Abstract
Single-nucleotide polymorphisms (SNPs) are the most prevalent type of variation in genomes that are increasingly being used as molecular markers in diversity analyses, mapping and cloning of genes, and germplasm characterization. However, only a few studies reported large-scale SNP discovery in Aegilops tauschii, restricting their potential use as markers for the low-polymorphic D genome. Here, we report 68,592 SNPs found on the gene-related sequences of the 5D chromosome of Ae. tauschii genotype MvGB589 using genomic and transcriptomic sequences from seven Ae. tauschii accessions, including AL8/78, the only genotype for which a draft genome sequence is available at present. We also suggest a workflow to compare SNP positions in homologous regions on the 5D chromosome of Triticum aestivum, bread wheat, to mark single nucleotide variations between these closely related species. Overall, the identified SNPs define a density of 4.49 SNPs per kilobyte, among the highest reported for the genic regions of Ae. tauschii so far. To our knowledge, this study also presents the first chromosome-specific SNP catalog in Ae. tauschii that should facilitate the association of these SNPs with morphological traits on chromosome 5D to be ultimately targeted for wheat improvement.
Similar content being viewed by others
References
Akhunov ED, Akhunova AR, Anderson OD et al (2010) Nucleotide diversity maps reveal variation in diversity among wheat genomes and chromosomes. BMC Genomics 11:702. doi:10.1186/1471-2164-11-702
Akpinar BA, Budak H (2016) Dissecting miRNAs in wheat D genome progenitor, Aegilops tauschii. Front Plant Sci 7:1–17. doi:10.3389/fpls.2016.00606
Akpinar BA, Yuce M, Lucas SJ et al (2015a) Molecular organization and comparative analysis of chromosome 5B of the wild wheat ancestor Triticum dicoccoides. Scientific Reports 5:Article number: 10763. doi:10.1038/srep10763
Akpinar BA, Lucas SJ, Vr J et al (2015b) Sequencing chromosome 5D of Aegilops tauschii and comparison with its allopolyploid descendant bread wheat ( Triticum aestivum ). Plant Biotechnol J 13:740–752. doi:10.1111/pbi.12302
Akpinar BA, Magni F, Yuce M et al (2015c) The physical map of wheat chromosome 5DS revealed gene duplications and small rearrangements. BMC Genomics 16:453. doi:10.1186/s12864-015-1641-y
Akpinar BA, Kantar M, Budak H (2015d) Root precursors of microRNAs in wild emmer and modern wheats show major differences in response to drought stress. Funct Integr Genomics 15:587. doi:10.1007/s10142-015-0453-0
Berkman PJ, Lai K, Lorenc MT, Edwards D (2012) Next-generation sequencing applications for wheat crop improvement. Am J Bot 99:365–371. doi:10.3732/ajb.1100309
Blechl AE, Anderson OD (1996) Expression of a novel high-molecular-weight glutenin subunit gene in transgenic wheat. Nat Biotechnol 14:875–879. doi:10.1038/nbt0796-875
Budak H, Kantar M (2015) Harnessing NGS and big data optimally: comparison of miRNA prediction from assembled versus non-assembled sequencing data—the case of the grass Aegilops tauschii complex genome. OMICS: A J Integr Biol 19(7):407–415. doi:10.1089/omi.2015.0038
Budak H, Baenziger PS, Beecher et al (2004) The effect of introgressions of wheat D-genome chromosomes of into ‘Presto’ tricale. Euphytica 137:261–270. doi:10.1023/B:EUPH.0000041590.55511.d0
Budak H, Shearman RC, Gulsen O et al (2005) Understanding ploidy complex and geographic origin of the Buchloe dactyloides genome using cytoplasmic and nuclear marker systems. Theor Appl Genet 111:1545–1552. doi:10.1007/s00122-005-0083-3
Budak H, Kantar M, Kurtoglu KY (2013a) Drought tolerance in modern and wild wheat. ScientificWorldJournal 2013:548246. doi:10.1155/2013/548246
Budak H, Akpinar BA, Unver T, Turktas M (2013b) Proteome changes in wild and modern wheat leaves upon drought stress by two-dimensional electrophoresis and nanoLC-ESI–MS/MS. Plant Mol Biol 83(1–2):89–103. doi:10.1007/s11103-013-0024-5
Budak H, Hussain B, Khan Z et al (2015) From genetics to functional genomics: improvement in drought signaling and tolerance in wheat. Front Plant Sci 6:1–13. doi:10.3389/fpls.2015.01012
Camacho C, Coulouris G, Avagyan V et al (2009) BLAST+: architecture and applications. BMC Bioinforma 10:421. doi:10.1186/1471-2105-10-421
Castillo A, Dorado G, Feuillet C, Sourdille P, Hernandez P (2010) Genetic structure and ecogeographical adaptation in wild barley (Hordeum chilense Roemer et Schultes) as revealed by microsatellite markers. BMC Plant Biol 10:266. doi:10.1186/1471-2229-10-266
Chantret N, Salse J, Sabot F et al (2005) Molecular basis of evolutionary events that shaped the hardness locus in diploid and polyploid wheat species (Triticum and Aegilops). Plant Cell 17:1033–1045. doi:10.1105/tpc.104.029181
Cloutier S, McCallum BD, Loutre C et al (2007) Leaf rust resistance gene Lr1, isolated from bread wheat (Triticum aestivum L.) is a member of the large psr567 gene family. Plant Mol Biol 65:93–106. doi:10.1007/s11103-007-9201-8
Conesa A, Götz S (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics 2008:619832. doi:10.1155/2008/619832
Dvorák J, Luo MC, Yang ZL (1998) Restriction fragment length polymorphism and divergence in the genomic regions of high and low recombination in self-fertilizing and cross-fertilizing aegilops species. Genetics 148:423–434
Dvorak J, Luo MC, Akhunov ED (2011) N.I. Vavilov’s theory of centres of diversity in the light of current understanding of wheat diversity, domestication and evolution
Galaeva MV, Fayt VI, Chebotar SV et al (2013) Association of microsatellite loci alleles of the group-5 of chromosomes and the frost resistance of winter wheat. Cytol Genet 47:261–267. doi:10.3103/S0095452713050046
Hong MJ, Kim DY, Seo YW (2013) SKP1-like-related genes interact with various F-box proteins and may form SCF complexes with Cullin–F-box proteins in wheat. Mol Biol Rep 40:969–981. doi:10.1007/s11033-012-2139-1
Iehisa JCM, Shimizu A, Sato K et al (2012) Discovery of high-confidence single nucleotide polymorphisms from large-scale de novo analysis of leaf transcripts of Aegilops tauschii, a wild wheat progenitor. DNA Res 19:487–497. doi:10.1093/dnares/dss028
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. doi:10.1038/nature12028
Kippes N, Debernardi JM, Vasquez-Gross HA et al (2015) Identification of the VERNALIZATION 4 gene reveals the origin of spring growth habit in ancient wheats from South Asia. Proc Natl Acad Sci U S A 112:E5401–E5410. doi:10.1073/pnas.1514883112
Kumar A, Seetan R, Mergoum M et al (2015) Radiation hybrid maps of the D-genome of Aegilops tauschii and their application in sequence assembly of large and complex plant genomes. BMC Genomics 16:800. doi:10.1186/s12864-015-2030-2
Kurtoglu KY, Kantar M, Lucas SJ et al (2013) Unique and conserved microRNAs in wheat chromosome 5D revealed by next-generation sequencing. PLoS One 8(7):e69801. doi:10.1371/journal.pone.0069801
Kuzuoglu-Ozturk D, Yalcinkaya O, Akpinar BA et al (2012) Autophagy-related gene, TdAtg8, in wild emmer wheat plays a role in drought and osmotic stress response. Planta 236:1081–1092. doi:10.1007/s00425-012-1657-3
Leach LJ, Belfield EJ, Jiang C, Brown C, Mithani A, Harberd NP (2014) Patterns of homoeologous gene expression shown by RNA sequencing in hexaploid bread wheat. BMC Genomics 15:276. doi:10.1186/1471-2164-15-276
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760. doi:10.1093/bioinformatics/btp324
Li H, Handsaker B, Wysoker A et al (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079. doi:10.1093/bioinformatics/btp352
Li A, Liu D, Wu J et al (2014) mRNA and small RNA transcriptomes reveal insights into dynamic homoeolog regulation of allopolyploid heterosis in nascent hexaploid wheat. Plant Cell 26(5):1878–1900. doi:10.1105/tpc.114.124388
Lin R, Ding L, Casola C, et al. (2007) Transposase-derived transcription factors regulate light signaling in Arabidopsis
Liu Y, Wang L, Deng M et al (2015a) Genome-wide association study of phosphorus-deficiency-tolerance traits in Aegilops tauschii. Theor Appl Genet 128:2203–2212. doi:10.1007/s00122-015-2578-x
Liu Y, Wang L, Mao S et al (2015b) Genome-wide association study of 29 morphological traits in Aegilops tauschii. Sci Rep 5:15562. doi:10.1038/srep15562
Lorenc MT, Hayashi S, Stiller J et al (2012) Discovery of single nucleotide polymorphisms in complex genomes using SGSautoSNP. Biology (Basel) 1:370–382. doi:10.3390/biology1020370
Lucas SJ, Durmaz E, Akpinar BA et al (2011a) The drought response displayed by a DRE binding protein from Triticum dicocoides. Plant Physiol Bioechem 49:346–352. doi:10.1016/j.plaphy.2011.01.016
Lucas SJ, Dogan E, Budak H (2011b) TMPIT1 from wild emmer wheat: first characterisation of a stress-inducible integral membrane protein. Gene 483:22–28. doi:10.1016/j.gene.2011.05.003
Lucas SJ, Simkova H, Safar J et al (2012) Functional features of a single chromosome arm in wheat (1AL) determined from its structure. Funct Integ Genomics 12:173. doi:10.1007/s10142-011-0250-3
Lucas SJ, Akpınar BA, Simková H et al (2014) Next-generation sequencing of flow-sorted wheat chromosome 5D reveals lineage-specific translocations and widespread gene duplications. BMC Genomics 15:1–18. doi:10.1186/1471-2164-15-1080
Luo M, Gu YQ, You FM, et al. (2013) A 4-gigabase physical map unlocks the structure and evolution of the complex genome of Aegilops tauschii, the wheat D-genome progenitor. PNAS. doi:10.1073/pnas.1219082110
Mammadov J, Aggarwal R, Buyyarapu R et al (2012) SNP markers and their impact on plant breeding. Int J Plant Genomics 2012:728398. doi:10.1155/2012/728398
Mayer KFX, Rogers J, Dolezel J et al (2014) A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345(6194):1251788–1251788. doi:10.1126/science.1251788
Mizuno N, Yamasaki M, Matsuoka Y et al (2010) Population structure of wild wheat D-genome progenitor Aegilops tauschii Coss.: implications for intraspecific lineage diversification and evolution of common wheat. Mol Ecol 19:999–1013. doi:10.1111/j.1365-294X.2010.04537.x
Mochida K, Shinozaki K (2013) Unlocking Triticeae genomics to sustainably feed the future. Plant Cell Physiol 54:1931–1950. doi:10.1093/pcp/pct163
Morris CF (2002) Puroindolines: the molecular genetic basis of wheat grain hardness. Plant Mol Biol 48:633–647
Nevo E, Chen G (2010) Drought and salt tolerances in wild relatives for wheat and barley improvement. Plant Cell Environ 33:670–685. doi:10.1111/j.1365-3040.2009.02107.x
Ning S-Z, Chen Q-J, Yuan Z-W et al (2009) Characterization of WAP2 gene in Aegilops tauschii and comparison with homoeologous loci in wheat. J Syst Evol 47:543–551. doi:10.1111/j.1759-6831.2009.00048.x
Paux E, Sourdille P, Mackay I, Feuillet C (2012) Sequence-based marker development in wheat: advances and applications to breeding. Biotechnol Adv 30:1071–1088. doi:10.1016/j.biotechadv.2011.09.015
Quarrie SA, Steed A, Calestani C et al (2005) A high-density genetic map of hexaploid wheat (Triticum aestivum L.) from the cross Chinese Spring x SQ1 and its use to compare QTLs for grain yield across a range of environments. Theor Appl Genet 110:865–880. doi:10.1007/s00122-004-1902-7
Shen JC, Rideout WM, Jones PA (1994) The rate of hydrolytic deamination of 5-methylcytosine in double-stranded DNA. Nucleic Acids Res 22:972–976
Tam PP, Barrette-Ng IH, Simon DM et al (2010) The Puf family of RNA-binding proteins in plants: phylogeny, structural modeling, activity and subcellular localization. BMC Plant Biol 10:44. doi:10.1186/1471-2229-10-44
Thomson MJ (2014) High-throughput SNP genotyping to accelerate crop improvement. Plant Breed Biotechnol 2:195–212. doi:10.9787/PBB.2014.2.3.195
Wang J, Luo MC, Chen Z et al (2013) Aegilops tauschii single nucleotide polymorphisms shed light on the origins of wheat D-genome genetic diversity and pinpoint the geographic origin of hexaploid wheat. New Phytol 198:925–937. doi:10.1111/nph.12164
Wang Z, Li H, Zhang D et al (2015) Genetic and physical mapping of powdery mildew resistance gene MlHLT in Chinese wheat landrace Hulutou. Theor Appl Genet 128:365–373. doi:10.1007/s00122-014-2436-2
Winfield MO, Allen AM, Burridge AJ et al (2015) High-density SNP genotyping array for hexaploid wheat and its secondary and tertiary gene pool. Plant Biotechnol J n/a-n/a. doi:10.1111/pbi.12485
Yoshida T, Nishida H, Zhu J et al (2010) Vrn-D4 is a vernalization gene located on the centromeric region of chromosome 5D in hexaploid wheat. Theor Appl Genet 120:543–552. doi:10.1007/s00122-009-1174-3
You FM, Luo M-C, Xu K et al (2010) A new implementation of high-throughput five-dimensional clone pooling strategy for BAC library screening. BMC Genomics 11:692. doi:10.1186/1471-2164-11-692
You FM, Huo N, Deal KR et al (2011) Annotation-based genome-wide SNP discovery in the large and complex Aegilops tauschii genome using next-generation sequencing without a reference genome sequence. BMC Genomics 12:59. doi:10.1186/1471-2164-12-59
Zhang J, Wang Y, Wu S et al (2012) A single nucleotide polymorphism at the Vrn-D1 promoter region in common wheat is associated with vernalization response. Theor Appl Genet 125:1697–1704. doi:10.1007/s00122-012-1946-z
Acknowledgements
We thank Dr. Istvan Molnar (Agricultural Institute, Centre for Agricultural Research, Martonvasar, Hungary) for providing Ae. tauschii accession MvGB589.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Funding
This work funded by Montana Plant Science Endowment, Montana State University and Sabanci University.
Electronic supplementary material
Supplementary Table S1
(XLSX 14593 kb)
Rights and permissions
About this article
Cite this article
Akpinar, B.A., Lucas, S. & Budak, H. A large-scale chromosome-specific SNP discovery guideline. Funct Integr Genomics 17, 97–105 (2017). https://doi.org/10.1007/s10142-016-0536-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10142-016-0536-6