Abstract
Bread wheat (Triticum aestivum L.) is a global staple crop vital for human nutrition. Heading date (HD) and flowering date (FD) are critical traits influencing wheat growth, development, and adaptability to diverse environmental conditions. A comprehensive study were conducted involving 190 bread wheat accessions to unravel the genetic basis of HD and FD using high-throughput genotyping and multi-environment field trials. Seven independent quantitative trait loci (QTLs) were identified to be significantly associated with HD and FD using two GWAS methods, which explained a proportion of phenotypic variance ranging from 1.43% to 9.58%. Notably, QTLs overlapping with known vernalization genes Vrn-D1 were found, validating their roles in regulating flowering time. Moreover, novel QTLs on chromosome 2A, 5B, 5D, and 7B associated with HD and FD were identified. The effects of these QTLs on HD and FD were confirmed in an additional set of 74 accessions across different environments. An increase in the frequency of alleles associated with early flowering in cultivars released in recent years was also observed, suggesting the influence of molecular breeding strategies. In summary, this study enhances the understanding of the genetic regulation of HD and FD in bread wheat, offering valuable insights into crop improvement for enhanced adaptability and productivity under changing climatic conditions. These identified QTLs and associated markers have the potential to improve wheat breeding programs in developing climate-resilient varieties to ensure food security.
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Data availability
All data that support the findings in this study are available in this article and its supplementary files. Furthermore, the R code used for conducting the statistical analysis has been submitted and is available at the following repository: https://github.com/qiao-001/SNP_HBbaseGWAS.
References
Abboye AD, Megersa A, Hirpa D (2020) Effect of plant population on growth, yields & quality of bread wheat (Triticum Aestivum L.) varieties at Kulumsa in Arsi Zone, South-Eastern Ethiopia. Int J Res Stud Agric Sci 6(2):32–53. https://doi.org/10.20431/2454-6224.0602005
Aldrich J, Cullis CA (1993) RAPD analysis in flax: Optimization of yield and reproducibility using klen Taq 1 DNA polymerase, chelex 100, and gel purification of genomic DNA. Plant Mol Biol Report 11(2):128–141. https://doi.org/10.1007/BF02670471
Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19:1655–1664. https://doi.org/10.1101/gr.094052.109
Amasino RM, Michaels SD (2010) The timing of flowering. Plant Physiol 154(2):516–520. https://doi.org/10.1104/pp.110.161653
Andeden E, Yediay F, Baloch F, Shaaf S, Kilian B, Nachit M, Özkan H (2011) Distribution of vernalization and photoperiod genes (Vrn-A1, Vrn-B1, Vrn-D1, Vrn-B3, Ppd-D1) in Turkish bread wheat cultivars and landraces. Cereal Res Commun 39(3):352–364. https://doi.org/10.1556/CRC.39.2011.3.5
Arjona JM, Villegas D, Ammar K et al (2020) The effect of photoperiod genes and flowering time on yield and yield stability in durum wheat. Plants 9:1723. https://doi.org/10.3390/plants9121723
Bates D, Mächler M, Bolker BM, Walker SC (2014) Fitting Linear Mixed-Effects Models Using lme4. 1. https://doi.org/10.18637/jss.v067.i01
Boden SA, Cavanagh C, Cullis BR, Ramm K, Greenwood J, Jean Finnegan E, Trevaskis B, Swain SM (2015) Ppd-1 is a key regulator of inflorescence architecture and paired spikelet development in wheat. Nat Plants 1(January):2–7. https://doi.org/10.1038/nplants.2014.16
Cane K, Eagles HA, Laurie DA, Trevaskis B, Vallance N, Eastwood RF, Gororo NN, Kuchel H, Martin PJ (2013) Ppd-B1 and Ppd-D1 and their effects in southern Australian wheat. Crop Pasture Sci 64(2):100–114. https://doi.org/10.1071/CP13086
Cao Y, Hu G, Zhuang M, Yin J, Wang X (2021) Molecular cloning and functional characterization of TaIRI9 gene in wheat (Triticum aestivum L.). Gene 791:145694. https://doi.org/10.1016/J.GENE.2021.145694
Capovilla G, Schmid M, Posé D (2015) Control of flowering by ambient temperature. J Exp Bot 66(1):59–69. https://doi.org/10.1093/jxb/eru416
Chai L, Xin M, Dong C, Chen Z, Zhai H, Zhuang J, Cheng X, Wang N, Geng J, Wang X, Bian R, Yao Y, Guo W, Hu Z, Peng H, Bai G, Sun Q, Su Z, Liu J, Ni Z (2022) A natural variation in Ribonuclease H-like gene underlies Rht8 to confer “Green Revolution” trait in wheat. Mol Plant 15(3):377–380. https://doi.org/10.1016/J.MOLP.2022.01.013
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020a) TBtools: An Integrative Toolkit Developed for Interactive Analyses of Big Biological Data. Shengwei Ma, Meng Wang, Jianhui Wu, Weilong Guo, Yongming Chen, Guangwei Li, Yanpeng Wang, Weiming Shi, Guangmin Xia, Daolin Fu, Zhensheng Kang, Fei Ni 13(8):1194–1202. https://doi.org/10.1016/j.molp.2020.06.009
Chen S, Cheng X, Yu K, Chang X, Bi H, Xu H, Wang J, Pei X, Zhang Z, Zhan K (2020b) Genome-wide association study of differences in 14 agronomic traits under low- and high-density planting models based on the 660k SNP array for common wheat. Plant Breed 139(2):272–283. https://doi.org/10.1111/pbr.12774
Cho EJ, Kang C-S, Jung J-U, Yoon YM, Park CS (2015) Allelic variation of Rht-1, Vrn-1 and Ppd-1 in Korean wheats and its effect on agronomic traits. Plant Breed Biotechnol 3(2):129–138. https://doi.org/10.9787/pbb.2015.3.2.129
Choi K, Kim J, Hwang HJ, Kim S, Park C, Kim SY, Lee I (2011) The FRIGIDA complex activates transcription of FLC, a strong flowering repressor in Arabidopsis, by recruiting chromatin modification factors. Plant Cell 23(1):289–303. https://doi.org/10.1105/tpc.110.075911
Chumanova EV, Efremova TT, Kruchinina YV (2020) The effect of different dominant VRN alleles and their combinations on the duration of developmental phases and productivity in common wheat lines. Russ J Genet 56(7):822–834. https://doi.org/10.1134/S1022795420070029
Dai C, Xue HW (2010) Rice early flowering1, a CKI, phosphorylates della protein SLR1 to negatively regulate gibberellin signalling. EMBO J 29(11):1916–1927. https://doi.org/10.1038/emboj.2010.75
Dai X, You C, Chen G, Li X, Zhang Q, Wu C (2011) OsBC1L4 encodes a COBRA-like protein that affects cellulose synthesis in rice. Plant Mol Biol 75(4–5):333–345. https://doi.org/10.1007/S11103-011-9730-Z/FIGURES/7
Distelfeld A, Li C, Dubcovsky J (2009) Regulation of flowering in temperate cereals. Curr Opin Plant Biol 12(2):178–184. https://doi.org/10.1016/j.pbi.2008.12.010
Dong SS, He WM, Ji JJ, Zhang C, Guo Y, Yang TL (2021) LDBlockShow: a fast and convenient tool for visualizing linkage disequilibrium and haplotype blocks based on variant call format files. Brief Bioinform 22(4):1–6. https://doi.org/10.1093/bib/bbaa227
Dyck JRB, Cheng JF, Stanley WC, Barr R, Chandler MP, Brown S, Wallace D, Arrhenius T, Harmon C, Yang G, Nadzan AM, Lopaschuk GD (2004) Malonyl coenzyme a decarboxylase inhibition protects the ischemic heart by inhibiting fatty acid oxidation and stimulating glucose oxidation. Circ Res 94(9). https://doi.org/10.1161/01.res.0000129255.19569.8f
Ellis MH, Bonnett DG, Rebetzke GJ (2007) A 192bp allele at the Xgwm261 locus is not always associated with the Rht8 dwarfing gene in wheat (Triticum aestivum L.). Euphytica 157(1–2):209–214. https://doi.org/10.1007/s10681-007-9413-7
Guo Z, Song Y, Zhou R, Ren Z, Jia J (2010) Discovery, evaluation and distribution of haplotypes of the wheat Ppd-D1 gene. New Phytol 185(3):841–851. https://doi.org/10.1111/j.1469-8137.2009.03099.x
Gupta P, Kabbaj H, Hassouni KE, Maccaferri M, Sanchez-Garcia M, Tuberosa R, Bassi FM (2020) Genomic regions associated with the control of flowering time in durum wheat. Plants 9(12):1–18. https://doi.org/10.3390/plants9121628
Hamazaki K, Iwata H (2020) Rainbow: Haplotype-based genome-wide association study using a novel SNP-set method. PLoS Comput Biol 16(2):e1007663. https://doi.org/10.1371/journal.pcbi.1007663
Harris FAJ, Eagles HA, Virgona JM, Martin PJ, Condon JR, Angus JF (2017) Effect of VRN1 and PPD1 genes on anthesis date and wheat growth. Crop Pasture Sci 68(3):195–201. https://doi.org/10.1071/CP16420
Huang X, Wei X, Sang T, Zhao Q, Feng Q, Zhao Y, Li C, Zhu C, Lu T, Zhang Z, Li M, Fan D, Guo Y, Wang A, Wang L, Deng L, Li W, Lu Y, Weng Q, … Han B (2010) Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 42:11:961–967. https://doi.org/10.1038/ng.695
Huo H, Wei S, Bradford KJ (2016) DELAY OF GERMINATION1 ( DOG1) regulates both seed dormancy and flowering time through microRNA pathways. Proc Natl Acad Sci 113(15):E2199–E2206. https://doi.org/10.1073/pnas.1600558113
Jia H, Wan H, Yang S, Zhang Z, Kong Z, Xue S, Zhang L, Ma Z (2013) Genetic dissection of yield-related traits in a recombinant inbred line population created using a key breeding parent in China’s wheat breeding. Theor Appl Genet 126(8):2123–2139. https://doi.org/10.1007/s00122-013-2123-8
Kamran A, Iqbal M, Spaner D (2014) Flowering time in wheat (Triticum aestivum L.): A key factor for global adaptability. Euphytica 197(1):1–26. https://doi.org/10.1007/s10681-014-1075-7
Kane NA, Agharbaoui Z, Diallo AO, Adam H, Tominaga Y, Ouellet F, Sarhan F (2008) TaVRT2 represses transcription of the wheat vernalization gene TaVRN1 (Plant Journal (2007) 51, (670–680)). Plant J 53(2):400. https://doi.org/10.1111/j.1365-313X.2007.03386.x
Kippes N, Debernardi JM, Vasquez-Gross HA, Akpinar BA, Budak H, Kato K, Chao S, Akhunov E, Dubcovsky J (2015) Identification of the VERNALIZATION 4 gene reveals the origin of spring growth habit in ancient wheats from South Asia. Proc Natl Acad Sci USA 112(39):E5401–E5410. https://doi.org/10.1073/pnas.1514883112
Kiseleva AA, Potokina EK, Salina EA (2017) Features of Ppd-B1 expression regulation and their impact on the flowering time of wheat near-isogenic lines. BMC Plant Biol 17(Suppl 1). https://doi.org/10.1186/s12870-017-1126-z
Kosová K, Prášil IT, Vítámvás P (2008) The relationship between vernalization- and photoperiodically-regulated genes and the development of frost tolerance in wheat and barley. Biol Plant 52(4):601–615. https://doi.org/10.1007/s10535-008-0120-6
Law CN, Worland AJ (1997) The control of adult-plant resistance to yellow rust by the translocated chromosome 5BS-7BS of bread wheat. Plant Breed 116(1):59–63. https://doi.org/10.1111/j.1439-0523.1997.tb00975.x
Li S, Ge FR, Xu M, Zhao XY, Huang GQ, Zhou LZ, Wang JG, Kombrink A, McCormick S, Zhang XS, Zhang Y (2013) Arabidopsis COBRA-LIKE 10, a GPI-anchored protein, mediates directional growth of pollen tubes. Plant J 74(3):486–497. https://doi.org/10.1111/TPJ.12139
Li Y, Xiong H, Guo H, Zhou C, Xie Y, Zhao L, Gu J, Zhao S, Ding Y, Liu L (2020) Identification of the vernalization gene VRN-B1 responsible for heading date variation by QTL mapping using a RIL population in wheat. BMC Plant Biol 20(1):1–15. https://doi.org/10.1186/s12870-020-02539-5
Ma S, Wang M, Wu J, Guo W, Chen Y, Li G, Wang Y, Shi W, Xia G, Fu D, Kang Z, Ni F (2021) WheatOmics: a platform combining multiple omics data to accelerate functional genomics studies in wheat. Mol Plant 1674(21):430. https://doi.org/10.1016/j.molp.2021.10.006
Mitchell RAC, Castells-Brooke N, Taubert J, Verrier PJ, Leader DJ, Rawlings CJ (2007) Wheat Estimated Transcript Server (WhETS): A tool to provide best estimate of hexaploid wheat transcript sequence. Nucleic Acids Res 35(SUPPL.2):148–151. https://doi.org/10.1093/nar/gkm220
Mizuno N, Nitta M, Sato K, Nasuda S (2012) A wheat homologue of PHYTOCLOCK 1 is a candidate gene conferring the early heading phenotype to einkorn wheat. Genes Genet Syst 87(6):357–367. https://doi.org/10.1266/ggs.87.357
Mohler V, Lukman R, Ortiz-Islas S, William M, Worland AJ, Van Beem J, Wenzel G (2004) Genetic and physical mapping of photoperiod insensitive gene Ppd-B1 in common wheat. Euphytica 138(1):33–40. https://doi.org/10.1023/B:EUPH.0000047056.58938.76
Okada T, Jayasinghe JEARM, Eckermann P, Watson-Haigh NS, Warner P, Hendrikse Y, Baes M, Tucker EJ, Laga H, Kato K, Albertsen M, Wolters P, Fleury D, Baumann U, Whitford R (2019) Effects of Rht-B1 and Ppd-D1 loci on pollinator traits in wheat. Theor Appl Genet 0123456789. https://doi.org/10.1007/s00122-019-03329-w
Pang Y, Liu C, Wang D, st. Amand P, Bernardo A, Li W, He F, Li L, Wang L, Yuan X, Dong L, Su Y, Zhang H, Zhao M, Liang Y, Jia H, Shen X, Lu Y, Jiang H, … Liu S (2020) High-resolution genome-wide association study identifies genomic regions and candidate genes for important agronomic traits in wheat. Mol Plant 13(9):1311–1327. https://doi.org/10.1016/j.molp.2020.07.008
Piñeiro M, Jarillo JA (2013) Ubiquitination in the control of photoperiodic flowering. In: Plant Science (Vol 198), pp 98–109. https://doi.org/10.1016/j.plantsci.2012.10.005
Ramírez-González RH, Borrill P, Lang D, Harrington SA, Brinton J, Venturini L, Davey M, Jacobs J, van Ex F, Pasha A, Khedikar Y, Robinson SJ, Cory AT, Florio T, Concia L, Juery C, Schoonbeek H, Steuernagel B, Xiang D, … Uauy C (2018) The transcriptional landscape of polyploid wheat. Science 361(6403). https://doi.org/10.1126/science.aar6089
R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
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 135:1049–1081. https://doi.org/10.1007/s00122-021-04018
Seki M, Chono M, Matsunaka H, Fujita M, Oda S, Kubo K, Kiribuchi-Otobe C, Kojima H, Nishida H, Kato K (2011) Distribution of photoperiod-insensitive alleles Ppd-B1a and Ppd-D1a and their effect on heading time in Japanese wheat cultivars. Breed Sci 61(4):405–412. https://doi.org/10.1270/jsbbs.61.405
Shcherban AB, Börner A, Salina EA (2015) Effect of VRN-1 and PPD-D1 genes on heading time in European bread wheat cultivars. Plant Breed 134(1):49–55. https://doi.org/10.1111/pbr.12223
Shimada S, Ogawa T, Kitagawa S, Suzuki T, Ikari C, Shitsukawa N, Abe T, Kawahigashi H, Kikuchi R, Handa H, Murai K (2009) A genetic network of flowering-time genes in wheat leaves, in which an APETALA1/FRUITFULL-like gene, VRN1, is upstream of FLOWERING LOCUS T. Plant J 58(4):668–681. https://doi.org/10.1111/j.1365-313X.2009.03806.x
Song J, Irwin J, Dean C (2013) Remembering the prolonged cold of winter. Curr Biol 23(17). https://doi.org/10.1016/J.CUB.2013.07.027
Sun H, Guo Z, Gao L, Zhao G, Zhang W, Zhou R, Wu Y, Wang H, An H, Jia J (2014) DNA methylation pattern of Photoperiod-B1 is associated with photoperiod insensitivity in wheat (Triticum aestivum). New Phytol 204(3):682–692. https://doi.org/10.1111/nph.12948
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(6):1354–1360. https://doi.org/10.1111/pbi.13361
Wang J, Zhang Z (2021) GAPIT version 3: boosting power and accuracy for genomic association and prediction. Genomics Proteomics Bioinformatics. https://doi.org/10.1016/J.GPB.2021.08.005
Whittal A, Kaviani M, Graf R, Humphreys G, Navabi A (2018) Allelic variation of vernalization and photoperiod response genes in a diverse set of North American high latitude winter wheat genotypes. PLoS ONE 13(8):1–17. https://doi.org/10.1371/journal.pone.0203068
Wilhelm EP, Boulton MI, Al-Kaff N, Balfourier F, Bordes J, Greenland AJ, Powell W, Mackay IJ (2013) Rht-1 and Ppd-D1 associations with height, GA sensitivity, and days to heading in a worldwide bread wheat collection. Theor Appl Genet 126(9):2233–2243. https://doi.org/10.1007/s00122-013-2130-9
Worland AJ, Sayers EJ, Korzun V (2001) Allelic variation at the dwarfing gene Rht8 locus and its significance in international breeding programmes. In: Bedö Z, Láng L (eds) Wheat in a global environment: Proceedings of the 6th International Wheat Conference, 5–9 June 2000, Budapest, Hungary. Springer Netherlands, Dordrecht, pp 747–753
Würschum T, Langer SM, Longin CFH, Tucker MR, Leiser WL (2018) A three-component system incorporating Ppd-D1, copy number variation at Ppd-B1, and numerous small-effect quantitative trait loci facilitates adaptation of heading time in winter wheat cultivars of worldwide origin. Plant Cell Environ 41(6):1407–1416. https://doi.org/10.1111/pce.13167
Xu S, Dong Q, Deng M, Lin D, Xiao J, Cheng P, Xing L, Niu Y, Gao C, Zhang W, Xu Y, Chong K (2021) The vernalization-induced long non-coding RNA VAS functions with the transcription factor TaRF2b to promote TaVRN1 expression for flowering in hexaploid wheat. Mol Plant 14(9):1525–1538. https://doi.org/10.1016/J.MOLP.2021.05.026
Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J (2003) Positional cloning of the wheat vernalization gene VRN1. Proc Natl Acad Sci USA 100(10):6263–6268. https://doi.org/10.1073/pnas.0937399100
Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, SanMiguel P, Bennetzen JL, Echenique V, Dubcovsky J (2004) The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303(5664):1640–1644. https://doi.org/10.1126/science.1094305
Yan L, Fu D, Li C, Blechl A, Tranquilli G, Bonafede M, Sanchez A, Valarik M, Yasuda S, Dubcovsky J (2006) The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc Natl Acad Sci USA 103(51):19581–19586. https://doi.org/10.1073/pnas.0607142103
Yang FP, Zhang XK, Xia XC, Laurie DA, Yang WX, He ZH (2009) Distribution of the photoperiod insensitive Ppd-D1a allele in Chinese wheat cultivars. Euphytica 165(3):445–452. https://doi.org/10.1007/s10681-008-9745-y
Yang Y, Amo A, Wei D, Chai Y, Zheng J, Qiao P, Cui C, Lu S, Chen L, Hu YG (2021) Large-scale integration of meta-QTL and genome-wide association study discovers the genomic regions and candidate genes for yield and yield-related traits in bread wheat. Theor Appl Genet 134(9):3083–3109. https://doi.org/10.1007/s00122-021-03881-4
Yin L, Zhang H, Tang Z, Xu J, Yin D, Zhang Z, Yuan X, Zhu M, Zhao S, Li X, Liu X (2021) rMVP: a memory-efficient, visualization-enhanced, and parallel-accelerated tool for genome-wide association study. Genomics Proteomics Bioinformatics. https://doi.org/10.1016/j.gpb.2020.10.007
Yoshida T, Nishida H, Zhu J, Nitcher R, Distelfeld A, Akashi Y, Kato K, Dubcovsky J (2010) Vrn-D4 is a vernalization gene located on the centromeric region of chromosome 5D in hexaploid wheat. Theor Appl Genet 120(3):543–552. https://doi.org/10.1007/s00122-009-1174-3
Zhang XK, Xiao YG, Zhang Y, Xia XC, Dubcovsky J, He ZH (2008) Allelic variation at the vernalization genes Vrn-A1, Vrn-B1, Vrn-D1, and Vrn-B3 in Chinese wheat cultivars and their association with growth habit. Crop Sci 48(2):458–470. https://doi.org/10.2135/cropsci2007.06.0355
Zhang X, Gao M, Wang S, Chen F, Cui D (2015) Allelic variation at the vernalization and photoperiod sensitivity loci in Chinese winter wheat cultivars (Triticum aestivum L.). Front Plant Sci 6(JULY):1–10. https://doi.org/10.3389/fpls.2015.00470
Zhang X, Chen J, Yan Y, Yan X, Shi C, Zhao L, Chen F (2018) Genome-wide association study of heading and flowering dates and construction of its prediction equation in Chinese common wheat. Theor Appl Genet 131(11):2271–2285. https://doi.org/10.1007/s00122-018-3181-8
Zhang K, Wang J, Qin H, Wei Z, Hang L, Zhang P, Reynolds M, Wang D (2019) Assessment of the individual and combined effects of Rht8 and Ppd-D1a on plant height, time to heading and yield traits in common wheat. Crop J 7(6):845–856. https://doi.org/10.1016/j.cj.2019.06.008
Zhang L, Zhang H, Qiao L, Miao L, Yan D, Liu P, Zhao G, Jia J, Gao L (2021) Wheat MADS-box gene TaSEP3-D1 negatively regulates heading date. Crop J, xxxx. https://doi.org/10.1016/j.cj.2020.12.007
Zhou H, Alexander D, Lange K (2011) A quasi-Newton acceleration for high-dimensional optimization algorithms. Stat Comput 21(2):261–273. https://doi.org/10.1007/s11222-009-9166-3
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This work was financially supported by the National Natural Science Foundation of China (32171991), the Key Research and Development Program of Shaanxi Province (2021KWZ-23), Chinese Universities Scientific Fund (2452021166), the China 111 Project (B12007), the Construction of Overseas Demonstration Zone and the Tang Chung Ying Breeding Funds (NWAFU), P. R. China.
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Y.G.H. and L.C. designed the experiment, P.F.Q and X.L performed the experiment and wrote the paper, D.Z.L., S.L. L.Z. collected the previous studies, P.F.Q., A.R analyzed the data, Y.G.H. and L.C. reviewed the paper. All authors read and approved the article.
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Qiao, P., Li, X., Liu, D. et al. Mining novel genomic regions and candidate genes of heading and flowering dates in bread wheat by SNP- and haplotype-based GWAS. Mol Breeding 43, 76 (2023). https://doi.org/10.1007/s11032-023-01422-z
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DOI: https://doi.org/10.1007/s11032-023-01422-z