Towards a whole-genome sequence for rye (Secale cereale L.)

Plant Journal

Volumn 89, Issue 5, 2017, Pages 853-869

  Bauer, Eva ^a   Schmutzer, Thomas ^b   Barilar, Ivan ^c   Mascher, Martin ^b   Gundlach, Heidrun ^d   Martis, Mihaela M ^d,g   Twardziok, Sven O ^d   Hackauf, Bernd ^e   Gordillo, Andres ^f   Wilde, Peer ^f   Schmidt, Malthe ^f   Korzun, Viktor ^f   Mayer, Klaus F X ^d   Schmid, Karl ^c   Schön, Chris Carolin ^a   Scholz, Uwe ^b  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^c UNIVERSITY OF HOHENHEIM   (Germany)

^d INSTITUTE OF EPIDEMIOLOGY   (Germany)

^e INSTITUTE FOR EPIDEMIOLOGY AND PATHOGEN DIAGNOSTICS   (Germany)

^f KWS LOCHOW GmbH   (Germany)

^g LINKÖPING UNIVERSITY   (Sweden)

Author keywords

de novo genome assembly; diversity; high density genetic map; rye; rye genome zipper; Rye600k genotyping array; Secale cereale L.; selection signals; single nucleotide variants; whole genome shotgun sequencing

Indexed keywords

FACSIMILE; GENETIC ENGINEERING; NUCLEOTIDES; SCAFFOLDS;

DIVERSITY; GENETIC MAP; GENOME ASSEMBLY; GENOME ZIPPERS; GENOTYPING; SECALE CEREALE; SELECTION SIGNAL; SINGLE NUCLEOTIDES; WHOLE-GENOME SHOTGUN;

GENES;

GENETIC ENGINEERING; RESEARCH;

PLANT DNA;

GENETICS; GENOMICS; GENOTYPE; PLANT CHROMOSOME; PLANT GENOME; SECALE; SYNTENY;

CHROMOSOMES, PLANT; DNA, PLANT; GENOME, PLANT; GENOMICS; GENOTYPE; SECALE; SYNTENY;

EID: 85013218379     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.13436     Document Type: Article

References (100)

1. Antao, T., Lopes, A., Lopes, R.J., Beja-Pereira, A. and Luikart, G. (2008) LOSITAN: a workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinformatics, 9, 1–5.
2. Arend, D., Lange, M., Chen, J., Colmsee, C., Flemming, S., Hecht, D. and Scholz, U. (2014) e!DAL – a framework to store, share and publish research data. BMC Bioinformatics, 15, 214.
3. Arend, D., Junker, A., Scholz, U., Schüler, D., Wylie, J. and Lange, M. (2016) PGP repository: a plant phenomics and genomics data publication infrastructure. Database, 2016, 1–10.
4. Auinger, H.-J., Schönleben, M., Lehermeier, C. et al. (2016) Model training across multiple breeding cycles significantly improves genomic prediction accuracy in rye (Secale cereale L.) Theor. Appl. Genet. 129, 2043–2053. (accepted)
5. Banaei-Moghaddam, A.M., Martis, M.M., Macas, J., Gundlach, H., Himmelbach, A., Altschmied, L., Mayer, K.F.X. and Houben, A. (2015) Genes on B chromosomes: old questions revisited with new tools. BBA-Gene Regul. Mech. 1849, 64–70.
6. Bartoš, J., Paux, E., Kofler, R. et al. (2008) A first survey of the rye (Secale cereale) genome composition through BAC end sequencing of the short arm of chromosome 1R. BMC Plant Biol. 8, 1–12.
7. Beaumont, M. and Nichols, R. (1996) Evaluating loci for use in the genetic analysis of population structure. Proc. Roy. Soc. Lond. B: Biol. Sci. 263, 1619–1626.
8. Beier, S., Himmelbach, A., Schmutzer, T. et al. (2015) Multiplex sequencing of bacterial artificial chromosomes for assembling complex plant genomes. Plant Biotechnol. J. 14, 1511–1522.
9. Boetzer, M., Henkel, C.V., Jansen, H.J., Butler, D. and Pirovano, W. (2011) Scaffolding pre-assembled contigs using SSPACE. Bioinformatics, 27, 578–579.
10. Chao, S., Dubcovsky, J., Dvorak, J. et al. (2010) Population- and genome-specific patterns of linkage disequilibrium and SNP variation in spring and winter wheat (Triticum aestivum L.). BMC Genom. 11, 1–17.
11. Chapman, J.A., Mascher, M., Buluç, A. et al. (2015) A whole-genome shotgun approach for assembling and anchoring the hexaploid bread wheat genome. Genome Biol. 16, 26.
12. Danecek, P., Auton, A., Abecasis, G. et al. (2011) The variant call format and VCFtools. Bioinformatics, 27, 2156–2158.
13. Deng, W., Nickle, D.C., Learn, G.H., Maust, B. and Mullins, J.I. (2007) ViroBLAST: a stand-alone BLAST web server for flexible queries of multiple databases and user's datasets. Bioinformatics, 23, 2334–2336.
14. Devos, K.M., Atkinson, M.D., Chinoy, C.N. et al. (1993) Chromosomal rearrangements in the rye genome relative to that of wheat. Theor. Appl. Genet. 85, 673–680.
15. Doyle, J.J. and Doyle, J.L. (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19, 11–15.
16. Dray, S. and Dufour, A.B. (2007) The ade4 package: implementing the duality diagram for ecologists. J. Stat. Software, 22, 1–20.
17. Esch, M., Chen, J., Colmsee, C., Klapperstück, M., Grafahrend-Belau, E., Scholz, U. and Lange, M. (2015) LAILAPS: the plant science search engine. Plant Cell Physiol. 56, e8.
18. Falke, K.C., Wilde, P. and Miedaner, T. (2009a) Rye introgression lines as source of alleles for pollen-fertility restoration in Pampa CMS. Plant Breeding, 128, 528–531.
19. Falke, K.C., Wilde, P., Wortmann, H., Geiger, H.H. and Miedaner, T. (2009b) Identification of genomic regions carrying QTL for agronomic and quality traits in rye Secale cereale introgression libraries. Plant Breeding, 128, 615–623.
20. Fischer, S., Melchinger, A.E., Korzun, V. et al. (2010) Molecular marker assisted broadening of the Central European heterotic groups in rye with Eastern European germplasm. Theor. Appl. Genet. 120, 291–299.
21. Flavell, R.B., Bennett, M.D., Smith, J.B. and Smith, D.B. (1974) Genome size and the proportion of repeated nucleotide sequence DNA in plants. Biochem. Genet. 12, 257–269.
22. Fowler, D.B. and Carles, R.J. (1979) Growth, development, and cold tolerance of fall-acclimated cereal-grains. Crop Sci. 19, 915–922.
23. Fujii, S. and Toriyama, K. (2008) DCW11, down-regulated gene 11 in CW-type cytoplasmic male sterile rice, encoding mitochondrial protein phosphatase 2C is related to cytoplasmic male sterility. Plant Cell Physiol. 49, 633–640.
24. Gao, H., Webster, T., Pirani, A., Zhan, Y., Lu, Y. and Shen, M.-M. (2012) SNPolisher: tools for SNP classification, visualization and OTV genotyping (R package version 1.3.6.6).
25. Geiger, H.H. and Miedaner, T. (2009) Rye (Secale cereale L.). In Cereals (Carena, M.J., ed.). New York, USA: Springer, pp. 157–181.
26. Glémin, S., Clément, Y., David, J. and Ressayre, A. (2014) GC content evolution in coding regions of angiosperm genomes: a unifying hypothesis. Trends Genet. 30, 263–270.
27. Götz, S., García-Gómez, J.M., Terol, J. et al. (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res. 36, 3420–3435.
28. Gremme, G., Brendel, V., Sparks, M.E. and Kurtz, S. (2005) Engineering a software tool for gene structure prediction in higher organisms. Inform. Software Technol. 47, 965–978.
29. Günther, T. and Coop, G. (2013) Robust identification of local adaptation from allele frequencies. Genetics, 195, 205–220.
30. Haseneyer, G., Schmutzer, T., Seidel, M. et al. (2011) From RNA-seq to large-scale genotyping – genomics resources for rye (Secale cereale L.). BMC Plant Biol. 11, 131.
31. Hastie, A.R., Dong, L.L., Smith, A. et al. (2013) Rapid genome mapping in nanochannel arrays for highly complete and accurate de novo sequence assembly of the complex Aegilops tauschii genome. PLoS ONE, 8, e55864.
32. Hunt, M., Newbold, C., Berriman, M. and Otto, T.D. (2014) A comprehensive evaluation of assembly scaffolding tools. Genome Biol. 15, 1–15.
33. International Brachypodium Initiative (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature, 463, 763–768.
34. Jia, J., Zhao, S., Kong, X. et al. (2013) Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature, 496, 91–95.
35. Jones, J.D.G. and Flavell, R.B. (1982) The structure, amount and chromosomal localisation of defined repeated DNA sequences in species of the genus Secale. Chromosoma, 86, 613–641.
36. Kawahara, Y., de la Bastide, M., Hamilton, J.P. et al. (2013) Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice (New York, N.Y.), 6, 4.
37. Krzywinski, M., Schein, J., Birol, I., Connors, J., Gascoyne, R., Horsman, D., Jones, S.J. and Marra, M.A. (2009) Circos: an information aesthetic for comparative genomics. Genome Res. 19, 1639–1645.
38. Lee, T.-H., Guo, H., Wang, X., Kim, C. and Paterson, A.H. (2014) SNPhylo: a pipeline to construct a phylogenetic tree from huge SNP data. BMC Genom. 15, 1–6.
39. Li, H. (2011) Improving SNP discovery by base alignment quality. Bioinformatics, 27, 1157–1158.
40. Li, H. and Durbin, R. (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25, 1754–1760.
41. Li, H., Handsaker, B., Wysoker, A. et al. (2009a) The Sequence Alignment/Map format and SAMtools. Bioinformatics, 25, 2078–2079.
42. Li, S., Qian, Q., Fu, Z. et al. (2009b) Short panicle1 encodes a putative PTR family transporter and determines rice panicle size. Plant J. 58, 592–605.
43. Li, Y., Haseneyer, G., Schön, C.-C., Ankerst, D., Korzun, V., Wilde, P. and Bauer, E. (2011) High levels of nucleotide diversity and fast decline of linkage disequilibrium in rye (Secale cereale L.) genes involved in frost response. BMC Plant Biol. 11, 6.
44. Ling, H.-Q., Zhao, S., Liu, D. et al. (2013) Draft genome of the wheat A-genome progenitor Triticum urartu. Nature, 496, 87–90.
45. Mahone, G.S., Frisch, M., Bauer, E., Haseneyer, G., Miedaner, T. and Falke, K.C. (2015) Detection of donor effects in a rye introgression population with genome-wide prediction. Plant Breeding, 134, 406–415.
46. Manzanero, S., Puertas, M.J., Jiménez, G. and Vega, J.M. (2000) Neocentric activity of rye 5RL chromosome in wheat. Chromosome Res. 8, 543–554.
47. Martis, M.M., Zhou, R., Haseneyer, G. et al. (2013) Reticulate evolution of the rye genome. Plant Cell, 25, 3685–3698.
48. Mascher, M., Muehlbauer, G.J., Rokhsar, D.S. et al. (2013a) Anchoring and ordering NGS contig assemblies by population sequencing (POPSEQ). Plant J. 76, 718–727.
49. Mascher, M., Richmond, T.A., Gerhardt, D.J. et al. (2013b) Barley whole exome capture: a tool for genomic research in the genus Hordeum and beyond. Plant J. 76, 494–505.
50. Mascher, M., Jost, M., Kuon, J.-E., Himmelbach, A., Aßfalg, A., Beier, S., Scholz, U., Graner, A. and Stein, N. (2014) Mapping-by-sequencing accelerates forward genetics in barley. Genome Biol. 15, R78.
51. Matsumoto, T., Tanaka, T., Sakai, H. et al. (2011) Comprehensive sequence analysis of 24,783 barley full-length cDNAs derived from 12 clone libraries. Plant Physiol. 156, 20–28.
52. Mayer, K.F.X., Martis, M., Hedley, P.E. et al. (2011) Unlocking the barley genome by chromosomal and comparative genomics. Plant Cell, 23, 1249–1263.
53. Mayer, K.F.X., Waugh, R., Brown, J.W.S. et al. (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature, 491, 711–716.
54. Mayer, K.F.X., Rogers, J., Dolezel, J. et al. (2014) A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science, 345, 1251788.
55. McMullen, M.D., Kresovich, S., Villeda, H.S. et al. (2009) Genetic properties of the maize nested association mapping population. Science, 325, 737–740.
56. Middleton, C.P., Stein, N., Keller, B., Kilian, B. and Wicker, T. (2013) Comparative analysis of genome composition in Triticeae reveals strong variation in transposable element dynamics and nucleotide diversity. Plant J. 73, 347–356.
57. Miedaner, T., Glass, C., Dreyer, F., Wilde, P., Wortmann, H. and Geiger, H.H. (2000) Mapping of genes for male-fertility restoration in ‘Pampa’ CMS winter rye (Secale cereale L.). Theor. Appl. Genet. 101, 1226–1233.
58. Miedaner, T., Müller, B.U., Piepho, H.P. and Falke, K.C. (2011) Genetic architecture of plant height in winter rye introgression libraries. Plant Breeding, 130, 209–216.
59. Miedaner, T., Hübner, M., Korzun, V., Schmiedchen, B., Bauer, E., Haseneyer, G., Wilde, P. and Reif, J. (2012) Genetic architecture of complex agronomic traits examined in two testcross populations of rye (Secale cereale L.). BMC Genom. 13, 706.
60. Naranjo, T. and Fernández-Rueda, P. (1991) Homoeology of rye chromosome arms to wheat. Theor. Appl. Genet. 82, 577–586.
61. Oettler, G. (2005) The fortune of a botanical curiosity – Triticale: past, present and future. J. Agric. Sci. 143, 329–346.
62. Parat, F., Schwertfirm, G., Rudolph, U., Miedaner, T., Korzun, V., Bauer, E., Tellier, A. and Schön, C.-C. (2015) Geography and end use drive the diversification of worldwide winter rye populations. Mol. Ecol. 25, 500–514.
63. Passaia, G., Caverzan, A., Fonini, L.S., Carvalho, F.E.L., Silveira, J.A.G. and Margis-Pinheiro, M. (2014) Chloroplastic and mitochondrial GPX genes play a critical role in rice development. Biol. Plant. 58, 375–378.
64. Paterson, A.H., Bowers, J.E., Bruggmann, R. et al. (2009) The Sorghum bicolor genome and the diversification of grasses. Nature, 457, 551–556.
65. Plaschke, J., Börner, A., Xie, D.X., Koebner, R.M.D., Schlegel, R. and Gale, M.D. (1993) RFLP mapping of genes affecting plant height and growth habit in rye. Theor. Appl. Genet. 85, 1049–1054.
66. R Core Team (2015) A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.
67. Rabinovich, S.V. (1998) Importance of wheat-rye translocations for breeding modern cultivar of Triticum aestivum L. Euphytica, 100, 323–340.
68. Roberts, A., Pimentel, H., Trapnell, C. and Pachter, L. (2011) Identification of novel transcripts in annotated genomes using RNA-Seq. Bioinformatics, 27, 2325–2329.
69. Rogers, J.S. (1972) Measures of genetic similarity and genetic distance. In Studies in Genetics (Wheeler, M.R., ed.). Austin, Texas, USA: University of Texas, pp. 145–153.
70. Saghai-Maroof, M.A., Soliman, K.M., Jorgensen, R.A. and Allard, R.W. (1984) Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics. Proc. Natl Acad. Sci. USA, 81, 8014–8018.
71. Schatz, M.C., Delcher, A.L. and Salzberg, S.L. (2010) Assembly of large genomes using second-generation sequencing. Genome Res. 20, 1165–1173.
72. Schittenhelm, S., Kraft, M. and Wittich, K.-P. (2014) Performance of winter cereals grown on field-stored soil moisture only. Eur. J. Agron. 52, Part B, 247–258.
73. Schlegel, R. (1987) Neocentric activity in chromosome 5R of rye revealed by haploidy. Hereditas, 107, 1–6.
74. Schmutzer, T., Ma, L., Pousarebani, N., Bull, F., Stein, N., Houben, A. and Scholz, U. (2014) Kmasker – a tool for in silico prediction of single-copy FISH probes for the large-genome species Hordeum vulgare. Cytogenet. Genome Res. 142, 66–78.
75. Semagn, K., Babu, R., Hearne, S. and Olsen, M. (2014) Single nucleotide polymorphism genotyping using Kompetitive Allele Specific PCR (KASP): overview of the technology and its application in crop improvement. Mol. Breed. 33, 1–14.
76. Simão, F.A., Waterhouse, R.M., Ioannidis, P., Kriventseva, E.V. and Zdobnov, E.M. (2015) BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics, 31, 3210–3212.
77. Spannagl, M., Alaux, M., Lange, M. et al. (2016a) transPLANT resources for Triticeae genomic data. The Plant Genome, 9, 1–13.
78. Spannagl, M., Nussbaumer, T., Bader, K.C., Martis, M.M., Seidel, M., Kugler, K.G., Gundlach, H. and Mayer, K.F.X. (2016b) PGSB PlantsDB: updates to the database framework for comparative plant genome research. Nucl. Acids Res. 44, D1141–D1147.
79. Tanabe, S., Ashikari, M., Fujioka, S. et al. (2005) A novel cytochrome P450 is implicated in brassinosteroid biosynthesis via the characterization of a rice dwarf mutant, dwarf11, with reduced seed length. Plant Cell, 17, 776–790.
80. Taylor, J. and Butler, D. (2014) ASMap: an (A)ccurate and (S)peedy linkage map construction package for inbred populatons that uses the extremely efficient MSTmap algorithm. (R package version 0.3-3).
81. The International Barley Genome Sequencing Consortium (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature, 491, 711–716.
82. Thompson, J.B. and Rees, H. (1956) Selection for heterozygotes during inbreeding. Nature, 177, 385–386.
83. Treangen, T.J. and Salzberg, S.L. (2012) Repetitive DNA and next-generation sequencing: computational challenges and solutions. Nat. Rev. Genet. 13, 36–46.
84. Unterseer, S., Bauer, E., Haberer, G. et al. (2014) A powerful tool for genome analysis in maize: development and evaluation of the high density 600 k SNP genotyping array. BMC Genom. 15, 823.
85. Unterseer, S., Pophaly, S.D., Peis, R. et al. (2016) A comprehensive study of the genomic differentiation between temperate Dent and Flint maize. Genome Biol. Evol. 17, 137.
86. Vergara, I.A., Frech, C. and Chen, N. (2012) CooVar: co-occurring variant analyzer. BMC Research Notes, 5, 1–7.
87. Visser, E.A., Wegrzyn, J.L., Steenkmap, E.T., Myburg, A.A. and Naidoo, S. (2015) Combined de novo and genome guided assembly and annotation of the Pinus patula juvenile shoot transcriptome. BMC Genom. 16, 1–13.
88. Voss-Fels, K. and Snowdon, R.J. (2015) Understanding and utilizing crop genome diversity via high-resolution genotyping. Plant Biotechnol. J. 14, 1086–1094.
89. Weir, B.S. and Cockerham, C.C. (1984) Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358–1370.
90. Wicker, T., Matthews, D.E. and Keller, B. (2002) TREP: a database for Triticeae repetitive elements. Trends Plant Sci. 7, 561–562.
91. Wicker, T., Taudien, S., Houben, A., Keller, B., Graner, A., Platzer, M. and Stein, N. (2009) 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. Plant J. 59, 712–722.
92. Wilcoxon, F. (1945) Individual comparisons by ranking methods. Biometrics Bulletin, 1, 80–83.
93. Wimmer, V., Albrecht, T., Auinger, H.-J. and Schön, C.-C. (2012) Synbreed: a framework for the analysis of genomic prediction data using R. Bioinformatics, 28, 2086–2087.
94. Winfield, M.O., Allen, A.M., Burridge, A.J. et al. (2016) High-density SNP genotyping array for hexaploid wheat and its secondary and tertiary gene pool. Plant Biotechnol. J. 14, 1195–1206.
95. Wricke, G., Wilde, P., Wehling, P. and Gieselmann, C. (1993) An isozyme marker for pollen fertility restoration in the Pampa cms system of rye (Secale cereale L.). Plant Breeding, 111, 290–294.
96. Wu, T.D. and Nacu, S. (2010) Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics, 26, 873–881.
97. Xu, C., Jiao, C., Zheng, Y. et al. (2015) De novo and comparative transcriptome analysis of cultivated and wild spinach. Sci. Rep. 5, 17706.
98. Yonemaru, J.-I., Yamamoto, T., Fukuoka, S., Uga, Y., Hori, K. and Yano, M. (2010) Q-TARO: QTL annotation rice online database. Rice, 3, 194–203.
99. Zhang, Z., Schwartz, S., Wagner, L. and Miller, W. (2000) A greedy algorithm for aligning DNA sequences. J. Comput. Biol. 7, 203–214.
100. Zhou, H., Muehlbauer, G. and Steffenson, B. (2012) Population structure and linkage disequilibrium in elite barley breeding germplasm from the United States. J. Zhejiang Uni. Sci. B, 13, 438–451.