Abstract
Genetic dissection of yield component traits including spike and kernel characteristics is essential for the continuous improvement in wheat yield. Genome-wide association studies (GWAS) have been frequently used to identify genetic determinants for spike and kernel-related traits in wheat, though none have been employed in hard winter wheat (HWW) which represents a major class in US wheat acreage. Further, most of these studies relied on assembled diversity panels instead of adapted breeding lines, limiting the transferability of results to practical wheat breeding. Here we assembled a population of advanced/elite breeding lines and well-adapted cultivars and evaluated over four environments for phenotypic analysis of spike and kernel traits. GWAS identified 17 significant multi-environment marker–trait associations (MTAs) for various traits, representing 12 putative quantitative trait loci (QTLs), with five QTLs affecting multiple traits. Four of these QTLs mapped on three chromosomes 1A, 5B, and 7A for spike length, number of spikelets per spike (NSPS), and kernel length are likely novel. Further, a highly significant QTL was detected on chromosome 7AS that has not been previously associated with NSPS and putative candidate genes were identified in this region. The allelic frequencies of important quantitative trait nucleotides (QTNs) were deduced in a larger set of 1,124 accessions which revealed the importance of identified MTAs in the US HWW breeding programs. The results from this study could be directly used by the breeders to select the lines with favorable alleles for making crosses, and reported markers will facilitate marker-assisted selection of stable QTLs for yield components in wheat breeding.
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Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
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Publicly available statistical tools were used in this study.
References
Adamski NM, Simmonds J, Brinton JF et al (2021) Ectopic expression of Triticum polonicum VRT-A2 underlies elongated glumes and grains in hexaploid wheat in a dosage-dependent manner. Plant Cell 33:2296–2319. https://doi.org/10.1093/plcell/koab119
Alqudah AM, Haile JK, Alomari DZ et al (2020) Genome-wide and SNP network analyses reveal genetic control of spikelet sterility and yield-related traits in wheat. Sci Rep 10:1–12. https://doi.org/10.1038/s41598-020-59004-4
AlTameemi R, Gill HS, Ali S, Ayana G, Halder J, Sidhu JS, Gill US, Turnipseed B, Gonzalez Hernandez JL, Sehgal SK (2021) Genome-wide association analysis permits characterization of Stagonospora nodorum blotch (SNB) resistance in hard winter wheat. Scientific Reports 11(1). https://doi.org/10.1038/s41598-021-91515-6
Alvarado G, Rodríguez FM, Pacheco A et al (2020) META-R: a software to analyze data from multi-environment plant breeding trials. Crop J 8:745–756. https://doi.org/10.1016/j.cj.2020.03.010
Backhaus AE, Lister A, Tomkins M et al (2022) High expression of the MADS-box gene VRT2 increases the number of rudimentary basal spikelets in wheat. Plant Physiol 189:536–1552. https://doi.org/10.1093/plphys/kiac156
Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21:263–265. https://doi.org/10.1093/bioinformatics/bth457
Bates Douglas, Mächler Martin, Bolker Ben, Walker Steve (2015) Fitting linear mixed-effects models using lme4. J Stat Softw. https://doi.org/10.18637/jss.v067.i01
Begum H, Spindel JE, Lalusin A et al (2015) Genome-wide association mapping for yield and other agronomic traits in an elite breeding population of tropical rice (Oryza sativa). PLoS ONE. https://doi.org/10.1371/journal.pone.0119873
Börner A, Schumann E, Fürste A et al (2002) Mapping of quantitative trait loci determining agronomic important characters in hexaploid wheat (Triticum aestivum L.). Theor Appl Genet 105:921–936. https://doi.org/10.1007/s00122-002-0994-1
Bradbury PJ, Zhang Z, Kroon DE et al (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635. https://doi.org/10.1093/bioinformatics/btm308
Browning SR, Browning BL (2007) Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am J Hum Genet 81:1084–1097. https://doi.org/10.1086/521987
Chai S, Yao Q, Liu R et al (2021) Identification and validation of a major gene for kernel length at the P1 locus in Triticum polonicum. Crop J. https://doi.org/10.1016/j.cj.2021.07.006
Chen G, Zhang H, Deng Z et al (2016) Genome-wide association study for kernel weight-related traits using SNPs in a Chinese winter wheat population. Euphytica 212:173–185. https://doi.org/10.1007/s10681-016-1750-y
Chen Z, Cheng X, Chai L et al (2020) Dissection of genetic factors underlying grain size and fine mapping of QTgw.cau-7D in common wheat (Triticum aestivum L.). Theor Appl Genet 133:149–162. https://doi.org/10.1007/s00122-019-03447-5
Conesa A, Gotz S, Garcia-Gomez JM et al (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676. https://doi.org/10.1093/bioinformatics/bti610
Dhakal S, Liu X, Chu C et al (2021) Genome-wide QTL mapping of yield and agronomic traits in two widely adapted winter wheat cultivars from multiple mega-environments. PeerJ 9:e12350. https://doi.org/10.7717/peerj.12350
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull
Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. https://doi.org/10.1007/s12686-011-9548-7
Epskamp S, Cramer AOJ, Waldorp LJ et al (2012) Qgraph Network visualizations of relationships in psychometric data. J Stat Softw. https://doi.org/10.18637/jss.v048.i04
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. https://doi.org/10.1111/j.1365-294X.2005.02553.x
FAO (2017) The future of food and agriculture – Trends and challenges. FAO, Rome
Faris JD, Zhang Z, Garvin DF, Xu SS (2014) Molecular and comparative mapping of genes governing spike compactness from wild emmer wheat. Mol Genet Genomics 289:641–651. https://doi.org/10.1007/s00438-014-0836-2
Fischer R, Byerlee D, Edmeades G (2014) Crop yields and global food security. ACIAR: Canberra, ACT
Gao F, Wen W, Liu J et al (2015) Genome-wide linkage mapping of QTL for yield components, plant height and yield-related physiological traits in the Chinese wheat cross Zhou 8425B/Chinese spring. Front Plant Sci. https://doi.org/10.3389/fpls.2015.01099
Gegas VC, Nazari A, Griffiths S et al (2010) A genetic framework for grain size and shape variation in wheat. Plant Cell 22:1046–1056. https://doi.org/10.1105/tpc.110.074153
Gill HS, Li C, Sidhu JS et al (2019) Fine mapping of the wheat leaf rust resistance gene Lr42. Int J Mol Sci. https://doi.org/10.3390/ijms20102445
Gill HS, Halder J, Zhang J et al (2021) Multi-trait multi-environment genomic prediction of agronomic traits in advanced breeding lines of winter wheat. Front Plant Sci. https://doi.org/10.3389/fpls.2021.709545
Grote U, Fasse A, Nguyen TT, Erenstein O (2021) Food security and the dynamics of wheat and maize value Chains in Africa and Asia. Front Sustain Food Syst 4:317
Guo Z, Chen D, Alqudah AM et al (2017) Genome-wide association analyses of 54 traits identified multiple loci for the determination of floret fertility in wheat. New Phytol 214:257–270. https://doi.org/10.1111/nph.14342
Habyarimana E, De Franceschi P, Ercisli S et al (2020) Genome-wide association study for biomass related traits in a panel of sorghum bicolor and S. bicolor × S. halepense populations. Front Plant Sci. 11:1796. https://doi.org/10.3389/fpls.2020.551305
Halder J, Zhang J, Ali S et al (2019) Mining and genomic characterization of resistance to tan spot, Stagonospora nodorum blotch (SNB), and Fusarium head blight in Watkins core collection of wheat landraces. BMC Plant Biol 19:1–15. https://doi.org/10.1186/s12870-019-2093-3
Hill WG, Weir BS (1988) Variances and covariances of squared linkage disequilibria in finite populations. Theor Popul Biol 33:54–78. https://doi.org/10.1016/0040-5809(88)90004-4
Hou J, Jiang Q, Hao C et al (2014) Global selection on sucrose synthase haplotypes during a century of wheat breeding. Plant Physiol 164:1918–1929. https://doi.org/10.1104/pp.113.232454
Hu MJ, Zhang HP, Cao JJ et al (2016) Characterization of an IAA-glucose hydrolase gene TaTGW6 associated with grain weight in common wheat (Triticum aestivum L.). Mol Breed 36:1–11. https://doi.org/10.1007/s11032-016-0449-z
Hu J, Wang X, Zhang G et al (2020) QTL mapping for yield-related traits in wheat based on four RIL populations. Theor Appl Genet 133:917–933. https://doi.org/10.1007/s00122-019-03515-w
Huang M, Liu X, Zhou Y et al (2019) BLINK: a package for the next level of genome-wide association studies with both individuals and markers in the millions. Gigascience 8:1–12. https://doi.org/10.1093/gigascience/giy154
IWGSC (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361:eaar7191. https://doi.org/10.1126/science.aar7191
Juliana P, Singh RP, Poland J et al (2021) Elucidating the genetics of grain yield and stress-resilience in bread wheat using a large-scale genome-wide association mapping study with 55,568 lines. Sci Rep 11:1–15. https://doi.org/10.1038/s41598-021-84308-4
Katkout M, Kishii M, Kawaura K et al (2014) QTL analysis of genetic loci affecting domestication-related spike characters in common wheat. Genes Genet Syst 89:121–131. https://doi.org/10.1266/ggs.89.121
Kaur B, Mavi GS, Gill MS, Saini DK (2020) Utilization of KASP technology for wheat improvement. Cereal Res Commun 48(4):409–421. https://doi.org/10.1007/s42976-020-00057-6
Kumar A, Mantovani EE, Seetan R et al (2016) Dissection of genetic factors underlying wheat kernel shape and size in an Elite × Nonadapted cross using a high density SNP linkage map. Plant Genome. https://doi.org/10.3835/plantgenome2015.09.0081
Kumar D, Sharma S, Sharma R et al (2021) Genome-wide association study in hexaploid wheat identifies novel genomic regions associated with resistance to root lesion nematode (Pratylenchus thornei). Sci Rep 11:3572. https://doi.org/10.1038/s41598-021-80996-0
Kuzay S, Xu Y, Zhang J et al (2019) Identification of a candidate gene for a QTL for spikelet number per spike on wheat chromosome arm 7AL by high-resolution genetic mapping. Theor Appl Genet 132:2689–2705. https://doi.org/10.1007/s00122-019-03382-5
Kuzay S, Lin H, Li C et al (2022) WAPO-A1 is the causal gene of the 7AL QTL for spikelet number per spike in wheat. PLOS Genet 18:e1009747. https://doi.org/10.1371/journal.pgen.1009747
Li F, Wen W, He Z et al (2018) Genome-wide linkage mapping of yield-related traits in three Chinese bread wheat populations using high-density SNP markers. Theor Appl Genet 131:1903–1924. https://doi.org/10.1007/s00122-018-3122-6
Li F, Wen W, Liu J et al (2019) Genetic architecture of grain yield in bread wheat based on genome-wide association studies. BMC Plant Biol 19:168. https://doi.org/10.1186/s12870-019-1781-3
Li K, Debernardi JM, Li C et al (2021) Interactions between SQUAMOSA and SHORT VEGETATIVE PHASE MADS-box proteins regulate meristem transitions during wheat spike development. Plant Cell 33:3621–3644. https://doi.org/10.1093/plcell/koab243
Liu G, Jia L, Lu L et al (2014) Mapping QTLs of yield-related traits using RIL population derived from common wheat and Tibetan semi-wild wheat. Theor Appl Genet 127:2415–2432. https://doi.org/10.1007/s00122-014-2387-7
Liu X, Huang M, Fan B et al (2016) Iterative usage of fixed and random effect models for powerful and efficient genome-wide association studies. PLOS Genet 12:e1005767. https://doi.org/10.1371/journal.pgen.1005767
Liu J, Xu Z, Fan X et al (2018a) A genome-wide association study of wheat spike related traits in China. Front Plant Sci 871:1584. https://doi.org/10.3389/fpls.2018.01584
Liu K, Sun X, Ning T et al (2018b) Genetic dissection of wheat panicle traits using linkage analysis and a genome-wide association study. Theor Appl Genet 131:1073–1090. https://doi.org/10.1007/s00122-018-3059-9
Liu H, Zhang X, Xu Y et al (2020) Identification and validation of quantitative trait loci for kernel traits in common wheat (Triticum aestivum L.). BMC Plant Biol. 20:529. https://doi.org/10.1186/s12870-020-02661-4
Liu L, Wang M, Zhang Z et al (2020b) Identification of stripe rust resistance loci in u.s. spring wheat cultivars and breeding lines using genome-wide association mapping and yr gene markers. Plant Dis 104:2181–2192. https://doi.org/10.1094/PDIS-11-19-2402-RE
Liu J, Chen Z, Wang Z et al (2021) Ectopic expression of VRT-A2 underlies the origin of (Triticum polonicum L.) and Triticum petropavlovskyi with long outer glumes and grains. Mol Plant 14:1472–1488. https://doi.org/10.1016/j.molp.2021.05.021
Mendiburu Felipe de (2021) “agricolae”: Statistical Procedures for Agricultural Research
Mohler V, Albrecht T, Castell A et al (2016) Considering causal genes in the genetic dissection of kernel traits in common wheat. J Appl Genet 57:467–476. https://doi.org/10.1007/s13353-016-0349-2
Muqaddasi QH, Brassac J, Koppolu R et al (2019) TaAPO-A1, an ortholog of rice ABERRANT PANICLE ORGANIZATION 1, is associated with total spikelet number per spike in elite European hexaploid winter wheat (Triticum aestivum L.) varieties. Sci Rep 9:1–12. https://doi.org/10.1038/s41598-019-50331-9
Pang Y, Liu C, Wang D et al (2020) High-resolution genome-wide association study identifies genomic regions and candidate genes for important agronomic traits in wheat. Mol Plant 13:1311–1327. https://doi.org/10.1016/j.molp.2020.07.008
Poland J, Endelman J, Dawson J et al (2012) Genomic selection in wheat breeding using genotyping-by-sequencing. Plant Genome. https://doi.org/10.3835/plantgenome2012.06.0006
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Saini DK, Srivastava P, Pal N, Gupta PK (2022) Meta-QTLs, ortho-meta-QTLs and candidate genes for grain yield and associated traits in wheat (Triticum aestivum L.). Theor Appl Genet 135(3):1049–1081. https://doi.org/10.1007/s00122-021-04018-3
Sidhu JS, Singh D, Gill HS et al (2020) Genome-wide association study uncovers novel genomic regions associated with coleoptile length in hard winter wheat. Front Genet 10:1345. https://doi.org/10.3389/fgene.2019.01345
Sourdille P, Tixier MH, Charmet G et al (2000) Location of genes involved in ear compactness in wheat (Triticum aestivum L.) by means of molecular markers. Mol Breed 6:247–255. https://doi.org/10.1023/A:1009688011563
Su Z, Hao C, Wang L et al (2011) Identification and development of a functional marker of TaGW2 associated with grain weight in bread wheat (Triticum aestivum L.). Theor Appl Genet 122:211–223. https://doi.org/10.1007/s00122-010-1437-z
Su Q, Zhang X, Zhang W et al (2018) QTL detection for kernel size and weight in bread wheat (Triticum aestivum L.) Using a high-density SNP and SSR-based linkage map. Front Plant Sci 9:1484. https://doi.org/10.3389/fpls.2018.01484
Sukumaran S, Dreisigacker S, Lopes M et al (2014) Genome-wide association study for grain yield and related traits in an elite spring wheat population grown in temperate irrigated environments. Theor Appl Genet 128:353–363. https://doi.org/10.1007/s00122-014-2435-3
Team RC (2014) R: a language and environment for statistical computing.
USDA (2021) Acreage (June 2021): USDA National Agricultural Statistics Service. https://www.nass.usda.gov/Publications/Todays_Reports/reports/acrg0621.pdf. Accessed 13 Mar 2022
Wang J, Zhang Z (2021) GAPIT Version 3: boosting power and accuracy for genomic association and prediction. Genomics Proteomics Bioinform. https://doi.org/10.1016/j.gpb.2021.08.005
Wang RX, Hai L, Zhang XY et al (2009) QTL mapping for grain filling rate and yield-related traits in RILs of the Chinese winter wheat population Heshangmai x Yu8679. Theor Appl Genet 118:313–325. https://doi.org/10.1007/s00122-008-0901-5
Ward BP, Brown-Guedira G, Kolb FL et al (2019) Genome-wide association studies for yield-related traits in soft red winter wheat grown in Virginia. PLoS ONE 14:e0208217. https://doi.org/10.1371/journal.pone.0208217
Wheeler T, Von Braun J (2013) Climate change impacts on global food security. Science 341:508–513
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York
William R (2013) psych: procedures for Personality and Psychological Research. Evanston, Illinois, USA
Wu X, Chang X, Jing R (2012) Genetic insight into yield-associated traits of wheat grown in multiple rain-fed environments. PLoS ONE 7:e31249. https://doi.org/10.1371/journal.pone.0031249
Würschum T, Leiser WL, Langer SM et al (2018) Phenotypic and genetic analysis of spike and kernel characteristics in wheat reveals long-term genetic trends of grain yield components. Theor Appl Genet 131:2071–2084. https://doi.org/10.1007/s00122-018-3133-3
Yu J, Pressoir G, Briggs WH et al (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208. https://doi.org/10.1038/ng1702
Yu M, Mao SL, Chen GY et al (2014) QTLs for uppermost internode and spike length in two wheat RIL populations and their affect upon plant height at an individual QTL level. Euphytica 200:95–108. https://doi.org/10.1007/s10681-014-1156-7
Zanke CD, Ling J, Plieske J et al (2015) Analysis of main effect QTL for thousand grain weight in European winter wheat (Triticum aestivum L.) by genome-wide association mapping. Front Plant Sci 6:644. https://doi.org/10.3389/fpls.2015.00644
Zhai H, Feng Z, Li J et al (2016) QTL analysis of spike morphological traits and plant height in winter wheat (Triticum aestivum L) using a high-density SNP and SSR-based linkage map. Front Plant Sci. https://doi.org/10.3389/fpls.2016.01617
Zhang J, Gizaw SA, Bossolini E et al (2018) Identification and validation of QTL for grain yield and plant water status under contrasting water treatments in fall-sown spring wheats. Theor Appl Genet 131:1741–1759. https://doi.org/10.1007/s00122-018-3111-9
Zhou Y, Conway B, Miller D et al (2017) Quantitative trait loci mapping for spike characteristics in hexaploid wheat. Plant Genome. https://doi.org/10.3835/plantgenome2016.10.0101
Zhu T, Wang L, Rimbert H et al (2021) Optical maps refine the bread wheat Triticum aestivum cv. Chinese Spring Genome Assembly. Plant J 107:303–314. https://doi.org/10.1111/tpj.15289
Acknowledgements
The authors would like to thank the South Dakota Agriculture Experimental Station (Brookings, SD, USA) for providing the resources to conduct the experiments. The authors are also thankful to Cody Hall and Navreet Brar for their efforts in planting and harvesting of the trials. The mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the United States Department of Agriculture. The USDA is an equal opportunity provider and employer.
Funding
This project was collectively funded by the USDA hatch projects SD00H695-20, and the USDA Agriculture and Food Research Initiative Competitive Grants 2022–68013-36439 (Wheat-CAP) from the USDA National Institute of Food and Agriculture and South Dakota Wheat Commission grant 3X1340. The funders had no role in the study design, data collection, analysis, decision to publish, or manuscript preparation.
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Gill, H.S., Halder, J., Zhang, J. et al. Whole-genome analysis of hard winter wheat germplasm identifies genomic regions associated with spike and kernel traits. Theor Appl Genet 135, 2953–2967 (2022). https://doi.org/10.1007/s00122-022-04160-6
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DOI: https://doi.org/10.1007/s00122-022-04160-6