Abstract
Nutritional benefits of cultivated oat (Avena sativa L., 2n = 6x = 42, AACCDD) are well recognized; however, seed protein levels are modest and resources for genetic improvement are scarce. The wild tetraploid, A. magna Murphy et Terrell (syn A. maroccana Gdgr., 2n = 4x = 28, CCDD), which contains approximately 31% seed protein, was hybridized with cultivated oat to produce a domesticated A. magna. Wild and cultivated accessions were crossed to generate a recombinant inbred line (RIL) population. Although these materials could be used to develop domesticated, high-protein oat, mapping and quantitative trait loci introgression is hindered by a near absence of genetic markers. Objectives of this study were to develop high-throughput, A. magna-specific markers; generate a genetic linkage map based on the A. magna RIL population; and map genes controlling oat domestication. A Diversity Arrays Technology (DArT) array derived from 10 A. magna genotypes was used to generate 2,688 genome-specific probes. These, with 12,672 additional oat clones, produced 2,349 polymorphic markers, including 498 (21.2%) from A. magna arrays and 1,851 (78.8%) from other Avena libraries. Linkage analysis included 974 DArT markers, 26 microsatellites, 13 SNPs, and 4 phenotypic markers, and resulted in a 14-linkage-group map. Marker-to-marker correlation coefficient analysis allowed classification of shared markers as unique or redundant, and putative linkage-group-to-genome anchoring. Results of this study provide for the first time a collection of high-throughput tetraploid oat markers and a comprehensive map of the genome, providing insights to the genome ancestry of oat and affording a resource for study of oat domestication, gene transfer, and comparative genomics.
Similar content being viewed by others
References
Acevedo M, Jackson EW, Chong J, Rines HW, Harrison S, Bonman JM (2010) Identification and validation of quantitative trait loci for partial resistance to crown rust in oat. Phytopathology 100:511–521
Akbari M, Wenzl P, Caig V, Carling J, Xia L, Yang S, Uszynski G, Mohler V, Lehmensiek A, Kuchel H, Hayden MJ, Howes N, Sharp P, Vaughan P, Rathmell B, Huttner E, Kilian A (2006) Diversity arrays technology (DArT) for high-throughput profiling of the hexaploid wheat genome. Theor Appl Genet 113:1409–1420
Baum BR (1972) Material for international oat register. Cat No A52-4772
Braaten JT, Wood PJ, Scott FW, Wolynetz MS, Lowe MK, Bradley-White P, Collins MW (1994) Oat beta-glucan reduces blood cholesterol concentration in hypercholesterolemic subjects. Eur J Clin Nutr 48:465–474
Brown CM, Jedlinski H (1983) Ogle spring oat. Crop Sci 23:1012
Cheng Z, Presting GG, Buell CR, Wing RA, Jiang J (2001) High-resolution pachytene chromosome mapping of bacterial artificial chromosomes anchored by genetic markers reveals the centromere location and the distribution of genetic recombination along chromosome 10 of rice. Genetics 157:1749–1757
Chong J, Reimer E, Somers D, Aung T, Penner GA (2004) Development of sequence-characterized amplified region (SCAR) markers for resistance gene Pc94 to crown rust in oat. Can J Plant Path 26:89–96
Distelfeld A, Uauy C, Fahima T, Dubcovsky J (2006) Physical map of wheat high-grain protein content gene Gpc-B1 and development of a high-throughput molecular marker. New Phytolog 169:753–763
Duerst RD, Kaeppler HF, Forsberg RA (1999) Registration of ‘Gem’ oat. Crop Sci 39:879–880
Dumlupinar Z, Jellen EN, Anderson J, Bonman JM, Carson M, Chao S, Obert DE, Hu G, Jackson EW (2011) The art of attrition: Development of robust oat microsatellites (unpublished)
Eggum BO, Hansen I, Larsen T (1989) Protein quality and digestible energy of selected food determined in balanced trials with rats. Plant Foods Hum Nutr 39:13–21
Gardner KM, Latta RG (2006) Identifying loci under selection across contrasting environments in Avena barbata using quantitative trait locus mapping. Mol Ecol 15:1321–1333
Groh S, Zacharias A, Kianian SF, Penner GA, Chong J, Rines HW, Phillips RL (2001) Comparative AFLP mapping in two hexaploid oat populations. Theor Appl Genet 102:876–884
Harlan JR, DeWet JMJ, Price EG (1973) Comparative evolution of cereals. Evolution 27:311–325
Hoffman DL, Chong J, Jackson EW, Obert DE (2006) Characterization and mapping of a crown rust resistance gene complex (Pc58) in TAM O-301. Crop Sci 46:2630–2635
Jaccoud D, Peng K, Feinstein D, Kilian A (2001) Diversity arrays: a solid state technology for sequence information independent genotyping. Nucleic Acids Res 29:E25
Jackson EW, Obert DE, Menz M, Hu G, Avant JB, Chong J, Bonman JM (2007) Characterization and mapping of oat crown rust resistance genes using three assessment methods. Phytopathology 97:1063–1070
Jackson E, Jellen E, Oliver R, Lazo G, Tinker N, Rossnagel B, Anderson J, Bonman JM (2009) Resolving the oat mapping story by weaving together a consensus map. In: Tinker NA (ed) Proc Plant Animal Gen Conf XVII, San Diego, W337
Jackson EW, Obert DE, Avant JB, Harrison SA, Chong J, Carson ML, Bonman JM (2010) Quantitative trait loci in the Ogle/TAM O-301 oat mapping population controlling resistance to Puccinia coronata in the field. Phytopathology 100:484–492
Jellen EN, Ladizinsky G (2000) Giemsa C-banding in Avena insularis Ladizinsky. Genet Res Crop Evol 47:227–230
Jellen EN, Phillips RL, Rines HW (1993) C-banded karyotypes and polymorphisms in hexaploid oat accessions (Avena spp.) using Wright’s stain. Genome 36:1129–1137
Jones DB, Caldwell A, Widness KD (1948) Comparative growth-promoting values of the proteins of cereal grains. Cereal Chem 35:639–649
Kato A (1999) Air drying method using nitrous oxide for chromosome counting in maize. Biotech Histochem 74:160–166
Korol A, Mester D, Frenkel Z, Ronin Y (2009) Methods for genetic analysis in the Triticeae. In: Feuillet C, Muehlbauer GJ (eds) Genetics and genomics of the Triticeae, 1st edn. Springer, New York, pp 163–199
Kremer CA, Lee M, Holland JB (2001) A restriction fragment length polymorphism based linkage map of a diploid Avena recombinant inbred line population. Genome 4:192–204
Künzel G, Korzun L, Meister A (2000) Cytologically integrated physical restriction fragment length polymorphism maps for the barley genome based on translocation breakpoints. Genetics 154:397–412
Ladizinsky G (1995) Domestication via hybridization of the wild tetraploid oats Avena magna and A. murphyi. Theor Appl Genet 91:639–646
Ladizinsky G (2000) A synthetic hexaploid (2n = 42) oat from the cross of Avena strigosa (2n = 14) and domesticated A. magna (2n = 28). Euphytica 116:231–235
Ladizinsky G, Fainstein R (1977) Domestication of the protein-rich tetraploid wild oats Avena magna and A. murphyi. Euphytica 26:221–223
Li CD, Rossnagel BG, Scoles GJ (2000) The development of oat microsatellite markers and their use in identifying relationships among Avena species and oat cultivars. Theor Appl Genet 101:1259–1268
Linares C, Vega C, Ferrer E, Fominaya A (1992) Identification of C-banded chromosomes in meiosis and the analysis of nucleolar activity in Avena byzantine C. Koch cv ‘Kanota’. Theor Appl Genet 83:650–654
Linares C, Ferrer E, Fominaya A (1998) Discrimination of the closely related A and D genomes of the hexaploid oat Avena sativa L. Proc Natl Acad Sci USA 95:12450–12455
Lukaszewski AJ, Curtis CA (1993) Physical distribution of recombination in B-genome chromosomes of tetraploid wheat. Theor Appl Genet 86:121–127
McDaniel ME (1974) Registration of TAM O-301 oat. Crop Sci 14:127–128
McFerson JK, Frey KJ (1991) Recurrent selection for protein yield of oat. Crop Sci 31:1–8
McMullen MS, Doehlert DC, Miller JD (2005) Registration of ‘HiFi’ oat. Crop Sci 45:1664
Mester D, Ronin Y, Minkov D, Nevo E, Korol A (2003) Constructing large-scale genetic maps using an evolutionary strategy algorithm. Genetics 165:2269–2282
Mester DI, Ronin YI, Nevo E, Korol AB (2004) Fast and high precision algorithms for optimization in large-scale genomic problems. Comput Biol Chem 28:281–290
Middleton GK (1938) Inheritance in a cross between Avena sativa and Avena sterilis ludoviciana. J Am Soc Agron 30:193–208
Morishima H (1984) Wild plants and domestication. In: Tsunoda S, Takahashi N (eds) Biology of rice. Jap Sci Press/Elsevier, Tokyo/Amsterdam, pp 3–30
Nutall FQ, Mooradian AD, Gannon MC, Billington C, Krezowsi P (1984) Effect of protein ingestion on the glucose and insulin response to a standardized oral glucose load. Diabetes Care 7:465–470
O’Donoughue LS, Wang Z, Röder M, Kneen B, Leggett M, Sorrells ME, Tanksley SD (1992) An RFLP-based linkage map of oats based on a cross between two diploid taxa (Avena atlantica × A. hirtula). Genome 35:765–771
Ohm HW, Shaner G (1992) Breeding oat for resistance to diseases. In: Marshall HG, Sorrells ME (eds) Oat science and technology. Amer Soc Agron, Madison, WI, pp 657–698
Oliver RE, Obert DE, Hu G, Bonman JM, O’Leary-Jepsen E, Jackson EW (2010) Development of oat-based markers from barley and wheat microsatellites. Genome 53:458–471
Oliver RE, Lazo GR, Lutz JD, Rubenfield MJ, Tinker NA, Anderson JM, Wisniewski-Morehead MH, Adhikary D, Jellen EN, Maughan PJ, Brown-Guedira GL, Chao S, Beattie AD, Carson ML, Rines HW, Obert DE, Bonman JM, Jackson EW (2011) Model SNP development based on the complex oat genome using high-throughput 454 sequencing technology. BMC Genomics 12:77
Orr W, Molnar SJ (2008) Development of PCR-based SCAR and CAPS markers linked to β-glucan and protein content QTL regions in oat. Genome 51:421–425
Pal N, Sandhu JS, Domier LL, Kolb FL (2002) Development and characterization of microsatellite and RFLP-derived PCR markers in oat. Crop Sci 42:912–918
Paterson AH, Lin YR, Li Z, Schertz KF, Doebley JF, Pinson SRM, Liu SC, Stansel JW, Irvine JE (1995) Convergent domestication of cereal crops by independent mutations at corresponding genetic loci. Science 269:1714–1718
Peng J, Korol AM, Fahima T, Röder MS, Ronin YI, Li YC, Nevo E (2000) Molecular genetic maps in wild emmer wheat, Triticum dicoccoides: genome-wide coverage, massive negative interference, and putative quasi-linkage. Genome Res 10:1509–1531
Peng J, Ronin Y, Fahima T, Röder MS, Li Y, Nevo E, Korol A (2003) Domestication quantitative trait loci in Triticum dicoccoides, the progenitor of wheat. Proc Natl Acad Sci USA 100:2489–2494
Poncet V, Lamy F, Devos KM, Gale MD, Sarr A, Robert T (2000) Genetic control of domestication traits in pearl millet (Pennisetum glaucum L., Poaceae). Theor Appl Genet 100:147–159
Sandhu D, Gill KS (2002) Gene-containing regions of wheat and the other grass genomes. Plant Physiol 128:803–811
Stanton TR (1955) Oat identification and classification. USDA-ARS Tech Bull No 1100. US Govt Print Office, Washington
Stewart VR, Wesenberg DM, Hayes RM, Petr FC (1978) Registration of Otana oats. Crop Sci 18:693
Thomas H (1992) Breeding oat for resistance to diseases. In: Marshall HG, Sorrells ME (eds) Oat science and technology. Amer Soc Agron, Madison, WI, pp 473–507
Tinker NA, Kilian A, Wight CP, Heller-Uszynska K, Wenzyl P, Rines HW, Bjørnstad Å, Howarth CJ, Jannink J-L, Anderson JM, Rossnagel BG, Stuthman DD, Sorrells ME, Jackson EW, Tuvesson S, Kolb FL, Olsson O, Federizzi LC, Carson ML, Ohm HW, Molnar SJ, Scoles GJ, Eckstein PE, Bonman MJ, Ceplitis A, Langdon T (2009) New DArT markers for oat provide enhanced map coverage and global germplasm characterization. BMC Genomics 10:39
Wang YF, Yancy WS, Yu D, Champagne C, Appel LJ, Lin P-H (2008) The relationship between dietary protein intake and blood pressure: results from the PREMIER study. J Human Hypertens 22:745–754
Ward JH (1963) Hierarchical grouping to optimize an objective function. J Am Stat Assoc 58:236–244
Wenzl P, Carling J, Kudrna D, Jaccoud D, Huttner E, Kleinhofs A, Kilian A (2004) Diversity Arrays Technology (DArT) for whole-genome profiling of barley. Proc Natl Acad Sci USA 101:9915–9920
Wenzl P, Li H, Carling J, Zhou M, Raman H, Paul E, Hearnden P, Maier C, Xia L, Caig V, Ovesná J, Cakir M, Poulsen D, Wang J, Raman R, Smith KP, Muehlbauer GJ, Chalmers KJ, Kleinhofs A, Huttner E, Kilian A (2006) A high-density consensus map of barley linking DArT markers to SSR, RFLP and STS loci and agricultural traits. BMC Genomics 7:206
Werner JE, Endo TR, Gill BS (1992) Toward a cytogenetically based physical map of the wheat genome. Proc Natl Acad Sci USA 89:11307–11311
Wight CP, Tinker NA, Kianian SF, Sorrells ME, O’Donoughue LS, Hoffman DL, Groh S, Scoles GJ, Li CD, Webster FH, Phillips RL, Rines HW, Livingston SM, Armstrong KC, Fedak G, Molnar SJ (2003) A molecular marker map in ‘Kanota’ × ‘Ogle’ hexaploid oat (Avena spp.) enhanced by additional markers and a robust framework. Genome 46:28–47
Wu K-S, Tanksley TD (1993) Genetic and physical mapping of telomeres and macrosatellites of rice. Plant Mol Biol 22:861–872
Xiong LZ, Liu KD, Dai XK, Xu CG, Zhang Q (1999) Identification of genetic factors controlling domestication-related traits of rice using and F2 population of a cross between Oryza sativa and O. rufipogon. Theor Appl Genet 98:243–251
Yan H, Kikuchi S, Neumann P, Zhang W, Wu Y, Chen F, Jiang J (2010) Genome-wide mapping of cytosine methylation revealed dynamic DNA methylation patterns associated with genes and centromeres in rice. Plant J 63:353–365
Young VR, Pellett PL (1994) Plant proteins in relation to human protein and amino acid nutrition. Am J Clin Nutr 59:1203S–1212S
Young WP, Schupp JM, Keim P (1999) DNA methylation and AFLP marker distribution in the soybean genome. Theor Appl Genet 99:785–790
Zhu S, Rossnagel BG, Kaeppler HF (2004) Genetic analysis of quantitative trait loci for groat protein and oil content in oat. Crop Sci 44:254–260
Acknowledgments
We appreciate the excellent technical assistance of Robert Campbell in SSR development and mapping and Irene Shackelford in maintenance of the BAM population. We also thank Dr. Steven Harrison for RIL seed increase.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by A. Schulman.
Electronic supplementary material
Below is the link to the electronic supplementary material.
122_2011_1656_MOESM1_ESM.xls
Online Resource 1. Segregation data and polymorphic information content (PIC) values for 214 markers across the BAM population (XLS 101 kb)
122_2011_1656_MOESM2_ESM.doc
Online Resource 2. Heat plots generated by marker-to-marker correlation coefficients. Outlined markers represent loci containing minor alleles (DOC 1305 kb)
Rights and permissions
About this article
Cite this article
Oliver, R.E., Jellen, E.N., Ladizinsky, G. et al. New Diversity Arrays Technology (DArT) markers for tetraploid oat (Avena magna Murphy et Terrell) provide the first complete oat linkage map and markers linked to domestication genes from hexaploid A. sativa L.. Theor Appl Genet 123, 1159–1171 (2011). https://doi.org/10.1007/s00122-011-1656-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-011-1656-y