Abstract
High β-glucan content is one of the main goals of oat breeding programs worldwide. However, the genomic regions and genes controlling β-glucan content in oats are not fully understood. In this sense, the objectives of this study were as follows: (i) to characterize structure and linkage disequilibrium (LD) in a panel of oat germplasm adapted to subtropical environments; and (ii) to identify genomic regions associated with oat β-glucan content. An oat panel with 413 genotypes was evaluated for β-glucan content under subtropical conditions in different years and genotyped using genotyping-by-sequencing. Population structure, LD, and genome-wide association (GWA) analyses were carried out. GWA mapping was performed for each year separately and in a multi-environment model. The UFRGS Oat Panel showed weak population structure and has great potential to elucidate many agronomic traits in subtropical environments. Seven quantitative trait loci (QTL) associated with β-glucan content were identified. These QTL are located on Mrg02, Mrg06, Mrg11, Mrg12, Mrg19, and Mrg20. The QTL located on Mrg02, Mrg06, and Mrg11 seem to be genomic regions syntenic with barley. The use of these QTL may be useful to accelerate the genetic progress of oat β-glucan content in subtropical environments.
Similar content being viewed by others
References
AACC - American association of cereal chemists. Approved methods Saint Paul, 1999
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
Andrews S. (2010) FastQC: a quality control tool for high throughput sequence data [cited 2018 March 15]. Available from: http://www.bioinformatics.babraham.ac.uk/projects/fastqc
AOAC - Association of Official Analytical Chemistry. Official methods of analysis of the Association of Official Analytical Chemistry. Washington, 1997
Asoro FG, Newell MA, Scott MP, Beavis WD, Jannink JL (2013) Genome-wide association study for beta-glucan concentration in elite North American oat. Crop Sci 53:542–553. https://doi.org/10.2135/cropsci2012.01.0039
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. https://doi.org/10.1111/pbi.12888
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics. 23:2633–2635. https://doi.org/10.1093/bioinformatics/btm308
Burrows VD (1986) Breeding oats for food and feed: conventional and new techniques and materials. In: Webster FH (ed) Oats: chemistry and technology. Saint Paul, American Association of Cereal Chemists, pp. 13–46
Burton RA, Collins HM, Kibble NAJ, Smith JA, Shirley NJ, Jobling SA, Henderson M, Singh RR, Pettolino F, Wilson SM, Bird AR, Topping DL, Bacic A, Fincher GB (2011) Overexpression of specific HvCslF cellulose synthase-like genes in transgenic barley increases the levels of cell wall (1,3;1,4)-β-D-glucans and alters their fine structure. Plant Biotechnol J 9:117–135. https://doi.org/10.1111/j.1467-7652.2010.00532.x
Chu Y (2013) Oats nutrition and technology. John Wiley & Sons Incorporated, Oxford. https://doi.org/10.1002/9781118354100
De Koeyer DL, Tinker NA, Wight CP, Deyl J, Burrows VD, O'Donoughue LS, Lybaert A, Molnar SJ, Armstrong KC, Fedak G, Wesenberg DM, Rossnagel BG, McElroy AR (2004) A molecular linkage map with associated QTLs from a hulless x covered spring oat population. Theor Appl Genet 108:1285–1298. https://doi.org/10.1007/s00122-003-1556-x
Endelman JB (2011) Ridge regression and other kernels for genomic selection with R package rrBLUP. Plant Genome 4:250–255. https://doi.org/10.3835/plantgenome2011.08.0024
Esvelt Klos K, Huang YF, 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 JL, 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. Plant Genome 9:1–12. https://doi.org/10.3835/plantgenome2015.10.0103
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 13:479–491
Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Longman Group Limited, London
Fincher GB, Stone BA (2004) Chemistry of nonstarch polysaccharides. In: Wrigley C, Corke H, Walker CE (eds) Encyclopedia of grain science. Elsevier, Oxford, pp 206–223. https://doi.org/10.1016/B0-12-765490-9/00107-5
Fogarty MC, Smith SM, Sheridan JL, Hu G, Islamovic E, Reid R, Jackson EW, Maughan PJ, Ames NP, Jellen EN, Hsieh T (2020) Identification of mixed linkage β-glucan quantitative trait loci and evaluation of CslF6 homoeologs in hexaploid oat. Crop Sci 1-20. https://doi.org/10.1002/csc2.20015
Herrera MP, Gao J, Vasanthan T, Temelli F, Henderson K (2016) β-Glucan content, viscosity, and solubility of Canadian grown oat as influenced by cultivar and growing location. Can J Plant Sci 96:183–196. https://doi.org/10.1139/cjps-2014-0440
Herrmann MH, Yu J, Beuch S, Weber WE (2014) Quantitative trait loci for quality and agronomic traits in two advanced backcross populations in oat (Avena sativa L.). Plant Breed 133:588–601. https://doi.org/10.1111/pbr.12188
Houston K, Russell J, Schreiber M, Halpin C, Oakey H, Washington JM, Booth A, Shirley N, Burton RA, Fincher GB, Waugh R (2014) A genome wide association scan for (1, 3; 1, 4)-β-glucan content in the grain of contemporary 2-row Spring and Winter barleys. BMC Genomics 15:907. https://doi.org/10.1186/1471-2164-15-907
Huang Y, Poland JA, Wight CP, Jackson EW, Tinker NA (2014) Using genotyping-by-sequencing (GBS) for genomic discovery in cultivated oat. PLoS One 9:e102448. https://doi.org/10.1371/journal.pone.0102448
Islamovic E, Obert DE, Oliver RE, Harrison SA, Ibrahim A, Marshall JM, Miclaus KJ, Hu G, Jackson EW (2013) Genetic dissection of grain beta-glucan and amylose content in barley (Hordeum vulgare L.). Mol Breed 31:15–25. https://doi.org/10.1007/s11032-012-9764-1
Kianian SF, Phillips RL, Rines HW, Fulcher RG, Webster FH, Stuthman DD (2000) Quantitative trait loci influencing β-glucan content in oat (Avena sativa, 2n= 6x= 42). Theor Appl Genet 101:1039–1048. https://doi.org/10.1007/s001220051578
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:e1003215. https://doi.org/10.1371/journal.pgen.1003215
Mangin B, Siberchicot A, Nicolas S, Doligez A, This P, Cierco-Ayrolles C (2012) Novel measures of linkage disequilibrium that correct the bias due to population structure and relatedness. Heredity 108:285–291. https://doi.org/10.1038/hdy.2011.73
McCleary BV, Codd R (1991) Measurement of (1→3),(1→4)-β-D-glucan in barley and oats: a streamlined enzymic procedure. J Sci Food Agric 55:303–312. https://doi.org/10.1002/jsfa.2740550215
McNish IG, Zimmer CM, Susko AQ, Jo HD, Tiede T, Case AJ, Smith KP (2020) Mapping crown rust resistance at multiple time points in elite oat germplasm. Plant Genome 13:e20007. https://doi.org/10.1002/tpg2.20007
Miller SS, Fulcher RG, Vincent DJ, Weisz J (1993) Oat β-glucans: an evaluation of eastern Canadian cultivars and unregistered lines. Can J Plant Sci 73:429–436. https://doi.org/10.4141/cjps93-062
Mohammadi M, Endelman JB, Nair S, Chao S, Jones SS, Muehlbauer GJ, Ullrich SE, Baik BK, Wise ML, Smith KP (2014) Association mapping of grain hardness, polyphenol oxidase, total phenolics, amylose content, and β-glucan in US barley breeding germplasm. Mol Breed 34:1229–1243. https://doi.org/10.1007/s11032-014-0112-5
Nemeth C, Freeman J, Jones HD, Sparks C, TPellny TK et al (2010) Down-regulation of the CslF6 gene results in decreased (1,3;1,4)-β-D-glucan in endosperm of wheat. Plant Physiol 152:1209–1218. https://doi.org/10.1104/pp.109.151712
Newell MA, Asoro FG, Scott MP, White PJ, Beavis WD, Jannink JL (2012) Genome-wide association study for oat (Avena sativa L.) beta-glucan concentration using germplasm of worldwide origin. Theor Appl Genet 125:1687–1696. https://doi.org/10.1007/s00122-012-1945-0
Paradis E (2010) pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–420. https://doi.org/10.1093/bioinformatics/btp696
Peterson DM (1991) Genotype and environment effects on oat beta-glucan concentration. Crop Sci 31:1517–1520. https://doi.org/10.2135/cropsci1991.0011183X003100060025x
Poland JA, Brown PJ, Sorrells ME, Jannink JL (2012) Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PLoS One 7:e32253. https://doi.org/10.1371/journal.pone.0032253
R Development Core Team (2008) R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing
Saastamoinen M (1995) Effects of environmental factors on the β-glucan content of two oat varieties. Acta Agric Scand 45:181–187. https://doi.org/10.1080/09064719509413102
Saastamoinen M, Plaami S, Kumpulainen J (1992) Genetic and environmental variation in β-glucan content of oats cultivated or tested in Finland. J Cereal Sci 16:279–290. https://doi.org/10.1016/S0733-5210(09)80090-8
Taketa S, Yuo T, Tonooka T, Tsumuraya Y, Inagaki Y, Haruyama N, Larroque O, Jobling SA (2012) Functional characterization of barley betaglucanless mutants demonstrates a unique role for CslF6 in (1,3;1,4)-β-D-glucan biosynthesis. J Exp Bot 63:381–392. https://doi.org/10.1093/jxb/err285
Tanhuanpää P, Manninen O, Kiviharju E (2010) QTLs for important breeding characteristics in the doubled haploid oat progeny. Genome 53:482–493. https://doi.org/10.1139/G10-022
Tanhuanpää P, Manninen O, Beattie A, Eckstein P, Scoles G, Rossnagel B, Kiviharju E (2012) An updated doubled haploid oat linkage map and QTL mapping of agronomic and grain quality traits from Canadian field trials. Genome 55:289–301. https://doi.org/10.1139/g2012-017
Tinker NA, Bekele WA, Hattori J (2016) Haplotag: software for haplotype-based genotyping-by-sequencing analysis. Genes Genom Genet 6:857–863. https://doi.org/10.1534/g3.115.024596
Voorrips RE (2012) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78. https://doi.org/10.1093/jhered/93.1.77
Whitehead A, Beck EJ, Tosh S, Wolever TM (2014) Cholesterol-lowering effects of oat β-glucan: a meta-analysis of randomized controlled trials. Am J Clin Nutr 100:1413–1421. https://doi.org/10.3945/ajcn.114.086108
Ye EQ, Chacko SA, Chou EL, Kugizaki M, Liu S (2012) Greater whole-grain intake is associated with lower risk of type 2 diabetes, cardiovascular disease and weight gain. J Nutr 142:1304–1313. https://doi.org/10.3945/jn.111.155325
Yu J, Pressoir G, Briggs WH, Bi IV, Yamasaki M et al (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Genetics 38:203–208. https://doi.org/10.1038/ng1702
Zimmer CM, Ubert IP, Pacheco MT, Federizzi LC (2018) Molecular and comparative mapping for heading date and plant height in oat. Euphytica 214:101. https://doi.org/10.1007/s10681-018-2182-7
Acknowledgments
The authors are thankful to the PepsiCo Agro & Discovery Laboratory/University of Minnesota for supporting the genotyping-by-sequencing. A special thanks to professor Stephen Harrison (Louisiana State University), David Eickholt (PepsiCo), and Mandy Waters (PepsiCo) for collaborating with this research.
Funding
This study was supported by the Coordination for the Improvement of Higher Education Personnel (CAPES), National Council for Scientific and Technological Development (CNPq), and Rio Grande do Sul State Research Support Foundation (PRONEX/FAPERGS; grant number 16/0484-6). The first author was recipient of CNPq (process number 140273/2016-6) and CAPES (process number 88881.187633/2018-01) PhD fellowships.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Supplementary Fig. 1
Association between enzymatic (reference) and NIRS methods for β-glucan content quantification in oats (PNG 87 kb)
Supplementary Fig. 2
Linkage disequilibrium (LD) scatter plots showing correlations (r2) between marker pairs within each consensus group as a function of genetic position; the red line is a smoothing spline (PNG 504 kb)
Supplementary Fig. 3
Rainfall (gray), mean daily maximum (red), and minimum (blue) temperatures recorded from planting to maturity in three environments: Londrina 2017 (a); Eldorado do Sul 2017 (b); and Eldorado do Sul 2018 (c). Two irrigations of 20 mm were performed in Londrina 2017 between 60 and 95 days after planting. Sources: IAPAR and UFRGS local data (PNG 478 kb)
Supplementary Fig. 4
Quantile-quantile (Q-Q) plots of the observed versus expected p values under the null hypothesis for β-glucan content in oats. a, Londrina 2017 (enzymatic); b, Londrina 2017 (NIRS); c, Eldorado do Sul 2017 (NIRS); d, Eldorado do Sul 2018 (NIRS); e, Multi-environment (NIRS) (PNG 65 kb)
ESM 1
(DOCX 12 kb)
ESM 2
(XLSX 12 kb)
ESM 3
(XLSX 39 kb)
Rights and permissions
About this article
Cite this article
Zimmer, C.M., McNish, I.G., Klos, K.E. et al. Genome-wide association for β-glucan content, population structure, and linkage disequilibrium in elite oat germplasm adapted to subtropical environments. Mol Breeding 40, 103 (2020). https://doi.org/10.1007/s11032-020-01182-0
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11032-020-01182-0