Abstract
In the present study in wheat, GWAS was conducted for identification of marker trait associations (MTAs) for the following six grain morphology traits: (1) grain cross-sectional area (GCSA), (2) grain perimeter (GP), (3) grain length (GL), (4) grain width (GWid), (5) grain length–width ratio (GLWR) and (6) grain form-density (GFD). The data were recorded on a subset of spring wheat reference set (SWRS) comprising 225 diverse genotypes, which were genotyped using 10,904 SNPs and phenotyped for two consecutive years (2017–2018, 2018–2019). GWAS was conducted using five different models including two single-locus models (CMLM, SUPER), one multi-locus model (FarmCPU), one multi-trait model (mvLMM) and a model for Q x Q epistatic interactions. False discovery rate (FDR) [P value -log10(p) ≥ 5] and Bonferroni correction [P value -log10(p) ≥ 6] (corrected p value < 0.05) were applied to eliminate false positives due to multiple testing. This exercise gave 88 main effect and 29 epistatic MTAs after FDR and 13 main effect and 6 epistatic MTAs after Bonferroni corrections. MTAs obtained after Bonferroni corrections were further utilized for identification of 55 candidate genes (CGs). In silico expression analysis of CGs in different tissues at different parts of the seed at different developmental stages was also carried out. MTAs and CGs identified during the present study are useful addition to available resources for MAS to supplement wheat breeding programmes after due validation and also for future strategic basic research.
Similar content being viewed by others
References
Ain QU, Rasheed A, Anwar A et al (2015) Genome-wide association for grain yield under rainfed conditions in historical wheat cultivars from Pakistan. Front Plant Sci 6:1–15
Alemu A, Feyissa T, Tuberosa R et al (2020) Genome-wide association mapping for grain shape and color traits in Ethiopian durum wheat (Triticum turgidum ssp durum). Crop J 8:757
Alemu A, Suliman S, Hagras A et al (2021) Multi-model genome-wide association and genomic prediction analysis of 16 agronomic, physiological and quality related traits in ICARDA spring wheat. Euphytica 217:1–22
Allard RW (1999) Principles of plant breeding, 2nd edn. John Wiley & Sons, Hoboken
An J, Li Q, Yang J et al (2019) Wheat F-box protein TaFBA1 positively regulates plant drought tolerance but negatively regulates stomatal closure. Front Plant Sci 10:1–20
Arora S, Singh N, Kaur S et al (2017) Genome-wide association study of grain architecture in wild wheat aegilops tauschii. Front Plant Sci 8:1–13
Bates D, Machler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Bateson W (1909) Mendel’s Principles of Heredity: Cambridge University Press. März 1909; 2nd Impr, 3:1913.
Boeven PHG, Zhao Y, Thorwarth P et al (2020) Negative dominance and dominance-by-dominance epistatic effects reduce grain-yield heterosis in wide crosses in wheat. Sci Adv 6:1–12
Bradbury PJ, Zhang Z, Kroon DE, et al (2008) Genetics and population analysis TASSEL: software for association mapping of complex traits in diverse samples
Breseghello F, Sorrells ME (2007) QTL analysis of kernel size and shape in two hexaploid wheat mapping populations. Field Crops Res 101:172–179
Cabral AL, Jordan MC, Larson G et al (2018) Relationship between QTL for grain shape, grain weight, test weight, milling yield, and plant height in the spring wheat cross RL4452/ ‘AC Domain.’ PLoS ONE 13:1–32
Campbell BT, Baenziger PS, Gill KS et al (2003) Identification of QTLs and environmental interactions associated with agronomic traits on chromosome 3A of wheat. Crop Sci 43:1493–1505
Chastain TG, Ward KJ, Wysocki DJ (1995) Stand establishment responses of soft white winter wheat to seedbed residue and seed size. Crop Sci 35:213–218
Chen Y, Wu H, Yang W, Zhao W, Tong C (2021) Multivariate linear mixed model enhanced the power of identifying genome-wide association to poplar tree heights in a randomized complete block design. G3 11:1–32
Cho J II, Kim HB, Kim CY, Hahn TR, Jeon JS (2011) Identification and characterization of the duplicate rice sucrose synthase genes OsSUS5 and OsSUS7 which are associated with the plasma membrane. Mol Cells 31:553–561
Cortes LT, Zhang Z, Yu J (2021) Status and prospects of genome-wide association studies in plants. Plant Genome 14:1–38
Dai Z, Yin Y, Wang Z (2009) Comparison of starch accumulation and enzyme activity in grains of wheat cultivars differing in kernel type. Plant Growth Regul 57:153–162
Deng X, Wang B, Fisher V, Peloso G, Cupples A, Liu CT (2018) Genome-wide association study for multiple phenotype analysis. BMC Proc 12:139–144
Dholakia BB, Ammiraju JSS, Singh H et al (2003) Molecular marker analysis of kernel size and shape in bread wheat. Plant Breed 122:392–395
Dong X, Jiang Y, Hur Y (2019) Genome-wide analysis of glycoside hydrolase family 1 β-glucosidase genes in Brassica rapa and their potential role in Pollen development. Int J Mol Sci 20:1–17
Evers AD (2000) Grain size and morphology: implications for quality. Spec Publ-Royal Soc Chem 212:19–24
Feldman M, Levy AA, Fahima T, Korol A (2012) Genomic asymmetry in allopolyploid plants: wheat as a model. J Exp Bot 63:5045–5059
Furlotte NA, Eskin E (2015) Efficient multiple-trait association and estimation of genetic correlation using the matrix-variate linear mixed model. Genetics 200:59–68
Gahlaut V, Jaiswal V, Singh S, Balyan HS, Gupta PK (2019) Multi-locus genome wide association mapping for yield and its contributing traits in hexaploid wheat under different water regimes. Sci Rep 9:1–15
Gahlaut V, Kumari P, Jaiswal V, Kumar S (2021) Genetics, genomics and breeding in Rosa species. J Hortic Sci Biotechnol 96:1–16
Gahlaut V, Zinta G, Jaiswal V, Kumar S (2020) Quantitative epigenetics: a new avenue for crop improvement. Epigenomes 4:1–17
Gan Y, Stobbe EH (1996) Seedling vigor and grain yield of “Roblin” wheat affected by seed size. Agron J 88:456–460
Gao Y, Xu X, Jin J et al (2021) Dissecting the genetic basis of grain morphology traits in Chinese wheat by genome wide association study. Euphytica 217:1–12
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
Giura A, Saulescu NN (1996) Chromosomal location of genes controlling grain size in a large grained selection of wheat (Triticum aestivum L.). Euphytica 89:77–80
Gonzalez JR, Armengol L, Solé X et al (2007) SNPassoc: an R package to perform whole genome association studies. Bioinformatics 23:644–645
Gupta PK, Balyan HS, Kulwal PL et al (2007) QTL analysis for some quantitative traits in bread wheat. J Zhejiang Univ Sci B 8:807–814
Gupta PK, Kulwal PL, Jaiswal V (2014) Association mapping in crop plants: opportunities and challenges. Adv Genet 85:109–147
Gupta PK, Kulwal PL, Jaiswal V (2019) Association mapping in plants in the post-GWAS genomics era. Adv Genet 104:75–154
Holland JB (2001) Epistasis and plant breeding. Plant Breed Rev 21:27–92
Hu J, Wang Y, Fang Y et al (2015) A rare allele of GS2 enhances grain size and grain yield in rice. Mol Plant 8:1455–1465
Huang R, Jiang L, Zheng J et al (2013) Genetic bases of rice grain shape: So many genes, so little known. Trends Plant Sci 18:218–226
Huang M, Liu X, Zhou Y et al (2018) BLINK: a package for the next level of genome-wide association studies with both individuals and markers in the millions. GigaScience 8:1–12
IWGSC (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 345:1251788
Jaiswal V, Gahlaut V, Meher PK et al (2016) Genome wide single locus single trait, multi-locus and multi-trait association mapping for some important agronomic traits in common wheat (T. aestivum L.). PLoS ONE 11:1–25
Jamil M, Ali A, Gul A et al (2019) Genome-wide association studies of seven agronomic traits under two sowing conditions in bread wheat. BMC Plant Biol 19:1–18
Jiang C, Xiao S, Li D et al (2019) Identification and expression pattern analysis of bacterial blight resistance genes in Oryza officinalis wall ex watt under xanthomonas oryzae Pv. oryzae Stress. Plant Mol Biol Report 37:436–449
Jing HC, Kornyukhin D, Kanyuka K et al (2007) Identification of variation in adaptively important traits and genome-wide analysis of trait-marker associations in Triticum monococcum. J Exp Bot 58:3749–3764
Kao CH, Zeng ZB, Teasdale RD (1999) Multiple interval mapping for quantitative trait loci. Genetics 152:1203–1216
Korte A, Vilhjálmsson BJ, Segura V, Platt A, Long Q, Nordborg M (2012) A mixed-model approach for genome-wide association studies of correlated traits in structured populations. Nat Genet 44:1066–1071
Kovach MJ, Sweeney MT, McCouch SR (2007) New insights into the history of rice domestication. Trends Genet 23:578–587
Kumar J, Saripalli G, Gahlaut V et al (2018) Genetics of Fe, Zn, β-carotene, GPC and yield traits in bread wheat (Triticum aestivum L.) using multi-locus and multi-traits GWAS. Euphytica 214:1–17
Kumari S, Jaiswal V, Mishra VK, Paliwal R, Balyan HS, Gupta PK (2018) QTL mapping for some grain traits in bread wheat (Triticum aestivum L.). Physiol Mol Biol Plants 24:909–920
Langer SM, Longin CFH, Würschum T (2014) Flowering time control in European winter wheat. Front Plant Sci 5:1–12
Li J, Horstman B, Chen Y (2011) Detecting epistatic effects in association studies at a genomic level based on an ensemble approach. Bioinformatics 27:222–229
Li Q, Zhang Y, Liu T et al (2015) Genetic analysis of kernel weight and kernel size in wheat (Triticum aestivum L.) using unconditional and conditional QTL mapping. Mol Breed 35:1–15
Lipka AE, Tian F, Wang Q et al (2012) GAPIT: Genome association and prediction integrated tool. Bioinformatics 28:2397–2399
Liu X, Huang M, Fan B, Buckler ES, Zhang Z (2016) Iterative usage of fixed and random effect models for powerful and efficient genome-wide association studies. PLOS Genet 12:1–24
Lu HY, Liu XF, Wei SP, Zhang YM (2011) Epistatic association mapping in homozygous crop cultivars. PLoS One 6:e17773
Ma J, Zhang H, Li S et al (2019) Identification of quantitative trait loci for kernel traits in a wheat cultivar Chuannong16. BMC Genet 20:1–12
Mackay TF (2014) Epistasis and quantitative traits: using model organisms to study gene-gene interactions. Nat Rev Genet 15:22–33
Malik P, Kumar J, Singh S et al (2021) Single-trait, multi-locus and multi-trait GWAS using four different models for yield traits in bread wheat. Mol Breed 41:1–21
Maulana F, Ayalew H, Anderson JD, Kumssa TT, Huang W, Ma XF (2018) Genome-wide association mapping of seedling heat tolerance in winter wheat. Front Plant Sci 9:1–16
Mendiburu D, Yaseen M (2020) Agricolae: s tatistical procedures for agricultural research, R package version 1.4.0.
Merida-García R, Bentley AR, Gálvez S et al (2020) Mapping agronomic and quality traits in elite durum wheat lines under differing water regimes. Agronomy 10:1–23
Moellers TC, Singh A, Zhang J et al (2017) Main and epistatic loci studies in soybean for Sclerotinia sclerotiorum resistance reveal multiple modes of resistance in multi-environments. Sci Rep 7:1–13
Niel C, Sinoquet C, Dina C, Rocheleau G (2015) A survey about methods dedicated to epistasis detection. Front Genet 6:285
Okamoto Y, Nguyen AT, Yoshioka M, Iehisa JCM, Takumi S (2013) Identification of quantitative trait loci controlling grain size and shape in the D genome of synthetic hexaploid wheat lines. Breed Sci 63:423–429
Patil RM, Tamhankar SA, Oak MD et al (2013) Mapping of QTL for agronomic traits and kernel characters in durum wheat (Triticum durum Desf.). Euphytica 190:117–129
Peterson BG, Carl P, Boudt K et al (2018) Package ‘PerformanceAnalytics.’ R Team Cooperation 3:13–14
Prashant R, Kadoo N, Desale C et al (2012) Kernel morphometric traits in hexaploid wheat (Triticum aestivum L.) are modulated by intricate QTL × QTL and genotype × environment interactions. J Cereal Sci 56:432–439
Qaseem MF, Qureshi R, Muqaddasi QH, Shaheen H, Kousar R, Roder MS (2018) Genome-wide association mapping in bread wheat subjected to independent and combined high temperature and drought stress. PLoS ONE 13:1–22
Rahimi Y, Bihamta MR, Taleei A, Alipour H, Ingvarsson PK (2019) Genome-wide association study of agronomic traits in bread wheat reveals novel putative alleles for future breeding programs. BMC Plant Biol 19:1–19
Ramya P, Chaubal A, Kulkarni K et al (2010) QTL mapping of 1000-kernel weight, kernel length, and kernel width in bread wheat (Triticum aestivum L.). J Appl Genet 51:421–429
Rasheed A, Xia X, Ogbonnaya F et al (2014) Genome-wide association for grain morphology in synthetic hexaploid wheats using digital imaging analysis. BMC Plant Biol 14:1–21
Reif JC, Maurer HP, Korzun V, Ebmeyer E, Miedaner T, Wurschum T (2011) Mapping QTLs with main and epistatic effects underlying grain yield and heading time in soft winter wheat. Theor Appl Genet 123:283–292
Ritchie MD, Van Steen K (2018) The search for gene-gene interactions in genome-wide association studies: challenges in abundance of methods, practical considerations, and biological interpretation. Ann Transl Med 6:1–14
Rouse MN, Talbert LE, Singh D, Sherman JD (2014) Complementary epistasis involving Sr12 explains adult plant resistance to stem rust in Thatcher wheat (Triticum aestivum L.). Theor Appl Genet 127:1549–1559
Röder MS, Huang XQ, Börner A (2008) Fine mapping of the region on wheat chromosome 7D controlling grain weight. Funct Integr Genom 8:79–86
Schierenbeck M, Alqudah AM, Lohwasser U, Tarawneh RA, Simon MR (2021) Genetic dissection of grain architecture-related traits in a winter wheat population. BMC Plant Biol 21:1–14
Sehgal D, Autrique E, Singh R, Ellis M, Singh S, Dreisigacker S (2017) Identification of genomic regions for grain yield and yield stability and their epistatic interactions. Sci Rep 7:1–12
Sehgal D, Rosyara U, Mondal S et al (2020) Incorporating genome-wide association mapping results into genomic prediction models for grain yield and yield stability in CIMMYT spring bread wheat. Front Plant Sci 11:197
Shubha V, Giri J, Dansana PK, Kapoor S, Tyagi AK (2008) The receptor-like cytoplasmic kinase (OsRLCK) gene family in rice: Organization, phylogenetic relationship, and expression during development and stress. Mol Plant 1:732–750
Singh K, Batra R, Sharma S, et al (2021) WheatQTLdb: a QTL database for wheat. Mol Genet Genomics 1–7.
Slim L, Chatelain C, Azencott CA, Vert JP (2020) Novel methods for epistasis detection in genome-wide association studies. PLoS One 15:e0242927
Sun C, Dong Z, Zhao L, Ren Y, Zhang N, Chen F (2020) The Wheat 660K SNP array demonstrates great potential for marker-assisted selection in polyploid wheat. Plant Biotechnol J 18:1354–1360
Sun XY, Wu K, Zhao Y et al (2009) QTL analysis of kernel shape and weight using recombinant inbred lines in wheat. Euphytica 165:615–624
Sun C, Zhang F, Yan X et al (2017) Genome-wide association study for 13 agronomic traits reveals distribution of superior alleles in bread wheat from the Yellow and Huai Valley of China. Plant Biotechnol J 15:953–969
Tanabata T, Shibaya T, Hori K, Ebana K, Yano M (2012) SmartGrain: high-throughput phenotyping software for measuring seed shape through image analysis. Plant Physiol 160:1871–1880
Tang Y, Liu X, Wang J et al (2016) GAPIT version 2: an enhanced integrated tool for genomic association and prediction. Plant Genome 9:1–9
Thudi M, Chen Y, Pang J et al (2021) Novel genes and genetic loci associated with root morphological traits, phosphorus-acquisition efficiency and phosphorus-use efficiency in chickpea. Front Plant Sci. https://doi.org/10.3389/fpls.2021.636973
Tyagi S, Mir RR, Kaur H et al (2014) Marker-assisted pyramiding of eight QTLs/genes for seven different traits in common wheat (Triticum aestivum L.). Mol Breed 34:167–175
VanRaden PM (2008) Efficient methods to compute genomic predictions. J Dairy Sci 91:4414–4423
Wang X, Dong L, Hu J et al (2019) Dissecting genetic loci affecting grain morphological traits to improve grain weight via nested association mapping. Theor Appl Genet 132:3115–3128
Wang Q, Tian F, Pan Y, Buckler ES, Zhang Z (2014) A SUPER powerful method for genome wide association study. PLoS ONE 9:1–9
Wang SX, Zhu YL, Zhang DX et al (2017) Genome-wide association study for grain yield and related traits in elite wheat varieties and advanced lines using SNP markers. PLoS ONE 12:1–14
Wang J, Zhang Z (2021) GAPIT Version 3: boosting power and accuracy for genomic association and prediction. Genomics Proteomics Bioinformatics (Published online Sep 4, 2021).
Williams K, Munkvold J, Sorrells M (2013) Comparison of digital image analysis using elliptic Fourier descriptors and major dimensions to phenotype seed shape in hexaploid wheat (Triticum aestivum L.). Euphytica 190:99–116
Williams K, Sorrells ME (2014) Three-dimensional seed size and shape QTL in hexaploid wheat (Triticum aestivum L.) populations. Crop Sci 54:98–110
Wu J, Zhang J, Wang S, Kong F (2016) Assessment of food security in China: a new perspective based on production-consumption coordination. Sustain 8:1–14
Xin F, Zhu T, Wei S et al (2020) OPEN QTL mapping of kernel traits and validation of a major QTL for kernel length-width ratio using SNP and bulked segregant analysis in wheat. Sci Rep 10:1–12
Xu Y, An D, Liu D, Zhang A, Xu H, Li B (2012) Molecular mapping of QTLs for grain zinc, iron and protein concentration of wheat across two environments. F Crop Res 138:57–62
Yan L, Liang F, Xu H et al (2017) Identification of QTL for grain size and shape on the D genome of natural and synthetic allohexaploid wheats with near-identical AABB genomes. Front Plant Sci 8:1–14
Yang Y, Guo M, Sun S et al (2019) Natural variation of OsGluA2 is involved in grain protein content regulation in rice. Nat Commun 10:1–12
Yoshioka M, Takenaka S, Nitta M, Li J, Mizuno N, Nasuda S (2019) Genetic dissection of grain morphology in hexaploid wheat by analysis of the NBRP-Wheat core collection. Genes Genet Syst 94:35
Yu K, Liu D, Chen Y et al (2019) Unraveling the genetic architecture of grain size in einkorn wheat through linkage and homology mapping and transcriptomic profiling. J Exp Bot 70:4671–4687
Yu K, Liu D, Wu W et al (2017) Development of an integrated linkage map of einkorn wheat and its application for QTL mapping and genome sequence anchoring. Theor Appl Genet 130:53–70
Yu LX, Lorenz A, Rutkoski J et al (2011) Association mapping and gene-gene interaction for stem rust resistance in CIMMYT spring wheat germplasm. Theor Appl Genet 123:1257–1268
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
Zhang Z, Ersoz E, Lai CQ et al (2010) Mixed linear model approach adapted for genome-wide association studies. Nat Genet 42:355–360
Zhang J, Zhang J, Liu W et al (2015) Introgression of Agropyron cristatum 6P chromosome segment into common wheat for enhanced thousand-grain weight and spike length. Theor Appl Genet 128:1827–1837
Zheng J, Zhang Y, Wang C (2015) Molecular functions of genes related to grain shape in rice. Breed Sci 65:120–126
Zhou X, Stephens M (2012) Genome-wide efficient mixed-model analysis for association studies. Nat Genet 44:821–824
Acknowledgements
The material for association panel and the genotypic data for this work was received from CIMMYT, Mexico. Thanks are due to the Department of Biotechnology (DBT), Govt of India for providing funds in the form of research projects awarded to Shailendra Sharma. The authors are thankful to Ch. Charan Singh University, Meerut for providing laboratory and field facilities. Harindra Singh Balyan was awarded positions of INSA Senior Scientist/Honorary Scientist during the course of the study by INSA, New Delhi.
Author information
Authors and Affiliations
Contributions
Shailendra Sharma conceived and conducted or directed the experiments. Parveen Malik, Jitendra Kumar and Shiveta Sharma performed the experiments. Prabina Kumar Meher, Jitendra Kumar, Parveen Malik analysed the data. Harindra Singh Balyan, Pushpendra Kumar Gupta and Shailendra Sharma participated in manuscript writing. Shailendra Sharma finalized the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
There is no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Malik, P., Kumar, J., Sharma, S. et al. GWAS for main effects and epistatic interactions for grain morphology traits in wheat. Physiol Mol Biol Plants 28, 651–668 (2022). https://doi.org/10.1007/s12298-022-01164-w
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12298-022-01164-w