Population genomics of Mediterranean oat (A. sativa) reveals high genetic diversity and three loci for heading date.
Journal
TAG. Theoretical and applied genetics. Theoretische und angewandte Genetik
ISSN: 1432-2242
Titre abrégé: Theor Appl Genet
Pays: Germany
ID NLM: 0145600
Informations de publication
Date de publication:
Jul 2021
Jul 2021
Historique:
received:
19
11
2020
accepted:
24
02
2021
pubmed:
27
3
2021
medline:
23
9
2021
entrez:
26
3
2021
Statut:
ppublish
Résumé
Genomic analysis of Mediterranean oats reveals high genetic diversity and three loci for adaptation to this environment. This information together with phenotyping and passport data, gathered in an interactive map, will be a vital resource for oat genetic improvement. During the twentieth century, oat landraces have increasingly been replaced by modern cultivars, resulting in loss of genetic diversity. However, landraces have considerable potential to improve disease and abiotic stress tolerance and may outperform cultivars under low input systems. In this work, we assembled a panel of 669 oat landraces from Mediterranean rim and 40 cultivated oat varieties and performed the first large-scale population genetic analysis of both red and white oat types of Mediterranean origin. We created a public database associated with an interactive map to visualize information for each accession. The oat collection was genotyped with 17,288 single-nucleotide polymorphism (SNP) loci to evaluate population structure and linkage disequilibrium (LD); to perform a genome-wide association study (GWAs) for heading date, a key character closely correlated with performance in this drought-prone area. Population genetic analysis using both structure and PCA distinguished two main groups composed of the red and white oats, respectively. The white oat group was further divided into two subgroups. LD decay was slower within white lines in linkage groups Mrg01, 02, 04, 12, 13, 15, 23, 33, whereas it was slower within red lines in Mrg03, 05, 06, 11, 21, 24, and 28. Association analysis showed several significant markers associated with heading date on linkage group Mrg13 in white oats and on Mrg01 and Mrg08 in red oats.
Identifiants
pubmed: 33770189
doi: 10.1007/s00122-021-03805-2
pii: 10.1007/s00122-021-03805-2
pmc: PMC8263550
doi:
Substances chimiques
Genetic Markers
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2063-2077Subventions
Organisme : Biotechnology and Biological Sciences Research Council
ID : BBS/E/G/00003012
Pays : United Kingdom
Organisme : Spanish Ministry of Science and Innovation
ID : PID2019-104518RB-100
Organisme : Ministerio de Ciencia, Innovación y Universidades
ID : AGL2016-78965AGR
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/H009582/1
Pays : United Kingdom
Organisme : Ministry of Economy and Competitiveness
ID : BES-2014-071044
Organisme : Biotechnology and Biological Sciences Research Council (GB)
ID : BBS/E/W/0012843B.
Références
Alheit KV, Maurer HP, Reif JC, Tucker MR, Hahn V, Weissmann EA, Wuerschum T (2012) Genome-wide evaluation of genetic diversity and linkage disequilibrium in winter and spring triticale (x Triticosecale Wittmack). BMC Genom 13:235. https://doi.org/10.1186/1471-2164-13-235
doi: 10.1186/1471-2164-13-235
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local aligment search tool. J Mol Biol 215:403–410
doi: 10.1016/S0022-2836(05)80360-2
Baohong G, Zhou X, Murphy JP (2003) Genetic variation within Chinese and western cultivated oat accessions. Cereal ResCommun 31:339–346. https://doi.org/10.1007/BF03543363
doi: 10.1007/BF03543363
Bekele WA, Wight CP, Chao S, Howarth CJ, Tinker NA (2018) Haplotype-based genotyping-by-sequencing in oat genome research. Plant Biotechnol J 16:1452–1463
doi: 10.1111/pbi.12888
Benjamini Y, Hochberg Y (2000) On the adaptive control of the false discovery fate in multiple testing with independent statistics. J Edu Behav Stat 25:60–83. https://doi.org/10.3102/10769986025001060
doi: 10.3102/10769986025001060
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinform 23:2633–2635
doi: 10.1093/bioinformatics/btm308
Buckler ES, Thornsberry JM (2002) Plant molecular diversity and applications to genomics. Curr Opin Plant Biol 5:107–111
doi: 10.1016/S1369-5266(02)00238-8
Canales FJ et al (2021) Data set from: Population genomics of Mediterranean oat (A. sativa) reveals high genetic diversity and three loci for heading date. Dryad, Dataset. https://doi.org/10.5061/dryad.0gb5mkm0g
Chalak L, Mzid R, Rizk W, Hmedeh H, Kabalan R, Breidy J, Hamadeh B, Machlab H, Rizk H, Elhajj S (2015) Performance of 50 Lebanese barley landraces (Hordeum vulgare L. subsp. vulgare) in two locations under rainfed conditions. Annals Agric Sci 60:325–334. https://doi.org/10.1016/j.aoas.2015.11.005
doi: 10.1016/j.aoas.2015.11.005
Chao S, Dubcovsky J, Dvorak J, Luo M-C, Baenziger SP, Matnyazov R, Clark DR, Talbert LE, Anderson JA, Dreisigacker S, Glover K, Chen J, Campbell K, Bruckner PL, Rudd JC, Haley S, Carver BF, Perry S, Sorrells ME, Akhunov ED (2010) Population- and genome-specific patterns of linkage disequilibrium and SNP variation in spring and winter wheat (Triticum aestivum L). BMC Genom 11:727. https://doi.org/10.1186/1471-2164-11-727
doi: 10.1186/1471-2164-11-727
Christiansen MJ, Andersen SB, Ortiz R (2002) Diversity changes in an intensively bred wheat germplasm during the 20th century. Mol Breeding 9:1–11. https://doi.org/10.1023/A:1019234323372
doi: 10.1023/A:1019234323372
Donini P, Law JR, Koebner RMD, Reeves JC, Cooke RJ (2000) Temporal trends in the diversity of UK wheat. Theor Appl Genet 100:912–917. https://doi.org/10.1007/s001220051370
doi: 10.1007/s001220051370
Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Res 4:359–361. https://doi.org/10.1007/s12686-011-9548-7
doi: 10.1007/s12686-011-9548-7
Ehlers W (1989) Transpiration efficiency of oat. Agronomy J 81:810–817. https://doi.org/10.2134/agronj1989.00021962008100050023x
doi: 10.2134/agronj1989.00021962008100050023x
Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple Genotyping-by-Sequencing (GBS) approach for high diversity species. PLoS ONE 6:e19379. https://doi.org/10.1371/journal.pone.0019379
doi: 10.1371/journal.pone.0019379
pubmed: 21573248
pmcid: 3087801
Esvelt Klos K, Huang Y-F, Bekele WA, Obert DE, Babiker E, Beattie AD, Bjornstad A, 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, Fetch JM, 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. Plant Genom. https://doi.org/10.3835/plantgenome2015.10.0103
doi: 10.3835/plantgenome2015.10.0103
Esvelt Klos K, Yimer BA, Babiker EM, Beattie AD, Bonman JM, Carson ML, Chong J, Harrison SA, Ibrahim A, 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 Genom. https://doi.org/10.3835/plantgenome2016.10.0107
doi: 10.3835/plantgenome2016.10.0107
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
doi: 10.1111/j.1365-294X.2005.02553.x
Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genet 164:1567–1587
doi: 10.1093/genetics/164.4.1567
Frankel OH (1970) Genetic conservation in perspective. In: Frankel OH, Bennett E (eds) Genetic Resources in Plants - Their Exploration and Conservation International Biological Programme Handbook No 11. Blackwell Scientific Publications, Oxford, pp 469–489
Fu YB, Kibite S, Richards KW (2004) Amplified fragment length polymorphism analysis of 96 Canadian oat cultivars released between 1886 and 2001. Can J Plant Sci 84:23–30. https://doi.org/10.4141/P02-141
doi: 10.4141/P02-141
Fu YB, Peterson GW, Morrison MJ (2007) Genetic diversity of Canadian soybean cultivars and exotic germplasm revealed by simple sequence repeat markers. Crop Sci 47:1947–1954. https://doi.org/10.2135/cropsci2006.12.0843
doi: 10.2135/cropsci2006.12.0843
Fu YB, Peterson GW, Williams D, Richards KW, Fetch JM (2005) Patterns of AFLP variation in a core subset of cultivated hexaploid oat germplasm. Theor Appl Genet 111:530–539
doi: 10.1007/s00122-005-2044-2
Google-LTD (2021) Google Maps of Mediterranean area. Retrieved from https://www.google.es/maps/@44.6530938,18.9948982,4z
Huang Y-F, Poland JA, Wight CP, Jackson EW, Tinker NA (2014) Using genotyping-by-sequencing (GBS) for genomic discovery in cultivated oat. PLoS ONE 9(7):e102448. https://doi.org/10.1371/journal.pone.0102448
doi: 10.1371/journal.pone.0102448
pubmed: 25047601
pmcid: 4105502
Jacoby WG (2000) Loess: a nonparametric, graphical tool for depicting relationships between variables. Elect Stud 19:577–613. https://doi.org/10.1016/S0261-3794(99)00028-1
doi: 10.1016/S0261-3794(99)00028-1
Kebede AZ, Admassu-Yimer B, Bekele WA, Gordon T, Bonman JM, Babiker E, Jin Y, Gale S, Wight CP, Tinker NA, Menzies JG, Beattie AD, Mitchell Fetch J, Fetch TG, Esvelt Klos K, McCartney CA (2020) Mapping of the stem rust resistance gene Pg13 in cultivated oat. Theor Appl Genet 133:259–270
doi: 10.1007/s00122-019-03455-5
Klepikova AV, Kasianov AS, Gerasimov ES, Logacheva MD, Penin AA (2016) A high resolution map of the Arabidopsis thaliana developmental transcriptome based on RNA-seq profiling. Plant J 88:1058–1070
doi: 10.1111/tpj.13312
Koebner RMD, Summers RW (2003) 21st century wheat breeding: plot selection or plate detection? Trends Biotechnol 21:59–63
doi: 10.1016/S0167-7799(02)00036-7
Kouidri A, Baumann U, Okada T, Baes M, Tucker EJ, Whitford R (2018) Wheat TaMs1 is aglycosylphosphatidylinositol-anchored lipid transfer protein necessary for pollen development. BMC Plant Biol 18:332
doi: 10.1186/s12870-018-1557-1
Lalanne E, Honys D, Johnson A, Borner GHH, Lilley KS, Dupree P, Grossniklaus U, Twell D (2004) SETH1 and SETH2, two components of the glycosylphosphatidylinositol anchor biosynthetic pathway, are required for pollen germination and tube growth in Arabidopsis. Plant Cell 16:229–240
doi: 10.1105/tpc.014407
Li Y, Haseneyer G, Schoen C-C, Ankerst D, Korzun V, Wilde P, 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. https://doi.org/10.1186/1471-2229-11-6
doi: 10.1186/1471-2229-11-6
pubmed: 21219606
pmcid: 3032657
Loskutov IG (2008) On evolutionary pathways of Avena species. Genet Res Crop Evol 55:211–220. https://doi.org/10.1007/s10722-007-9229-2
doi: 10.1007/s10722-007-9229-2
Lu F, Lipka AE, Glaubitz J, Elshire R, Cherney JH, Casler MD, Buckler ES, Costich DE (2013) Switchgrass genomic diversity, ploidy, and evolution: Novel insights from a network-based SNP discovery Protocol. Plos Genet 9(1):e1003215. https://doi.org/10.1371/journal.pgen.1003215
doi: 10.1371/journal.pgen.1003215
pubmed: 23349638
pmcid: 3547862
Mahadevan M, Calderini DF, Zwer PK, Sadras VO (2016) The critical period for yield determination in oat (Avena sativa L.). Field Crops Res 199:109–116. https://doi.org/10.1016/j.fcr.2016.09.021
doi: 10.1016/j.fcr.2016.09.021
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 Biol 17:92
doi: 10.1186/s12915-019-0712-y
Montilla-Bascón G, Rispail N, Sánchez-Martín J, Rubiales D, Mur LAJ, Langdon T, Howarth C, Prats E (2015) Genome-wide association study for crown rust (Puccinia coronata f. sp. avenae) and powdery mildew (Blumeria graminis f. sp. avenae) resistance in an oat (Avena sativa) collection of commercial varieties and landraces. Front Plant Sci 6:103. https://doi.org/10.3389/fpls.2015.00103
doi: 10.3389/fpls.2015.00103
pubmed: 25798140
pmcid: 4350391
Montilla-Bascón G, Sanchez-Martin J, Rispail N, Rubiales D, Mur L, Langdon T, Griffiths I, Howarth C, Prats E (2013) Genetic diversity and population structure among oat cultivars and landraces. Plant Mol Biol Report 31:1305–1314. https://doi.org/10.1007/s11105-013-0598-8
doi: 10.1007/s11105-013-0598-8
Murray MG, Thompson WF (1980) Rapid isolation of high Molecular-Weight plant DNA. Nucleic Acids Res 8:4321–4325
doi: 10.1093/nar/8.19.4321
Newell MA, Asoro FG, Scott MP, White PJ, Beavis WD, Jannink J-L (2012) Genome-wide association study for oat (Avena sativa L.) beta-glucan concentration using germplasm of worldwide origin. Theor Appl Genet 125:1687–1696
doi: 10.1007/s00122-012-1945-0
Newell MA, Cook D, Tinker NA, Jannink JL (2011) Population structure and linkage disequilibrium in oat (Avena sativa L.): implications for genome-wide association studies. Theor Appl Genet 122:623–632
doi: 10.1007/s00122-010-1474-7
Newton AC, Akar T, Baresel JP, Bebeli PJ, Bettencourt E, Bladenopoulos KV, Czembor JH, Fasoula DA, Katsiotis A, Koutis K, Koutsika-Sotiriou M, Kovacs G, Larsson H, de Carvalho M, Rubiales D, Russell J, Dos Santos TMM, Patto MCV (2010) Cereal landraces for sustainable agriculture. Rev Agron Sustain Dev 30:237–269. https://doi.org/10.1051/agro/2009032
doi: 10.1051/agro/2009032
Pei H, Ma N, Tian J, Luo J, Chen J, Li J, Zheng Y, Chen X, Fei Z, Gao J (2013) An NAC transcription factor controls ethylene-regulated cell expansion in flower petals. Plant Physiol 163:775–791
doi: 10.1104/pp.113.223388
Prats E, Sánchez-Martín J, Montilla-Bascón G, Rubiales D, Rispail N (2014) Overview and prospects of the oat crop in Spain. Oat Newslett 51:9
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959. https://doi.org/10.1093/genetics/155.2.945
doi: 10.1093/genetics/155.2.945
pubmed: 10835412
pmcid: 1461096
Ramasamy RK, Ramasamy S, Bindroo BB, Naik VG (2014) STRUCTURE PLOT: a program for drawing elegant STRUCTURE bar plots in user friendly interface. SpringerPlus 3(1):431. https://doi.org/10.1186/2193-1801-3-431
doi: 10.1186/2193-1801-3-431
pubmed: 25152854
pmcid: 4141070
Reed E, Nunez S, Kulp D, Qian J, Reilly MP, Foulkes AS (2015) A guide to genome-wide association analysis and post-analytic interrogation. Stat Med 34:3769–3792
doi: 10.1002/sim.6605
Reif JC, Zhang P, Dreisigacker S, Warburton ML, van Ginkel M, Hoisington D, Bohn M, Melchinger AE (2005) Wheat genetic diversity trends during domestication and breeding. Theor Appl Genet 110:859–864
doi: 10.1007/s00122-004-1881-8
Rispail N, Montilla-Bascon G, Sanchez-Martin J, Flores F, Howarth C, Langdon T, Rubiales D, Prats E (2018) Multi-environmental trials reveal genetic plasticity of oat agronomic traits associated with climate variable changes. Front Plant Sci. https://doi.org/10.3389/fpls.2018.01358
doi: 10.3389/fpls.2018.01358
pubmed: 30283476
pmcid: 6156136
Roussel V, Koenig J, Beckert M, Balfourier F (2004) Molecular diversity in French bread wheat accessions related to temporal trends and breeding programmes. Theor Appl Genet 108:920–930
doi: 10.1007/s00122-003-1502-y
Sánchez-Martín J, Rispail N, Flores F, Emeran AA, Sillero JC, Rubiales D, Prats E (2017) Higher rust resistance and similar yield of oat landraces versus cultivars under high temperature and drought. Agron Sustain Dev 37:3. https://doi.org/10.1007/s13593-016-0407-5
doi: 10.1007/s13593-016-0407-5
Sánchez-Martín J, Rubiales D, Flores F, Emeran AA, Shtaya MJY, Sillero JC, Allagui MB, Prats E (2014) Adaptation of oat (Avena sativa) cultivars to autumn sowings in Mediterranean environments. Field Crops Res 156:111–122. https://doi.org/10.1016/j.fcr.2013.10.018
doi: 10.1016/j.fcr.2013.10.018
Stevens EJ, Armstrong KW, Bezar HJ, Griffin WB, Hampton JG (2004) Fodder oats: an overview. In: Suttie JM, Reynolds SG (eds) Fodder oats: A world overview. FAO, Rome, pp 1–9
Storey JD (2002) A direct approach to false discovery rates. J Roy Stat Soc Ser B (Stat Methodol) 64(3):479–498. https://doi.org/10.1111/1467-9868.00346
doi: 10.1111/1467-9868.00346
Thomas H ( 1995) Oats. In: Smartt JS, N.W. (ed) Evolution of crop plants, Second edn. Longman, London, United Kingdom, pp 133–137
Tinker NA, Bekele WA, Hattori J (2016) Haplotag: Software for haplotype-based genotyping-by-sequencing analysis. G3-Genes Genomes Genetics 6:857–863
pubmed: 26818073
pmcid: 4825656
Tumino G, Voorrips RE, Rizza F, Badeck FW, Morcia C, Ghizzoni R, Germeier CU, Paulo M-J, Terzi V, Smulders MJM (2016) Population structure and genome-wide association analysis for frost tolerance in oat using continuous SNP array signal intensity ratios. Theor Appl Genet 129:1711–1724
doi: 10.1007/s00122-016-2734-y
Van Inghelandt D, Reif JC, Dhillon BS, Flament P, Melchinger AE (2011) Extent and genome-wide distribution of linkage disequilibrium in commercial maize germplasm. Theor Appl Genet 123:11–20
doi: 10.1007/s00122-011-1562-3
Warburton ML, Reif JC, Frisch M, Bohn M, Bedoya C, Xia XC, Crossa J, Franco J, Hoisington D, Pixley K, Taba S, Melchinger AE (2008) Genetic diversity in CIMMYT nontemperate maize germplasm: Landraces, open pollinated varieties, and inbred lines. Crop Sci 48:617–624. https://doi.org/10.2135/cropsci2007.02.0103
doi: 10.2135/cropsci2007.02.0103
Yoshiyama K, Conklin PA, Huefner ND, Britt AB (2009) Suppressor of gamma response 1 (SOG1) encodes a putative transcription factor governing multiple responses to DNA damage. Proceedings of the National Academy of Sciences of the United States of America 106:12843-12848
Yu JM, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nature Genet 38:203–208
doi: 10.1038/ng1702
Zohary D, Hopf M (2000) Domestication of plants in the old world, 3rd edn. Oxford University Press, Oxford-New York