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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.

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.

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References

  1. 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

    PubMed  Article  CAS  Google Scholar 

  2. 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

    PubMed  Article  CAS  Google Scholar 

  3. Baum BR (1972) Material for international oat register. Cat No A52-4772

  4. 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

    PubMed  CAS  Google Scholar 

  5. Brown CM, Jedlinski H (1983) Ogle spring oat. Crop Sci 23:1012

    Google Scholar 

  6. 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

    PubMed  CAS  Google Scholar 

  7. 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

    Article  CAS  Google Scholar 

  8. 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

    Article  CAS  Google Scholar 

  9. Duerst RD, Kaeppler HF, Forsberg RA (1999) Registration of ‘Gem’ oat. Crop Sci 39:879–880

    Article  Google Scholar 

  10. 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)

  11. 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

    PubMed  Article  CAS  Google Scholar 

  12. 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

    PubMed  Article  CAS  Google Scholar 

  13. 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

    Article  CAS  Google Scholar 

  14. Harlan JR, DeWet JMJ, Price EG (1973) Comparative evolution of cereals. Evolution 27:311–325

    Article  Google Scholar 

  15. 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

    Article  CAS  Google Scholar 

  16. 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

    PubMed  Article  CAS  Google Scholar 

  17. 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

    PubMed  Article  CAS  Google Scholar 

  18. 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

  19. 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

    PubMed  Article  CAS  Google Scholar 

  20. Jellen EN, Ladizinsky G (2000) Giemsa C-banding in Avena insularis Ladizinsky. Genet Res Crop Evol 47:227–230

    Article  Google Scholar 

  21. 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

    PubMed  Article  CAS  Google Scholar 

  22. Jones DB, Caldwell A, Widness KD (1948) Comparative growth-promoting values of the proteins of cereal grains. Cereal Chem 35:639–649

    CAS  Google Scholar 

  23. Kato A (1999) Air drying method using nitrous oxide for chromosome counting in maize. Biotech Histochem 74:160–166

    PubMed  Article  CAS  Google Scholar 

  24. 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

    Google Scholar 

  25. 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

    Google Scholar 

  26. 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

    PubMed  Google Scholar 

  27. Ladizinsky G (1995) Domestication via hybridization of the wild tetraploid oats Avena magna and A. murphyi. Theor Appl Genet 91:639–646

    Article  Google Scholar 

  28. 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

    Article  Google Scholar 

  29. Ladizinsky G, Fainstein R (1977) Domestication of the protein-rich tetraploid wild oats Avena magna and A. murphyi. Euphytica 26:221–223

    Article  Google Scholar 

  30. 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

    Article  CAS  Google Scholar 

  31. 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

    Article  Google Scholar 

  32. 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

    PubMed  Article  CAS  Google Scholar 

  33. Lukaszewski AJ, Curtis CA (1993) Physical distribution of recombination in B-genome chromosomes of tetraploid wheat. Theor Appl Genet 86:121–127

    Article  CAS  Google Scholar 

  34. McDaniel ME (1974) Registration of TAM O-301 oat. Crop Sci 14:127–128

    Article  Google Scholar 

  35. McFerson JK, Frey KJ (1991) Recurrent selection for protein yield of oat. Crop Sci 31:1–8

    Article  CAS  Google Scholar 

  36. McMullen MS, Doehlert DC, Miller JD (2005) Registration of ‘HiFi’ oat. Crop Sci 45:1664

    Article  Google Scholar 

  37. 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

    PubMed  CAS  Google Scholar 

  38. 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

    PubMed  Article  CAS  Google Scholar 

  39. Middleton GK (1938) Inheritance in a cross between Avena sativa and Avena sterilis ludoviciana. J Am Soc Agron 30:193–208

    Article  Google Scholar 

  40. 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

    Google Scholar 

  41. 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

    Article  Google Scholar 

  42. 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

    Article  Google Scholar 

  43. 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

  44. 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

    PubMed  Article  CAS  Google Scholar 

  45. 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

    PubMed  Article  CAS  Google Scholar 

  46. 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

    PubMed  Article  CAS  Google Scholar 

  47. 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

    Article  CAS  Google Scholar 

  48. 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

    PubMed  Article  CAS  Google Scholar 

  49. 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

    PubMed  Article  CAS  Google Scholar 

  50. 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

    PubMed  Article  CAS  Google Scholar 

  51. 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

    Article  CAS  Google Scholar 

  52. Sandhu D, Gill KS (2002) Gene-containing regions of wheat and the other grass genomes. Plant Physiol 128:803–811

    PubMed  Article  CAS  Google Scholar 

  53. Stanton TR (1955) Oat identification and classification. USDA-ARS Tech Bull No 1100. US Govt Print Office, Washington

    Google Scholar 

  54. Stewart VR, Wesenberg DM, Hayes RM, Petr FC (1978) Registration of Otana oats. Crop Sci 18:693

    Article  Google Scholar 

  55. 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

  56. 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

    PubMed  Article  Google Scholar 

  57. 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

    Article  CAS  Google Scholar 

  58. Ward JH (1963) Hierarchical grouping to optimize an objective function. J Am Stat Assoc 58:236–244

    Article  Google Scholar 

  59. 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

    PubMed  Article  CAS  Google Scholar 

  60. 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

    PubMed  Article  Google Scholar 

  61. 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

    PubMed  Article  CAS  Google Scholar 

  62. 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

    PubMed  Article  CAS  Google Scholar 

  63. Wu K-S, Tanksley TD (1993) Genetic and physical mapping of telomeres and macrosatellites of rice. Plant Mol Biol 22:861–872

    PubMed  Article  CAS  Google Scholar 

  64. 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

    Article  CAS  Google Scholar 

  65. 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

    Article  CAS  Google Scholar 

  66. Young VR, Pellett PL (1994) Plant proteins in relation to human protein and amino acid nutrition. Am J Clin Nutr 59:1203S–1212S

    PubMed  CAS  Google Scholar 

  67. Young WP, Schupp JM, Keim P (1999) DNA methylation and AFLP marker distribution in the soybean genome. Theor Appl Genet 99:785–790

    Article  CAS  Google Scholar 

  68. 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

    Article  CAS  Google Scholar 

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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.

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Correspondence to E. N. Jellen.

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Communicated by A. Schulman.

Electronic supplementary material

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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)

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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 (2011). https://doi.org/10.1007/s00122-011-1656-y

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Keywords

  • Linkage Group
  • Cetyl Trimethyl Ammonium Bromide
  • Recombinant Inbred Line Population
  • DArT Marker
  • Diversity Array Technology