One hundred years of comparative genetic and physical mapping in cultivated oat (Avena sativa)
Charlene P. Wight A * , Victoria C. Blake B C , Eric N. Jellen D , Eric Yao B E , Taner Z. Sen B E and Nicholas A. Tinker AA
B
C
D
E
Abstract
Researchers have been accumulating information concerning the locations of genes and quantitative trait loci (QTLs) in cultivated oat (Avena sativa L.) for more than 100 years.
The aim of this work was to create an inventory of genes and QTLs found in cultivated hexaploid oat and produce tools to make this resource more useful.
By using the positions of perfectly matched, single nucleotide polymorphism markers, each centimorgan (cM) location along the consensus map was assigned to a location on the OT3098 v2 physical map found on the GrainGenes database website (https://wheat.pw.usda.gov/jb/?data=/ggds/oat-ot3098v2-pepsico). This information was then used to assign physical locations to the genes and QTLs in the inventory, where possible.
A table comparing the major genetic maps of hexaploid oats to each other, to the 2018 oat consensus map, and to physical chromosomes was produced. Genome browser tracks aligning the consensus map regions and the locations of the genes and QTLs to OT3098 v2 were added to GrainGenes.
Many oat genes and QTLs identified using genetic mapping could be assigned positions on physical oat chromosomes. However, many of these assigned regions are quite long, owing to the presence of large areas of reduced recombination. Specific examples of identified patterns of recombination between the genetic and physical maps and validated gene and QTL locations are discussed.
These resources will assist researchers performing comparative genetic and physical mapping in oat.
Keywords: Avena, comparative mapping, curation, genes, genetic maps, molecular markers, oat, quantitative trait loci.
References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403-410.
| Crossref | Google Scholar | PubMed |
Bekele WA, Wight CP, Chao S, Howarth CJ, Tinker NA (2018) Haplotype-based genotyping-by-sequencing in oat genome research. Plant Biotechnology Journal 16, 1452-1463.
| Crossref | Google Scholar | PubMed |
Blake VC, Woodhouse MR, Lazo GR, et al. (2019) GrainGenes: centralized small grain resources and digital platform for geneticists and breeders. Database 2019, baz065.
| Crossref | Google Scholar |
Blake VC, Wight CP, Yao E, Sen TZ (2022) GrainGenes: Tools and content to assist breeders improving oat quality. Foods 11, 914.
| Crossref | Google Scholar | PubMed |
Brzozowski LJ, Hu H, Campbell MT, Broeckling CD, Caffe M, Gutiérrez L, Smith KP, Sorrells ME, Gore MA, Jannink J-L (2022) Selection for seed size has uneven effects on specialized metabolite abundance in oat (Avena sativa L.). G3 Genes|Genomes|Genetics 12, jkab419.
| Crossref | Google Scholar |
Bush AL, Wise RP (1996) Crown rust resistance loci on linkage groups 4 and 13 in cultivated oat. Journal of Heredity 87, 427-432.
| Crossref | Google Scholar |
Chaffin AS, Huang YY, Smith S, Bekele WA, Babiker E, Gnanesh BN, Foresman BJ, Blanchard SG, Jay JJ, Reid RW, Wight CP, Chao S, Oliver R, Islamovic E, Kolb FL, McCartney C, Mitchell Fetch JW, Beattie AD, Bjørnstad Å, Bonman JM, Langdon T, Howarth CJ, Brouwer CR, Jellen EN, Klos KE, Poland JA, Hsieh T-F, Brown R, Jackson E, Schlueter JA, Tinker NA (2016) A consensus map in cultivated hexaploid oat reveals conserved grass synteny with substantial subgenome rearrangement. Plant Genome 9, 1-21.
| Crossref | Google Scholar |
Cheng DW, He S, Armstrong KC (2002) Modified expression of two receptor kinase genes in hexaploid oat (Avena sativa L.) on inoculation with crown rust. Physiological and Molecular Plant Pathology 61, 281-288.
| Crossref | Google Scholar |
Chong J, Howes NK, Brown PD, Harder DE (1994) Identification of the stem rust resistance gene Pg9 and its association with crown rust resistance and endosperm proteins in ‘Dumont’ oat. Genome 37, 440-447.
| Crossref | Google Scholar | PubMed |
Esvelt Klos K, Yimer BA, Babiker EM, Beattie AD, Bonman JM, Carson ML, Chong J, Harrison SA, Ibrahim AMH, Kolb FL, McCartney CA, McMullen M, Mitchell Fetch J, Mohammadi M, Murphy JP, Tinker NA (2017) Genome-wide association mapping of crown rust resistance in oat elite germplasm. Plant Genome 10, plantgenome2016.10.0107.
| Crossref | Google Scholar |
Fang Z, Polacco M, Chen S, Schroeder S, Hancock D, Sanchez H, Coe E (2003) cMap: the comparative genetic map viewer. Bioinformatics 19, 416-417.
| Crossref | Google Scholar | PubMed |
Fogarty MC, Smith SM, Sheridan JL, Hu G, Islamovic E, Reid R, Jackson EW, Maughan PJ, Ames NP, Jellen EN, Hsieh T-F (2020) Identification of mixed linkage β-glucan quantitative trait loci and evaluation of AsCslF6 homoeologs in hexaploid oat. Crop Science 60, 914-933.
| Crossref | Google Scholar |
Fox SL, Jellen EN, Kianian SF, Rines HW, Phillips RL (2001) Assignment of RFLP linkage groups to chromosomes using monosomic F1 analysis in hexaploid oat. Theoretical and Applied Genetics 102, 320-326.
| Crossref | Google Scholar |
Fraser AC (1919) The inheritance of the weak awn in certain Avena crosses and its relation to other characters of the oat grain. Cornell University Agricultural Experiment Station Memoirs 23, 635-676.
| Google Scholar |
Hacker JB, Riley R (1965) Morphological and cytological effects of chromosome deficiency in Avena sativa. Canadian Journal of Genetics and Cytology 7, 304-315.
| Crossref | Google Scholar |
Howes NK, Chong J, Brown PD (1992) Oat endosperm proteins associated with resistance to stem rust of oats. Genome 35, 120-125.
| Crossref | Google Scholar |
Jellen EN, Beard J (2000) Geographical distribution of a chromosome 7C and 17 intergenomic translocation in cultivated oat. Crop Science 40, 256-263.
| Crossref | Google Scholar |
Jellen EN, Rooney WL, Phillips RL, Rines HW (1993) Characterization of the hexaploid oat Avena byzantina cv. Kanota monosomic series using C-banding and RFLPs. Genome 36, 962-970.
| Crossref | Google Scholar | PubMed |
Jellen EN, Phillips RL, Rooney WL, Rines HW (1995) Molecular genetic identification of Avena chromosomes related to the group 1 chromosomes of the Triticeae. Genome 38, 185-189.
| Crossref | Google Scholar | PubMed |
Jellen EN, Rines HW, Fox SL, Davis DW, Phillips RL, Gill BS (1997) Characterization of ‘Sun II’ oat monosomics through C-banding and identification of eight new ‘Sun II’ monosomics. Theoretical and Applied Genetics 95, 1190-1195.
| Crossref | Google Scholar |
Jellen EN, Wight CP, Spannagl M, Blake VC, Chong J, Herrman MH, Howarth CJ, Huang Y-F, Juqing J, Katsiotis A, Langdon T, Li C, Park R, Tinker NA, Sen TZ (2024) A uniform gene and chromosome nomenclature system for oat (Avena L.). Crop & Pasture Science 75, CP23247.
| Crossref | Google Scholar |
Kamal N, Tsardakas Renhuldt N, Bentzer J, Gundlach H, Haberer G, Haberer G, Juhász A, Lux T, Bose U, Tye-Din JA, Lang D, van Gessel N, Reski R, Fu Y-B, Spégel P, Ceplitis A, Himmelbach A, Waters AJ, Bekele WA, Colgrave ML, Hansson M, Stein N, Mayer KFX, Jellen EN, Maughan PJ, Tinker NA, Mascher M, Olsson O, Spannagl M, Sirijovski N (2022) The mosaic oat genome gives insights into a uniquely healthy cereal crop. Nature 606, 113-119.
| Crossref | Google Scholar | PubMed |
Kianian SF, Egli MA, Phillips RL, Rines HW, Somers DA, Gengenbach BG, Webster FH, Livingston SM, Groh S, O’Donoughue LS, Sorrells ME, Wesenberg DM, Stuthman DD, Fulcher RG (1999) Association of a major groat oil content QTL and an acetyl-CoA carboxylase gene in oat. Theoretical and Applied Genetics 98, 884-894.
| Crossref | Google Scholar |
Klos KE, Huang Y-F, Bekele WA, Obert DE, Babiker E, Beattie AD, Bjørnstad Å, Bonman JM, Carson ML, Chao S, Gnanesh BN, Griffiths I, Harrison SA, Howarth CJ, Hu G, Ibrahim A, Islamovic E, Jackson EW, Jannink J-L, Kolb FL, McMullen MS, Mitchell Fetch J, Murphy JP, Ohm HW, Rines HW, Rossnagel BG, Schlueter JA, Sorrells ME, Wight CP, Yan W, Tinker NA (2016) Population genomics related to adaptation in elite oat germplasm. The Plant Genome 9(2), plantgenome2015.10.0103.
| Crossref | Google Scholar |
Kulcheski FR, Graichen FAS, Martinelli JA, Locatelli AB, Federizzi LC, Delatorre CA (2010) Molecular mapping of Pc68, a crown rust resistance gene in Avena sativa. Euphytica 175, 423-432.
| Crossref | Google Scholar |
Luke HH, Wheeler HE, Wallace AT (1960) Victoria-type resistance to crown rust separated from susceptibility to Helminthosporium blight in oats. Phytopathology 50, 205-209.
| Google Scholar |
Martens JW, McKenzie RIH, Fleischmann G (1968) The inheritance of resistance to stem and crown rust in Kyto oats. Canadian Journal of Genetics and Cytology 10, 808-812.
| Crossref | Google Scholar |
Maughan PJ, Lee R, Walstead R, Vickerstaff RJ, Fogarty MC, Brouwer CR, Reid RR, Jay JJ, Bekele WA, Jackson EW, Tinker NA, Langdon T, Schlueter JA, Jellen EN (2019) Genomic insights from the first chromosome-scale assemblies of oat (Avena spp.) diploid species. BMC Biology 17, 92.
| Crossref | Google Scholar | PubMed |
McKenzie RIH, Green GJ (1965) Stem rust resistance in oats. I. The inheritance of resistance to race 6AF in six varieties of oats. Canadian Journal of Genetics and Cytology 7, 268-274.
| Crossref | Google Scholar |
Morikawa T (1985) Identification of the 21 monosomic lines in Avena byzantina C. Koch cv. ‘Kanota’. Theoretical and Applied Genetics 70, 271-278.
| Crossref | Google Scholar | PubMed |
O’Donoughue LS, Wang Z, Roder M, Kneen B, Leggett AM, 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.
| Crossref | Google Scholar |
O’Donoughue LS, Sorrells ME, Tanksley SD, Autrique E, Deynze AV, Kianian SF, Phillips RL, Wu B, Rines HW, Rayapati PJ, Lee M, Penner GA, Fedak G, Molnar SJ, Hoffman D, Salas CA (1995) A molecular linkage map of cultivated oat. Genome 38, 368-380.
| Crossref | Google Scholar | PubMed |
O’Donoughue LS, Chong J, Wight CP, Fedak G, Molnar SJ (1996) Localization of stem rust resistance genes and associated molecular markers in cultivated oat. Phytopathology 86, 719-727.
| Google Scholar |
Oliver RE, Tinker NA, Lazo GR, Chao S, Jellen EN, Carson ML, Rines HW, Obert DE, Lutz JD, Shackelford I, Korol AB, Wight CP, Gardner KM, Hattori J, Beattie AD, Bjørnstad Å, Bonman JM, Jannink J-L, Sorrells ME, Brown-Guedira GL, Mitchell Fetch JW, Harrison SA, Haworth CJ, Ibrahim A, Kolb FL, McMullen MS, Murphy JP, Ohm HW, Rossnagel BG, Yan W, Miclaus KJ, Hiller J, Maughan PJ, Redman Hulse RR, Anderson JM, Islamovic E, Jackson EW (2013) SNP discovery and chromosome anchoring provide the first physically-anchored hexaploid oat map and reveal synteny with model species. PLoS ONE 8, e58068.
| Crossref | Google Scholar | PubMed |
Peng Y, Yan H, Guo L, Deng C, Wang C, Wang Y, Kang L, Zhou P, Yu K, Dong X, Liu X, Sun Z, Peng Y, Zhao J, Deng D, Xu Y, Li Y, Jiang Q, Li Y, Wei L, Wang J, Ma J, Hao M, Li W, Kang H, Peng Z, Liu D, Jia J, Zheng Y, Ma T, Wei Y, Lu F, Ren C (2022) Reference genome assemblies reveal the origin and evolution of allohexaploid oat. Nature Genetics 54, 1248-1258.
| Crossref | Google Scholar | PubMed |
Penner GA, Chong J, Lévesque-Lemay M, Molnar SJ, Fedak G (1993a) Identification of a RAPD marker linked to the oat stem rust gene Pg3. Theoretical and Applied Genetics 85, 702-705.
| Crossref | Google Scholar | PubMed |
Penner GA, Chong J, Wight CP, Molnar SJ, Fedak G (1993b) Identification of an RAPD marker for the crown rust resistance gene Pc68 in oats. Genome 36, 818-820.
| Crossref | Google Scholar | PubMed |
Rines HW, Miller ME, Carson M, Chao S, Tiede T, Wiersma J, Kianian SF (2018) Identification, introgression, and molecular marker genetic analysis and selection of a highly effective novel oat crown rust resistance from diploid oat, Avena strigosa. Theoretical and Applied Genetics 131, 721-733.
| Crossref | Google Scholar | PubMed |
Salmon SC, Parker JH (1921) Kanota: An early oat for Kansas. Circular 91. Agricultural Experiment Station, Kansas State Agricultural College, Manhattan, KS, USA. Available at https://www.ksre.k-state.edu/historicpublications/pubs/SC091.PDF.
Satheeskumar S, Sharp PJ, Lagudah ES, McIntosh RA, Molnar SJ (2011) Genetic association of crown rust resistance gene Pc68, storage protein loci, and resistance gene analogues in oats. Genome 54, 484-497.
| Crossref | Google Scholar | PubMed |
Sayers EW, Bolton EE, Brister JR, Canese K, Chan J, Comeau DC, Connor R, Funk K, Kelly C, Kim S, Madej T, Marchler-Bauer A, Lanczycki C, Lathrop S, Lu Z, Thibaud-Nissen F, Murphy T, Phan L, Skripchenko Y, Tse T, Wang J, Williams R, Trawick BW, Pruitt KD, Sherry ST (2022) Database resources of the national center for biotechnology information. Nucleic Acids Research 50(D1), D20-D26.
| Crossref | Google Scholar | PubMed |
Siripoonwiwat W, O’Donoughue LS, Wesenberg D, Hoffman DL, Barbosa-Neto JF, Sorrells ME (1996) Chromosomal regions associated with quantitative traits in oat. Journal of Agricultural Genomics 2, Available at https://wheat.pw.usda.gov/jag/papers96/paper396/oatqtl3g.html [accessed 22 June 2023].
| Google Scholar |
Sowa S, Paczos-Grzęda E (2020) Identification of molecular markers for the Pc39 gene conferring resistance to crown rust in oat. Theoretical and Applied Genetics 133, 1081-1094.
| Crossref | Google Scholar | PubMed |
Sunstrum FG, Bekele WA, Wight CP, Yan W, Chen Y, Tinker NA (2019) A genetic linkage map in southern-by-spring oat identifies multiple quantitative trait loci for adaptation and rust resistance. Plant Breeding 138, 82-94.
| Crossref | Google Scholar |
Tanhuanpää P, Manninen O, Kiviharju E (2010) QTLs for important breeding characteristics in the doubled haploid oat progeny. Genome 53, 482-493.
| Crossref | Google Scholar | PubMed |
Tinker NA, Kilian A, Wight CP, Heller-Uszynska K, Wenzl P, Rines HW, Bjørnstad Å, Howarth CJ, Jannink JL, 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 JM, Ceplitis A, Langdon T (2009) New DArT markers for oat provide enhanced map coverage and global germplasm characterization. BMC Genomics 10, 39.
| Crossref | Google Scholar | PubMed |
Tinker NA, Wight CP, Bekele WA, Yan W, Jellen EN, Tsardakas Renhuldt N, Sirijovski N, Lux T, Spannagl M, Mascher M (2022) Genome analysis in Avena sativa reveals hidden breeding barriers and opportunities for oat improvement. Communications Biology 5, 474.
| Crossref | Google Scholar | PubMed |
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.
| Crossref | Google Scholar | PubMed |
Wight CP, O’Donoughue LS, Chong J, Tinker NA, Molnar SJ (2005) Discovery, localization, and sequence characterization of molecular markers for the crown rust resistance genes Pc38, Pc39, and Pc48 in cultivated oat (Avena sativa L.). Molecular Breeding 14, 349-361.
| Crossref | Google Scholar |
Wight CP, Yan W, Fetch JM, Deyl J, Tinker NA (2010) A set of new simple sequence repeat and Avenin DNA markers suitable for mapping and fingerprinting studies in oat (Avena spp.). Crop Science 50, 1207-1218.
| Crossref | Google Scholar |
Wilson WF, McMullen MS (1997a) Recombination between a crown rust resistance locus and an interchange breakpoint in hexaploid oat. Crop Science 37, 1694-1698.
| Crossref | Google Scholar |
Wilson WF, McMullen MS (1997b) Dosage dependent genetic suppression of oat crown rust resistance gene Pc-62. Crop Science 37, 1699-1705.
| Crossref | Google Scholar |
Wong LSL, McKenzie RIH, Harder DE, Martens JW (1983) The inheritance of resistance to Puccinia coronata and of floret characters in Avena sterilis. Canadian Journal of Genetics and Cytology 25, 329-335.
| Crossref | Google Scholar |
Yao E, Blake VC, Cooper L, Wight CP, Michel S, Cagirici HB, Lazo GR, Birkett CL, Waring DJ, Jannink J-L, Holmes I, Waters AJ, Eickholt DP, Sen TZ (2022) GrainGenes: a data-rich repository for small grains genetics and genomics. Database 2022, baac034.
| Crossref | Google Scholar |
Zhao J, Kebede AZ, Bekele WA, Menzies JG, Chong J, Mitchell Fetch JW, Tinker NA, Beattie AD, Peng YY, McCartney CA (2020) Mapping of the oat crown rust resistance gene Pc39 relative to single nucleotide polymorphism markers. Plant Disease 104, 1507-1513.
| Crossref | Google Scholar | PubMed |
Zimmer CM, McNish IG, Klos KE, Oro T, Arruda KMA, Gutkoski LC, Pacheco MT, Smith KP, Federizzi LC (2020) Genome-wide association for β-glucan content, population structure, and linkage disequilibrium in elite oat germplasm adapted to subtropical environments. Molecular Breeding 40, 103.
| Crossref | Google Scholar |