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Journal of Integrative Agriculture  2023, Vol. 22 Issue (11): 3380-3393    DOI: 10.1016/j.jia.2023.02.030
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Genome-wide association and linkage mapping strategies reveal the genetic loci and candidate genes of important agronomic traits in Sichuan wheat

ZHANG Zhi-peng1, 2, 3, 5*, LI Zhen1, 2, 3*, HE Fang4*, LÜ Ji-juan4, XIE Bin4, YI Xiao-yu1, 2, 3, LI Jia-min1, 2, 3, LI Jing5, SONG Jing-han6, PU Zhi-en1, 2, MA Jian1, 3, PENG Yuan-ying1, 3, CHEN Guo-yue1, 3, WEI Yu-ming1, 3, ZHENG You-liang1, 3, LI Wei1, 2, 3#

1 State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University, Chengdu 611130, P.R.China
2 College of Agronomy, Sichuan Agricultural University, Chengdu 611130, P.R.China 
3 Triticeae Research Institute, Sichuan Agricultural University, Chengdu 611130, P.R.China
4 Sichuan Provincial Seed Station, Chengdu 610044, P.R.China
5 Huaiyin Institute of Agricultural Sciences of Xuhuai Area in Jiangsu, Huai’an 223001, P.R.China 
6 Beijing Foreign Studies University, Beijing 100081, P.R.China
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摘要  

提高小麦产量是全球小麦育种者的长期目标。发掘优良遗传资源,解析小麦重要农艺性状的遗传基础,是小麦高产育种的必经之路。本研究评价了两年七个环境中由156个育成品种77个地方品种组成的四川小麦自然群体的9个重要农艺性状表现。农艺性状调查结果表明,地方品种分蘖较多,穗粒数(KNS)较高,育品种千粒重(TKW)和穗粒重(KWS)较高。9个农艺性状的广义遗传力(H 2)在0.74到0.95之间。用来自小麦55K SNP芯片的43198个单核苷酸多态性(SNP)标记进行群体结构分析可以将自然群体分为三组。基于混合线性模型Q+K方法的全基因组关联分析(GWAS)共鉴定出67个数量性状位点(QTL)。本研究主要对三个重要性状QTL进行了分析,即分别检测到的可育分蘖数(FTN)位点QFTN.sicau-7BL.1的四种单倍型、KNS位点QKNS.sicau-1AL.2的三种单倍型和TKW位点QTKW.sicau-3BS.1的四种单倍型。从2002—2013年区域试验的42个品种的产量表现来看,FTN-Hap2KNS-Hap1TKW-Hap2分别是每个QTL中的优良单倍型。具有三个优良单倍型的品种相比具有两个或一个优良单倍型的品种产量更高。此外,基于每穗粒数的QTL位点 QKNS.sicau-1AL.2开发了连锁的KASP-AX-108866053标记能2018年至2021年区域试验中鉴定63个品种的三种单倍型(或等位基因)。这些遗传位点和连锁标记可用于标记辅助选择或基于图谱的基因克隆,用于小麦产量的遗传改良。



Abstract  

Increasing wheat yield is a long-term goal for wheat breeders around the world.  Exploiting elite genetic resources and dissecting the genetic basis of important agronomic traits in wheat are the necessary methods for high-yield wheat breeding.  This study evaluated nine crucial agronomic traits found in a natural population of 156 wheat varieties and 77 landraces from Sichuan, China in seven environments over two years.  The results of this investigation of agronomic traits showed that the landraces had more tillers and higher kernel numbers per spike (KNS), while the breeding varieties had higher thousand-kernel weight (TKW) and kernel weight per spike (KWS).  The generalized heritability (H2) values of the nine agronomic traits varied from 0.74 to 0.95.  Structure analysis suggested that the natural population could be divided into three groups using 43 198 single nucleotide polymorphism (SNP) markers from the wheat 55K SNP chip.  A total of 67 quantitative trait loci (QTLs) were identified by the genome-wide association study (GWAS) analysis based on the Q+K method of a mixed linear model.  Three important QTLs were analyzed in this study.  Four haplotypes of QFTN.sicau-7BL.1 for fertile tillers number (FTN), three haplotypes of QKNS.sicau-1AL.2 for KNS, and four haplotypes of QTKW.sicau-3BS.1 for TKW were detected.  FTN-Hap2, KNS-Hap1, and TKW-Hap2 were excellent haplotypes for each QTL based on the yield performance of 42 varieties in regional trials from 2002 to 2013.  The varieties with all three haplotypes showed the highest yield compared to those with either two haplotypes or one haplotype.  In addition, the KASP-AX-108866053 marker of QTL QKNS.sicau-1AL.2 was successfully distinguished between three haplotypes (or alleles) in 63 varieties based on the number of kernels per spike in regional trials between 2018 and 2021.  These genetic loci and reliable makers can be applied in marker-assisted selection or map-based gene cloning for the genetic improvement of wheat yield. 

Keywords:  Sichuan wheat        GWAS        yield traits        haplotype analysis        KASP  
Received: 05 November 2022   Accepted: 27 December 2022
Fund: This work was supported by the Sichuan Science and Technology Program, China (2022ZDZX0014 and 2021YFYZ0002) and the Plan of Tianfu Qingcheng of Sichuan Province, China.
About author:  #Correspondence LI Wei, Tel/Fax: +86-28-82650350, E-mail: liw03@163.com * The authors have contributed equally to this paper.

Cite this article: 

ZHANG Zhi-peng, LI Zhen, HE Fang, LÜ Ji-juan, XIE Bin, YI Xiao-yu, LI Jia-min, LI Jing, SONG Jing-han, PU Zhi-en, MA Jian, PENG Yuan-ying, CHEN Guo-yue, WEI Yu-ming, ZHENG You-liang, LI Wei. 2023. Genome-wide association and linkage mapping strategies reveal the genetic loci and candidate genes of important agronomic traits in Sichuan wheat. Journal of Integrative Agriculture, 22(11): 3380-3393.

Andersen J R, Lübberstedt T. 2003. Functional markers in plants. Trends in Plant Science8, 554–560.

Barrett J C, Fry B, Maller J, Daly M J. 2005. Haploview: Analysis and visualization of LD and haplotype maps. Bioinformatics21, 263–265.

Bradbury P J, Zhang Z, Kroon D E, Casstevens T M, Ramdoss Y, Buckler E S. 2007. TASSEL: Software for association mapping of complex traits in diverse samples. Bioinformatics23, 2633–2635.

Brinton J, Uauy C. 2019. A reductionist approach to dissecting kernel weight and yield in wheat. Journal of Integrative Plant Biology61, 337–358.

Chen H, Wei Y, Wang Z, Zheng Y. 2006. Analysis of agronomic characters of Sichuan wheat landraces. Southwest China Journal of Agricultural Sciences19, 791–795. (in Chinese)

Chen Y, Yan Y, Wu T T, Zhang G L, Yin H, Chen W, Wang S, Chang F, Gou J Y. 2020. Cloning of wheat keto-acyl thiolase 2B reveals a role of jasmonic acid in grain weight determination. Nature Communications11, 1–11.

Deng S, Wu X, Wu Y, Zhou R, Wang H, Jia J, Liu S. 2011. Characterization and precise mapping of a QTL increasing spike number with pleiotropic effects in wheat. Theoretical and Applied Genetics122, 281–289.

Ding P, Mo Z, Tang H, Yang M, Mei D, Jiang Q, Liu Y, Chen G, Chen G, Wang J. 2022. A major and stable QTL for wheat spikelet number per spike validated in different genetic backgrounds. Journal of Integrative Agriculture21, 1551–1562.

Dwivedi S L, Crouch J H, Mackill D J, Xu Y, Blair M W, Ragot M, Upadhyaya H D, Ortiz R. 2007. The molecularization of public sector crop breeding: progress, problems, and prospects. Advances in Agronomy95, 163–318.

Earl D A, VonHoldt B M. 2012. STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources4, 359–361.

Echeverry-Solarte M, Kumar A, Kianian S, Mantovani E E, McClean P E, Deckard E L, Elias E, Simsek S, Alamri M S, Hegstad J. 2015. Genome wide mapping of spike related and agronomic traits in a common wheat population derived from a supernumerary spikelet parent and an elite parent. The Plant Genome8, doi: 10.3835/plantgenome2014.12.0089.

Eltaher S, Baenziger P S, Belamkar V, Emara H A, Nower A A, Salem K F, Alqudah A M, Sallam A. 2021. GWAS revealed effect of genotype×environment interactions for kernel yield of Nebraska winter wheat. BMC Genomics22, 1–14.

Fernandes R C, Busanello C, Viana V E, Venske E, de Oliveira V F, Lopes J L, da Maia L C, de Oliveira A C, Pegoraro C. 2022. Genetic variability and heritability of agronomic traits in a wheat collection used in southern Brazil. Journal of Crop Science and Biotechnology25, 337–348.

Gao Y, Xu X, Jin J, Duan S, Zhen W, Xie C, Ma J. 2021. Dissecting the genetic basis of kernel morphology traits in Chinese wheat by genome wide association study. Euphytica217, 1–12.

Ginestet C. 2011. ggplot2: Elegant graphics for data analysis. Journal-Royal Statistical Society (Series A), 174, 245–246.

Hubisz M J, Falush D, Stephens M, Pritchard J K. 2009. Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources9, 1322–1332.

Jaradat A A. 2011. Wheat landraces: Genetic resources for sustenance and sustainability. USDA-ARS, Morris, Minnesota, USA. [2022-03-17]. https://www.ars.usda.gov/ARSUserFiles/50600000/products-wheat/AAJ-Wheat% 20Landraces.pdf

Ji G S, Xu Z B, Fan X L, Zhou Q, Yu Q, Liu X F, Liao S M, Feng B, Wang T. 2021. Identification of a major and stable QTL on chromosome 5A confers spike length in wheat (Triticum aestivum L.). Molecular Breeding41, 1–13.

Kabir M R, Nonhebel H M. 2021. Reinvestigation of thousand kernel WEIGHT 6 kernel weight genes in wheat and rice indicates a role in pollen development rather than regulation of auxin content in kernels. Theoretical and Applied Genetics134, 2051–2062.

Kuzay S, Lin H, Li C, Chen S, Woods D P, Zhang J, Lan T, von Korff M, Dubcovsky J. 2022. WAPO-A1 is the causal gene of the 7AL QTL for spikelet number per spike in wheat. PLoS Genetics18, e1009747.

Liu D, Zhang X, Wu Q, Liu S, Zeng Q, Wang Q, Wang C, Li C, Singh R P, Bhavani S. 2022. Combined linkage and association mapping reveals two major QTL for stripe rust adult plant resistance in Shaanmai 155 and their haplotype variation in common wheat germplasm. The Crop Journal10, 783–792.

Liu K. 2005. PowerMarker: Integrated analysis environment for genetic marker data. Bioinformatics21, 2128–2129.

Liu Y, Lin Y, Gao S, Li Z, Ma J, Deng M, Chen G, Wei Y, Zheng Y. 2017. A genome-wide association study of 23 agronomic traits in Chinese wheat landraces. The Plant Journal91, 861–873.

Luo M, Yen C, Yang J. 1992. Crossability percentages of bread wheat landraces from Sichuan Province, China with rye. Euphytica61, 1–7.

Ma J, Zhang C, Yan G, Liu C. 2012. Identification of QTLs conferring agronomic and quality traits in hexaploid wheat. Journal of Integrative Agriculture11, 1399–1408.

Ma J, Zhang H, Li S, Zou Y, Li T, Liu J, Ding P, Mu Y, Tang H, Deng M. 2019. Identification of quantitative trait loci for kernel traits in a wheat cultivar Chuannong 16. BMC Genetics20, 1–12.

Ma L, Li T, Hao C, Wang Y, Chen X, Zhang X. 2016. Ta GS 5-3A, a kernel size gene selected during wheat improvement for larger kernel and yield. Plant Biotechnology Journal14, 1269–1280.

Murray M G, Thompson W F. 1980. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research8, 4321–4325.

Nyine M, Adhikari E, Clinesmith M, Aiken R, Betzen B, Wang W, Davidson D, Yu Z, Guo Y, He F. 2021. The haplotype-based analysis of Aegilops tauschii introgression into hard red winter wheat and its impact on productivity traits. Frontiers in Plant Science12, 716955.

Pandey R, Dhoundiyal M, Kumar A. 2015. Correlation analysis of big data to support machine learning. In: 2015 Fifth International Conference on Communication Systems and Network Technologies. IEEE, India. pp. 996–999.

Philipp N, Weichert H, Bohra U, Weschke W, Schulthess A W, Weber H. 2018. kernel number and kernel yield distribution along the spike remain stable despite breeding for high yield in winter wheat. PLoS ONE13, e0205452.

Qu X, Liu J, Xie X, Xu Q, Tang H, Mu Y, Pu Z, Li Y, Ma J, Gao Y. 2021. Genetic mapping and validation of loci for kernel-related traits in wheat (Triticum aestivum L.). Frontiers in Plant Science12, 667493.

Salsman E, Liu Y, Hosseinirad S A, Kumar A, Manthey F, Elias E, Li X. 2021. Assessment of genetic diversity and agronomic traits of durum wheat germplasm under drought environment of the northern Great Plains. Crop Science61, 1194–1206.

Scott M F, Fradgley N, Bentley A R, Brabbs T, Corke F, Gardner K A, Horsnell R, Howell P, Ladejobi O, Mackay I J. 2021. Limited haplotype diversity underlies polygenic trait architecture across 70 years of wheat breeding. Genome Biology22, 1–30.

Slafer G A, Savin R, Sadras V O. 2014. Coarse and fine regulation of wheat yield components in response to genotype and environment. Field Crops Research157, 71–83.

Smith S, Kuehl R, Ray I, Hui R, Soleri D. 1998. Evaluation of simple methods for estimating broad-sense heritability in stands of randomly planted genotypes. Crop Science38, 1125–1129.

Sthapit S R, Ruff T M, Hooker M A, See D R. 2022. Population structure and genetic diversity of US wheat varieties. The Plant Genome15, e20196.

Vikhe P, Venkatesan S, Chavan A, Tamhankar S, Patil R. 2019. Mapping of dwarfing gene Rht14 in durum wheat and its effect on seedling vigor, internode length and plant height. The Crop Journal7, 187–197.

Walkowiak S, Gao L, Monat C, Haberer G, Kassa M T, Brinton J, Ramirez-Gonzalez R H, Kolodziej M C, Delorean E, Thambugala D. 2020. Multiple wheat genomes reveal global variation in modern breeding. Nature588, 277–283.

Wang D, Yu K, Jin D, Sun L, Chu J, Wu W, Xin P, Gregová E, Li X, Sun J. 2020. Natural variations in the promoter of Awn Length Inhibitor 1 (ALI-1) are associated with awn elongation and kernel length in common wheat. The Plant Journal101, 1075–1090.

Wang S, Yan X, Wang Y, Liu H, Cui D, Chen F. 2016. Haplotypes of the TaGS5-A1 gene are associated with thousand kernel weight in Chinese bread wheat. Frontiers in Plant Science7, 783.

Wang W, Pan Q, Tian B, He F, Chen Y, Bai G, Akhunova A, Trick H N, Akhunov E. 2019. Gene editing of the wheat homologs of TONNEAU1-recruiting motif encoding gene affects kernel shape and weight in wheat. Plant Journal100, 251–264.

Wang Y, Hao C, Zheng J, Ge H, Zhou Y, Ma Z, Zhang X. 2015. A haplotype block associated with thousand-kernel weight on chromosome 5DS in common wheat (Triticum aestivum L.). Journal of Integrative Plant Biology57, 662–672.

White J, Law J, MacKay I, Chalmers K, Smith J, Kilian A, Powell W. 2008. The genetic diversity of UK, US and Australian cultivars of Triticum aestivum measured by DArT markers and considered by genome. Theoretical and Applied Genetics116, 439–453.

Wu B B, Shi M M, Pourkheirandish M, Qi Z, Ying W, Yang C K, Ling Q, Zhao J J, Yan S X, Zheng X W. 2022. Allele mining of wheat ABA receptor at TaPYL4 suggests neo-functionalization among the wheat homoeologs. Journal of Integrative Agriculture21, 2183–2196.

Xie Q, Li N, Yang Y, Lv Y, Yao H, Wei R, Sparkes D L, Ma Z. 2018. Pleiotropic effects of the wheat domestication gene Q on yield and kernel morphology. Planta247, 1089–1098.

Xin F, Zhu T, Wei S, Han Y, Zhao Y, Zhang D, Ma L, Ding Q. 2020. QTL mapping of kernel traits and validation of a major QTL for kernel length–width ratio using SNP and bulked segregant analysis in wheat. Scientific Reports10, 25.

Xu H, Sun H, Dong J, Ma C, Li J, Li Z, Wang Y, Ji J, Hu X, Wu M. 2022. The brassinosteroid biosynthesis gene TaD11-2A controls kernel size and its elite haplotype improves wheat kernel yields. Theoretical and Applied Genetics135, 2907–2923.

Xu T, Bian N, Wen M, Xiao J, Yuan C, Cao A, Zhang S, Wang X, Wang H. 2017. Characterization of a common wheat (Triticum aestivum L.) high-tillering dwarf mutant. Theoretical and Applied Genetics130, 483–494.

Yang Y, Dhakal S, Chu C, Wang S, Xue Q, Rudd J C, Ibrahim A M, Jessup K, Baker J, Fuentealba M P. 2020. Genome wide identification of QTL associated with yield and yield components in two popular wheat breeding TAM 111 and TAM 112. PLoS ONE15, e0237293.

Ye X, Li J, Cheng Y, Yao F, Long L, Wang Y, Wu Y, Li J, Wang J, Jiang Q. 2019. Genome-wide association study reveals new loci for yield-related traits in Sichuan wheat germplasm under stripe rust stress. BMC Genomics20, 1–17.

Yu S, Wu J, Wang M, Shi W, Xia G, Jia J, Kang Z, Han D. 2020. Haplotype variations in QTL for salt tolerance in Chinese wheat accessions identified by marker-based and pedigree-based kinship analyses. The Crop Journal8, 1011–1024.

Yuan Y, Scheben A, Edwards D, Chan T F. 2021. Toward haplotype studies in polyploid plants to assist breeding. Molecular Plant14, 1969–1972.

Zhai H, Feng Z, Du X, Song Y, Liu X, Qi Z, Song L, Li J, Li L, Peng H. 2018. A novel allele of TaGW2-A1 is located in a finely mapped QTL that increases kernel weight but decreases kernel number in wheat (Triticum aestivum L.). Theoretical and Applied Genetics131, 539–553.

Zhang C, Dong S S, Xu J Y, He W M, Yang T L. 2019. PopLDdecay: A fast and effective tool for linkage disequilibrium decay analysis based on variant call format files. Bioinformatics35, 1786–1788.

Zhang J, Gizaw S A, Bossolini E, Hegarty J, Howell T, Carter A H, Akhunov E, Dubcovsky J. 2018. Identification and validation of QTL for kernel yield and plant water status under contrasting water treatments in fall-sown spring wheats. Theoretical and Applied Genetics131, 1741–1759.

Zhang X, Jia H, Li T, Wu J, Nagarajan R, Lei L, Powers C, Kan C C, Hua W, Liu Z. 2022. TaCol-B5 modifies spike architecture and enhances grain yield in wheat. Science376, 180–183.

Zhang Y, Li D, Zhang D, Zhao X, Cao X, Dong L, Liu J, Chen K, Zhang H, Gao C. 2018. Analysis of the functions of TaGW2 homoeologs in wheat kernel weight and protein content traits. The Plant Journal94, 857–866.

Zhang Z, Ersoz E, Lai C Q, Todhunter R J, Tiwari H K, Gore M A, Bradbury P J, Yu J, Arnett D K, Ordovas J M. 2010.Mixed linear model approach adapted for genome-wide association studies. Nature Genetics42, 355–360.

Zhao B, Wu T T, Ma S S, Jiang D J, Bie X M, Sui N, Zhang X S, Wang F. 2020. TaD27-B gene controls the tiller number in hexaploid wheat. Plant Biotechnology Journal18, 513–525.

Zhao L, Zheng Y, Wang Y, Wang S, Wang T, Wang C, Chen Y, Zhang K, Zhang N, Dong Z. 2022. A HST1-like gene controls tiller angle through regulating endogenous auxin in common wheat. Plant Biotechnology Journal21, 122–135.

Zhou C Y, Xiong H C, Li Y T, Guo H J, Xie Y D, Zhao L S, Gu J Y, Zhao S R, Ding Y P, Song X Y, Liu L X. 2020. Genetic analysis and QTL mapping of a novel reduced height gene in common wheat (Triticum aestivum L.). Journal of Integrative Agriculture19, 1721–1730.

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