Genome Biology.

[20]  Christian Jung,et al.  The Role of a Pseudo-Response Regulator Gene in Life Cycle Adaptation and Domestication of Beet , 2012, Current Biology.

[21]  Sean R. Eddy,et al.  Rfam 11.0: 10 years of RNA families , 2012, Nucleic Acids Res..

[22]  J. G. Burleigh,et al.  Phylogenetic analysis of 83 plastid genes further resolves the early diversification of eudicots , 2010, Proceedings of the National Academy of Sciences.

[23]  J. Silberg,et al.  A transposase strategy for creating libraries of circularly permuted proteins , 2012, Nucleic acids research.

[24]  Volker Brendel,et al.  The ASRG database: identification and survey of Arabidopsis thaliana genes involved in pre-mRNA splicing , 2004, Genome Biology.

[25]  Jian Wang,et al.  SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler , 2012, GigaScience.

[26]  G. Benson,et al.  Tandem repeats finder: a program to analyze DNA sequences. , 1999, Nucleic acids research.

[27]  Pavel A. Pevzner,et al.  De novo identification of repeat families in large genomes , 2005, ISMB.

[28]  R. B. Flavell,et al.  Genome size and the proportion of repeated nucleotide sequence DNA in plants , 1974, Biochemical Genetics.

[29]  S. Eddy,et al.  tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. , 1997, Nucleic acids research.

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

[31]  O. Gascuel,et al.  New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. , 2010, Systematic biology.

[32]  Susumu Goto,et al.  KEGG for integration and interpretation of large-scale molecular data sets , 2011, Nucleic Acids Res..

[33]  Paul D. Shaw,et al.  Plant snoRNA database , 2003, Nucleic Acids Res..

[34]  Richard Reinhardt,et al.  Haplotype divergence in Beta vulgaris and microsynteny with sequenced plant genomes. , 2009, The Plant journal : for cell and molecular biology.

[35]  C. Jung,et al.  A bacterial artificial chromosome (BAC) library of sugar beet and a physical map of the region encompassing the bolting gene B , 2003, Molecular Genetics and Genomics.

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

[37]  Apgii.  An update of the angiosperm phylogeny group classification for the orders and families of flowering plants : APGII , 2003 .

[38]  Hans Eberhard Fischer,et al.  Origin of the ‘Weisse Schlesische Rübe’ (white Silesian beet) and resynthesis of sugar beet , 1989, Euphytica.

[39]  Jeremy D. DeBarry,et al.  MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity , 2012, Nucleic acids research.

[40]  Darren A. Natale,et al.  The COG database: an updated version includes eukaryotes , 2003, BMC Bioinformatics.

[41]  Peter F. Hallin,et al.  RNAmmer: consistent and rapid annotation of ribosomal RNA genes , 2007, Nucleic acids research.

[42]  Rolf Apweiler,et al.  InterProScan - an integration platform for the signature-recognition methods in InterPro , 2001, Bioinform..

[43]  Hans Lehrach,et al.  Palaeohexaploid ancestry for Caryophyllales inferred from extensive gene-based physical and genetic mapping of the sugar beet genome (Beta vulgaris). , 2012, The Plant journal : for cell and molecular biology.

[44]  Walter Pirovano,et al.  BIOINFORMATICS APPLICATIONS , 2022 .

[45]  Bernd Weisshaar,et al.  Isolation and linkage analysis of expressed disease-resistance gene analogues of sugar beet (Beta vulgaris L.). , 2003, Genome.