Development and preliminary evaluation of a 90 K Axiom® SNP array for the allo-octoploid cultivated strawberry Fragaria × ananassa

BackgroundA high-throughput genotyping platform is needed to enable marker-assisted breeding in the allo-octoploid cultivated strawberry Fragaria × ananassa. Short-read sequences from one diploid and 19 octoploid accessions were aligned to the diploid Fragaria vesca ‘Hawaii 4’ reference genome to identify single nucleotide polymorphisms (SNPs) and indels for incorporation into a 90 K Affymetrix® Axiom® array. We report the development and preliminary evaluation of this array.ResultsAbout 36 million sequence variants were identified in a 19 member, octoploid germplasm panel. Strategies and filtering pipelines were developed to identify and incorporate markers of several types: di-allelic SNPs (66.6%), multi-allelic SNPs (1.8%), indels (10.1%), and ploidy-reducing “haploSNPs” (11.7%). The remaining SNPs included those discovered in the diploid progenitor F. iinumae (3.9%), and speculative “codon-based” SNPs (5.9%). In genotyping 306 octoploid accessions, SNPs were assigned to six classes with Affymetrix’s “SNPolisher” R package. The highest quality classes, PolyHigh Resolution (PHR), No Minor Homozygote (NMH), and Off-Target Variant (OTV) comprised 25%, 38%, and 1% of array markers, respectively. These markers were suitable for genetic studies as demonstrated in the full-sib family ‘Holiday’ × ‘Korona’ with the generation of a genetic linkage map consisting of 6,594 PHR SNPs evenly distributed across 28 chromosomes with an average density of approximately one marker per 0.5 cM, thus exceeding our goal of one marker per cM.ConclusionsThe Affymetrix IStraw90 Axiom array is the first high-throughput genotyping platform for cultivated strawberry and is commercially available to the worldwide scientific community. The array’s high success rate is likely driven by the presence of naturally occurring variation in ploidy level within the nominally octoploid genome, and by effectiveness of the employed array design and ploidy-reducing strategies. This array enables genetic analyses including generation of high-density linkage maps, identification of quantitative trait loci for economically important traits, and genome-wide association studies, thus providing a basis for marker-assisted breeding in this high value crop.

[1]  R. Veilleux,et al.  Integration of Two Diploid Potato Linkage Maps with the Potato Genome Sequence , 2012, PloS one.

[2]  Chengyan Yue,et al.  RosBREED: Enabling marker-assisted breeding in Rosaceae , 2010 .

[3]  Marco C. A. M. Bink,et al.  Genomic Selection for Fruit Quality Traits in Apple (Malus×domestica Borkh.) , 2012, PloS one.

[4]  J. Poulain,et al.  The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla , 2007, Nature.

[5]  Dorrie Main,et al.  Development and Evaluation of a Genome-Wide 6K SNP Array for Diploid Sweet Cherry and Tetraploid Sour Cherry , 2012, PloS one.

[6]  A. Rafalski.  Applications of single nucleotide polymorphisms in crop genetics. , 2002, Current opinion in plant biology.

[7]  B. Denoyes-Rothan,et al.  Tracking the evolutionary history of polyploidy in Fragaria L. (strawberry): new insights from phylogenetic analyses of low-copy nuclear genes. , 2009, Molecular phylogenetics and evolution.

[8]  T. Davis,et al.  Conservation and loss of ribosomal RNA gene sites in diploid and polyploid Fragaria (Rosaceae) , 2011, BMC Plant Biology.

[9]  Roeland E. Voorrips,et al.  Software for the calculation of genetic linkage maps , 2001 .

[10]  D. Sargent,et al.  A genetic linkage map of the cultivated strawberry (Fragaria × ananassa) and its comparison to the diploid Fragaria reference map , 2009, Molecular Breeding.

[11]  M. Troggio,et al.  Genetic dissection of aroma volatile compounds from the essential oil of peach fruit: QTL analysis and identification of candidate genes using dense SNP maps , 2013, Tree Genetics & Genomes.

[12]  T. Davis,et al.  An enhanced method for sequence walking and paralog mining: TOPO® Vector-Ligation PCR , 2010, BMC Research Notes.

[13]  S. Tanksley,et al.  Restriction fragment length polymorphism maps and the concept of graphical genotypes , 2004, Theoretical and Applied Genetics.

[14]  Vladimir Shulaev,et al.  Simple Sequence Repeat Marker Development and Mapping Targeted to Previously Unmapped Regions of the Strawberry Genome Sequence , 2011 .

[15]  M. Clark,et al.  A consensus ‘Honeycrisp’ apple (Malus × domestica) genetic linkage map from three full-sib progeny populations , 2014, Tree Genetics & Genomes.

[16]  M. Feldman,et al.  Genomic asymmetry in allopolyploid plants: wheat as a model. , 2012, Journal of experimental botany.

[17]  R. Visser,et al.  Genomic rearrangements and signatures of breeding in the allo-octoploid strawberry as revealed through an allele dose based SSR linkage map , 2014, BMC Plant Biology.

[18]  Riccardo Velasco,et al.  Evaluation of SNP Data from the Malus Infinium Array Identifies Challenges for Genetic Analysis of Complex Genomes of Polyploid Origin , 2013, PloS one.

[19]  J. V. van Ooijen.  Multipoint maximum likelihood mapping in a full-sib family of an outbreeding species. , 2011, Genetics research.

[20]  David Sankoff,et al.  The dynamics of functional classes of plant genes in rediploidized ancient polyploids , 2013, BMC Bioinformatics.

[21]  R. Brennan,et al.  Wild Crop Relatives: Genomic and Breeding Resources. Temperate Fruits. Edited by C. Kole. Berlin: Springer (2011), pp. 247, £126.00. ISBN 978-3-642-16057-8. , 2011, Experimental Agriculture.

[22]  P. Fontana,et al.  Identification of Pyrus Single Nucleotide Polymorphisms (SNPs) and Evaluation for Genetic Mapping in European Pear and Interspecific Pyrus Hybrids , 2013, PloS one.

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

[24]  I. Verde,et al.  Fine mapping and identification of a candidate gene for a major locus controlling maturity date in peach , 2013, BMC Plant Biology.

[25]  Yasuko Takahashi,et al.  Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events , 2022 .

[26]  D. Sargent,et al.  Development of a dense SNP-based linkage map of an apple rootstock progeny using the Malus Infinium whole genome genotyping array , 2012, BMC Genomics.

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

[28]  M. Bink,et al.  Novel genomic approaches unravel genetic architecture of complex traits in apple , 2013, BMC Genomics.

[29]  Henry D. Priest,et al.  The genome of woodland strawberry (Fragaria vesca) , 2011, Nature Genetics.

[30]  Dorrie Main,et al.  Development and Evaluation of a 9K SNP Array for Peach by Internationally Coordinated SNP Detection and Validation in Breeding Germplasm , 2012, PloS one.

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

[32]  A. Walsh,et al.  Mining single-nucleotide polymorphisms from hexaploid wheat ESTs. , 2003, Genome.

[33]  R. Snowdon,et al.  A High-Density SNP Map for Accurate Mapping of Seed Fibre QTL in Brassica napus L , 2013, PloS one.

[34]  Riccardo Velasco,et al.  An Ancient Duplication of Apple MYB Transcription Factors Is Responsible for Novel Red Fruit-Flesh Phenotypes1[C][W] , 2012, Plant Physiology.

[35]  A. Liston,et al.  Insights into phylogeny, sex function and age of Fragaria based on whole chloroplast genome sequencing. , 2013, Molecular phylogenetics and evolution.

[36]  Dany Severac,et al.  Genome rearrangements derived from homoeologous recombination following allopolyploidy speciation in coffee. , 2014, The Plant journal : for cell and molecular biology.

[37]  G. Reighard,et al.  Mapping quantitative trait loci associated with blush in peach [Prunus persica (L.) Batsch] , 2014, Tree Genetics & Genomes.

[38]  J. Dvorak,et al.  Single nucleotide polymorphism genotyping in polyploid wheat with the Illumina GoldenGate assay , 2009, Theoretical and Applied Genetics.

[39]  Dr. Susumu Ohno.  Evolution by Gene Duplication , 1970, Springer Berlin Heidelberg.

[40]  G. Reighard,et al.  Mapping quantitative trait loci associated with resistance to bacterial spot (Xanthomonas arboricola pv. pruni) in peach , 2012, Tree Genetics & Genomes.

[41]  Marcel Martin.  Cutadapt removes adapter sequences from high-throughput sequencing reads , 2011 .

[42]  M. Bink,et al.  Bayesian QTL analyses using pedigreed families of an outcrossing species, with application to fruit firmness in apple , 2014, Theoretical and Applied Genetics.

[43]  T. Davis,et al.  A Phylogenetic Analysis of the Genus Fragaria (Strawberry) Using Intron-Containing Sequence from the ADH-1 Gene , 2014, PloS one.

[44]  J. V. Ooijen,et al.  Multipoint maximum likelihood mapping in a full-sib family of an outbreeding species. , 2011 .

[45]  R. S. Bringhurst.  Cytogenetics and Evolution in American Fragaria , 1990 .

[46]  Andreas Peil,et al.  ‘Schmidt's Antonovka’ is identical to ‘Common Antonovka’, an apple cultivar widely used in Russia in breeding for biotic and abiotic stresses , 2013, Tree Genetics & Genomes.

[47]  Riccardo Velasco,et al.  Development and Validation of a 20K Single Nucleotide Polymorphism (SNP) Whole Genome Genotyping Array for Apple (Malus × domestica Borkh) , 2014, PloS one.

[48]  M. Gribskov,et al.  The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray) , 2006, Science.

[49]  J. Forster,et al.  Identification, characterization and interpretation of single-nucleotide sequence variation in allopolyploid crop species. , 2012, Plant biotechnology journal.

[50]  Riccardo Velasco,et al.  Genome-Wide SNP Detection, Validation, and Development of an 8K SNP Array for Apple , 2012, PloS one.

[51]  A. Iezzoni,et al.  Construction and Comparative Analyses of Highly Dense Linkage Maps of Two Sweet Cherry Intra-Specific Progenies of Commercial Cultivars , 2013, PloS one.

[52]  M. DePristo,et al.  A framework for variation discovery and genotyping using next-generation DNA sequencing data , 2011, Nature Genetics.

[53]  Lex E. Flagel,et al.  Evolutionary rate variation, genomic dominance and duplicate gene expression evolution during allotetraploid cotton speciation. , 2010, The New phytologist.

[54]  G. Trotoux,et al.  High-density SNP-based genetic map development and linkage disequilibrium assessment in Brassica napus L , 2013, BMC Genomics.

[55]  D. Soltis,et al.  Rapid, Repeated, and Clustered Loss of Duplicate Genes in Allopolyploid Plant Populations of Independent Origin , 2012, Current Biology.

[56]  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.

[57]  J. Anderson,et al.  Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars , 2013, Proceedings of the National Academy of Sciences.

[58]  Jane Masterson,et al.  Stomatal Size in Fossil Plants: Evidence for Polyploidy in Majority of Angiosperms , 1994, Science.

[59]  J. Rafalski,et al.  Association genetics in crop improvement. , 2010, Current opinion in plant biology.

[60]  Helga Thorvaldsdóttir,et al.  Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration , 2012, Briefings Bioinform..

[61]  Ping Zheng,et al.  The Genome Database for Rosaceae (GDR): year 10 update , 2013, Nucleic Acids Res..

[62]  A. Dale,et al.  Reconstruction of the strawberry, fragaria ×ananassa, using genotypes of F. virginiana and F. chiloensis , 2010 .

[63]  Roger E Bumgarner,et al.  The genome of the domesticated apple (Malus × domestica Borkh.) , 2010, Nature Genetics.