The barley pan-genome reveals the hidden legacy of mutation breeding

  • 1.

    Bayer, P. E., Golicz, A. A., Scheben, A., Batley, J. & Edwards, D. Plant pan-genomes are the new reference. Nat. Plants 6, 914–920 (2020).

    PubMed 

    Google Scholar
     

  • 2.

    Dawson, I. K. et al. Barley: a translational model for adaptation to climate change. New Phytol. 206, 913–931 (2015).

    PubMed 

    Google Scholar
     

  • 3.

    Stein, N. & Muehlbauer, G. J. The Barley Genome (Springer, 2018).

  • 4.

    International Barley Genome Sequencing Consortium. A physical, genetic and functional sequence assembly of the barley genome. Nature 491, 711–716 (2012).

    ADS 

    Google Scholar
     

  • 5.

    Mascher, M. et al. A chromosome conformation capture ordered sequence of the barley genome. Nature 544, 427–433 (2017).

    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • 6.

    Monat, C. et al. TRITEX: chromosome-scale sequence assembly of Triticeae genomes with open-source tools. Genome Biol. 20, 284 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 7.

    Mascher, M. et al. Mapping-by-sequencing accelerates forward genetics in barley. Genome Biol. 15, R78 (2014).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 8.

    Russell, J. et al. Exome sequencing of geographically diverse barley landraces and wild relatives gives insights into environmental adaptation. Nat. Genet. 48, 1024–1030 (2016).

    CAS 
    PubMed 

    Google Scholar
     

  • 9.

    Milner, S. G. et al. Genebank genomics highlights the diversity of a global barley collection. Nat. Genet. 51, 319–326 (2019).

    CAS 
    PubMed 

    Google Scholar
     

  • 10.

    Muñoz-Amatriaín, M. et al. Distribution, functional impact, and origin mechanisms of copy number variation in the barley genome. Genome Biol. 14, R58 (2013).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 11.

    Taketa, S. et al. Barley grain with adhering hulls is controlled by an ERF family transcription factor gene regulating a lipid biosynthesis pathway. Proc. Natl Acad. Sci. USA 105, 4062–4067 (2008).

    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • 12.

    Tettelin, H. et al. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome”. Proc. Natl Acad. Sci. USA 102, 13950–13955 (2005).

    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • 13.

    Ho, S. S., Urban, A. E. & Mills, R. E. Structural variation in the sequencing era. Nat. Rev. Genet. 21, 171–189 (2019).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 14.

    Danilevicz, M. F., Tay Fernandez, C. G., Marsh, J. I., Bayer, P. E. & Edwards, D. Plant pangenomics: approaches, applications and advancements. Curr. Opin. Plant Biol. 54, 18–25 (2020).

    CAS 
    PubMed 

    Google Scholar
     

  • 15.

    Monat, C., Schreiber, M., Stein, N. & Mascher, M. Prospects of pan-genomics in barley. Theor. Appl. Genet. 132, 785–796 (2019).

    PubMed 

    Google Scholar
     

  • 16.

    Coronado, M.-J., Hensel, G., Broeders, S., Otto, I. & Kumlehn, J. Immature pollen-derived doubled haploid formation in barley cv. Golden Promise as a tool for transgene recombination. Acta Physiol. Plant. 27, 591–599 (2005).

    CAS 

    Google Scholar
     

  • 17.

    Schreiber, M. et al. A genome assembly of the barley ‘transformation reference’ cultivar Golden Promise. G3 10, 1823–1827 (2020).

    CAS 
    PubMed 

    Google Scholar
     

  • 18.

    Gottwald, S., Bauer, P., Komatsuda, T., Lundqvist, U. & Stein, N. TILLING in the two-rowed barley cultivar ‘Barke’ reveals preferred sites of functional diversity in the gene HvHox1. BMC Res. Notes 2, 258 (2009).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 19.

    Mascher, M. et al. Anchoring and ordering NGS contig assemblies by population sequencing (POPSEQ). Plant J. 76, 718–727 (2013).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 20.

    Hübner, S. et al. Strong correlation of wild barley (Hordeum spontaneum) population structure with temperature and precipitation variation. Mol. Ecol. 18, 1523–1536 (2009).

    PubMed 

    Google Scholar
     

  • 21.

    Chikhi, R., Limasset, A. & Medvedev, P. Compacting de Bruijn graphs from sequencing data quickly and in low memory. Bioinformatics 32, i201–i208 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 22.

    Luo, R. et al. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1, 18 (2012).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 23.

    Clavijo, B. J. et al. An improved assembly and annotation of the allohexaploid wheat genome identifies complete families of agronomic genes and provides genomic evidence for chromosomal translocations. Genome Res. 27, 885–896 (2017).

    MathSciNet 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 24.

    Anderson, S. N. et al. Transposable elements contribute to dynamic genome content in maize. Plant J. 100, 1052–1065 (2019).

    CAS 
    PubMed 

    Google Scholar
     

  • 25.

    Brunner, S., Fengler, K., Morgante, M., Tingey, S. & Rafalski, A. Evolution of DNA sequence nonhomologies among maize inbreds. Plant Cell 17, 343–360 (2005).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 26.

    Nattestad, M. & Schatz, M. C. Assemblytics: a web analytics tool for the detection of variants from an assembly. Bioinformatics 32, 3021–3023 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 27.

    Gordon, S. P. et al. Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure. Nat. Commun. 8, 2184 (2017).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 28.

    Yu, S. et al. A single nucleotide polymorphism of Nud converts the caryopsis type of barley (Hordeum vulgare L.). Plant Mol. Biol. Report. 34, 242–248 (2016).

    CAS 

    Google Scholar
     

  • 29.

    Arora, S. et al. Resistance gene cloning from a wild crop relative by sequence capture and association genetics. Nat. Biotechnol. 37, 139–143 (2019).

    CAS 
    PubMed 

    Google Scholar
     

  • 30.

    Lipka, A. E. et al. GAPIT: genome association and prediction integrated tool. Bioinformatics 28, 2397–2399 (2012).

    CAS 
    PubMed 

    Google Scholar
     

  • 31.

    Yu, J. et al. A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat. Genet. 38, 203–208 (2006).

    CAS 
    PubMed 

    Google Scholar
     

  • 32.

    Ekberg, I. Cytogenetic studies of three paracentric inversions in barley. Hereditas 76, 1–30 (1974).

    CAS 
    PubMed 

    Google Scholar
     

  • 33.

    Ramage, R. & Suneson, C. Translocation-gene linkages on barley chromosome 7. Crop Sci. 1, 319–320 (1961).


    Google Scholar
     

  • 34.

    Himmelbach, A. et al. Discovery of multi-megabase polymorphic inversions by chromosome conformation capture sequencing in large-genome plant species. Plant J. 96, 1309–1316 (2018).

    CAS 
    PubMed 

    Google Scholar
     

  • 35.

    Ederveen, A., Lai, Y., van Driel, M. A., Gerats, T. & Peters, J. L. Modulating crossover positioning by introducing large structural changes in chromosomes. BMC Genomics 16, 89 (2015).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 36.

    Bouma, J. & Ohnoutka, Z. Importance and Application of the Mutant ‘Diamant’ in Spring Barley Breeding (IAEA, 1991).

  • 37.

    Comadran, J. et al. Natural variation in a homolog of Antirrhinum CENTRORADIALIS contributed to spring growth habit and environmental adaptation in cultivated barley. Nat. Genet. 44, 1388–1392 (2012).

    CAS 
    PubMed 

    Google Scholar
     

  • 38.

    Bustos-Korts, D. et al. Exome sequences and multi-environment field trials elucidate the genetic basis of adaptation in barley. Plant J. 99, 1172–1191 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 39.

    Mascher, M. et al. Genebank genomics bridges the gap between the conservation of crop diversity and plant breeding. Nat. Genet. 51, 1076–1081 (2019).

    CAS 
    PubMed 

    Google Scholar
     

  • 40.

    Khan, A. W. et al. Super-pangenome by integrating the wild side of a species for accelerated crop improvement. Trends Plant Sci. 25, 148–158 (2020).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 41.

    Dvorak, J., McGuire, P. E. & Cassidy, B. Apparent sources of the A genomes of wheats inferred from polymorphism in abundance and restriction fragment length of repeated nucleotide sequences. Genome 30, 680–689 (1988).

    CAS 

    Google Scholar
     

  • 42.

    Himmelbach, A., Walde, I., Mascher, M. & Stein, N. Tethered chromosome conformation capture sequencing in Triticeae: a valuable tool for genome assembly. Bio Protoc. 8, e2955 (2018).

    CAS 

    Google Scholar
     

  • 43.

    Padmarasu, S., Himmelbach, A., Mascher, M. & Stein, N. in Plant Long Non-Coding RNAs (eds Chekanova, J. & Wang, H.-L.) 441–472 (Springer, 2019).

  • 44.

    Matsumoto, T. et al. Comprehensive sequence analysis of 24,783 barley full-length cDNAs derived from 12 clone libraries. Plant Physiol. 156, 20–28 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 45.

    Kent, W. J. BLAT—the BLAST-like alignment tool. Genome Res. 12, 656–664 (2002).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 46.

    Slater, G. S. C. & Birney, E. Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics 6, 31 (2005).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 47.

    Emms, D. M. & Kelly, S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 16, 157 (2015).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 48.

    Spannagl, M. et al. PGSB PlantsDB: updates to the database framework for comparative plant genome research. Nucleic Acids Res. 44, D1141–D1147 (2016).

    CAS 
    PubMed 

    Google Scholar
     

  • 49.

    Ellinghaus, D., Kurtz, S. & Willhoeft, U. LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinformatics 9, 18 (2008).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 50.

    Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 51.

    Gutierrez-Gonzalez, J. J., Mascher, M., Poland, J. & Muehlbauer, G. J. Dense genotyping-by-sequencing linkage maps of two synthetic W7984×Opata reference populations provide insights into wheat structural diversity. Sci. Rep. 9, 1793 (2019).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 52.

    Pedersen, B. S. & Quinlan, A. R. Mosdepth: quick coverage calculation for genomes and exomes. Bioinformatics 34, 867–868 (2018).

    CAS 
    PubMed 

    Google Scholar
     

  • 53.

    Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 54.

    R Core Team. R: A Language and Environment for Statistical Computing http://www.R-project.org (R Foundation for Statistical Computing, 2013).

  • 55.

    Bushnell, B. BBMap: A Fast, Accurate, Splice-aware Aligner (Lawrence Berkeley National Laboratory, 2014).

  • 56.

    Csardi, G. & Nepusz, T. The igraph software package for complex network research. InterJournal Complex Syst. 1695, 1–9 (2006).


    Google Scholar
     

  • 57.

    Schwartz, S. et al. PipMaker—a web server for aligning two genomic DNA sequences. Genome Res. 10, 577–586 (2000).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 58.

    Li, H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 27, 2987–2993 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 59.

    Zheng, X. & Gogarten, S. SeqArray: big data management of genome-wide sequence variants. R package version 1.10.6 https://github.com/zhengxwen/SeqArray (accessed January 2017).

  • 60.

    Zheng, X. et al. A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics 28, 3326–3328 (2012).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 61.

    Akbari, M. et al. Diversity arrays technology (DArT) for high-throughput profiling of the hexaploid wheat genome. Theor. Appl. Genet. 113, 1409–1420 (2006).

    CAS 
    PubMed 

    Google Scholar
     

  • 62.

    Hill, C. B. et al. Hybridisation-based target enrichment of phenology genes to dissect the genetic basis of yield and adaptation in barley. Plant Biotechnol. J. 17, 932–944 (2019).

    CAS 
    PubMed 

    Google Scholar
     

  • 63.

    Van Ooijen, J. MapQTL 5, Software for the Mapping of Quantitative Trait Loci in Experimental Populations (Kyazma, 2004).

  • 64.

    Xiao, C. L. et al. MECAT: fast mapping, error correction, and de novo assembly for single-molecule sequencing reads. Nat. Methods 14, 1072–1074 (2017).

    CAS 
    PubMed 

    Google Scholar
     

  • 65.

    Chin, C. S. et al. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat. Methods 10, 563–569 (2013).

    CAS 
    PubMed 

    Google Scholar
     

  • 66.

    Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Preprint at https://arxiv.org/abs/1303.3997 (2013).

  • 67.

    McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 68.

    Arend, D. et al. PGP repository: a plant phenomics and genomics data publication infrastructure. Database (Oxford) 2016, baw033 (2016).


    Google Scholar
     

  • 69.

    Arend, D. et al. e!DAL—a framework to store, share and publish research data. BMC Bioinformatics 15, 214 (2014).

    PubMed 
    PubMed Central 

    Google Scholar