Skip to main content
SpringerLink
Log in

Genome-wide association mapping for agronomic traits in an 8-way Upland cotton MAGIC population by SLAF-seq

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

One sub-MAGIC population was genotyped using SLAF-seq, and QTLs and candidate genes for agronomic traits were identified in Upland cotton.

Abstract

The agronomic traits of Upland cotton have serious impacts on cotton production, as well as economic benefits. To discover the genetic basis of important agronomic traits in Upland cotton, a subset MAGIC (multi-parent advanced generation inter-cross) population containing 372 lines (SMLs) was selected from an 8-way MAGIC population with 960 lines. The 372 lines and 8 parents were phenotyped in six environments and deeply genotyped by SLAF-seq with 60,495 polymorphic SNPs. The genetic diversity indexes of all SNPs were 0.324 and 0.362 for the parents and MAGIC lines, respectively. The LD decay distance of the SMLs was 600 kb (r2 = 0.1). Genome-wide association mapping was performed using 60,495 SNPs and the phenotypic data of the SMLs, and 177 SNPs were identified to be significantly associated with 9 stable agronomic traits in multiple environments. The identified SNPs were divided into 117 QTLs (quantitative trait loci) by LD decay distance, explaining 5.44% to 31.64% of the phenotypic variation. Among the 117 QTLs, 3 QTLs were stable in multiple environments, and 11 QTL regions were proven to have pleiotropism associated with multiple traits. Within QTL regions, 154 genes were preferentially expressed in correlated tissues, and 8 genes with known functions were identified as priori candidate genes. Two genes, GhACT1 and GhGASL3, reported to have clear functions, were, respectively, located in qFE-A05-4 and qFE-D04-3, two stable QTLs for FE. This study revealed the genetic basis of important agronomic traits of Upland cotton, and the results will facilitate molecular breeding in cotton.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abdurakhmonov IY, Kohel RJ, Yu JZ, Pepper AE, Abdullaev AA, Kushanov FN, Salakhutdinov IB, Buriev ZT, Saha S, Scheffler BE, Jenkins JN, Abdukarimov A (2008) Molecular diversity and association mapping of fiber quality traits in exotic G. hirsutum L. germplasm. Genomics 92:478–487

    Article  CAS  PubMed  Google Scholar 

  • Abdurakhmonov IY, Saha S, Jenkins JN, Buriev ZT, Shermatov SE, Scheffler BE, Pepper AE, Yu JZ, Kohel RJ, Abdukarimov A (2009) Linkage disequilibrium based association mapping of fiber quality traits in G. hirsutum L. variety germplasm. Genetica 136:401–417

    Article  PubMed  Google Scholar 

  • Abdurakhmonov IY, Buriev ZT, Saha S, Jenkins JN, Abdukarimov A, Pepper AE (2014) Phytochrome RNAi enhances major fibre quality and agronomic traits of the cotton Gossypium hirsutum L. Nature commun 5:3062

    Article  CAS  Google Scholar 

  • Argiriou A, Kalivas A, Michailidis G, Tsaftaris A (2012) Characterization of PROFILIN genes from allotetraploid (Gossypium hirsutum) cotton and its diploid progenitors and expression analysis in cotton genotypes differing in fiber characteristics. Mol Biol Rep 39:3523–3532

    Article  CAS  PubMed  Google Scholar 

  • Bai WQ, Xiao YH, Zhao J, Song SQ, Hu L, Zeng JY, Li XB, Hou L, Luo M, Li DM, Pei Y (2014) Gibberellin overproduction promotes sucrose synthase expression and secondary cell wall deposition in cotton fibers. PLoS ONE 9:e96537

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Cai C, Ye W, Zhang T, Guo W (2014) Association analysis of fiber quality traits and exploration of elite alleles in Upland cotton cultivars/accessions (Gossypium hirsutum L.). J Integr Plant Biol 56:51–62

    Article  CAS  PubMed  Google Scholar 

  • Chen ZJ, Scheffler BE, Dennis E, Triplett BA, Zhang T, Guo W, Chen X, Stelly DM, Rabinowicz PD, Town CD, Arioli T, Brubaker C, Cantrell RG, Lacape JM, Ulloa M, Chee P, Gingle AR, Haigler CH, Percy R, Saha S, Wilkins T, Wright RJ, Van Deynze A, Zhu Y, Yu S, Abdurakhmonov I, Katageri I, Kumar PA, Mehboob Ur R, Zafar Y, Yu JZ, Kohel RJ, Wendel JF, Paterson AH (2007) Toward sequencing cotton (Gossypium) genomes. Plant Physiol 145:1303–1310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet 12:499–510

    Article  CAS  PubMed  Google Scholar 

  • Fang X, Liu X, Wang X, Wang W, Liu D, Zhang J, Liu D, Teng Z, Tan Z, Liu F, Zhang F, Jiang M, Jia X, Zhong J, Yang J, Zhang Z (2017) Fine-mapping qFS07.1 controlling fiber strength in upland cotton (Gossypium hirsutum L.). Theor Appl Genet 130:795–806

    Article  CAS  PubMed  Google Scholar 

  • Flint-Garcia SA, Thornsberry JM, Buckler ESt, (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374

    Article  CAS  PubMed  Google Scholar 

  • Frankham R (1996) Introduction to quantitative genetics edition. Trends Genet. 12(7), 280

  • Handi SS, Katageri IS, Adiger S, Jadhav MP, Lekkala SP, Reddy Lachagari VB, Jenkins J (2017) Association mapping for seed cotton yield, yield components and fibre quality traits in upland cotton (Gossypium hirsutum L.) genotypes. Plant Breed 136:958–968

    Article  CAS  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGEDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  CAS  Google Scholar 

  • Huang X, Zhao Y, Wei X, Li C, Wang A, Zhao Q, Li W, Guo Y, Deng L, Zhu C, Fan D, Lu Y, Weng Q, Liu K, Zhou T, Jing Y, Si L, Dong G, Huang T, Lu T, Feng Q, Qian Q, Li J, Han B (2012) Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat Genet 44:32–39

    Article  CAS  Google Scholar 

  • Huang BE, Verbyla KL, Verbyla AP, Raghavan C, Singh VK, Gaur P, Leung H, Varshney RK, Cavanagh CR (2015) MAGIC populations in crops: current status and future prospects. Theor Appl Genet 128:999–1017

    Article  PubMed  Google Scholar 

  • Huang C, Nie X, Shen C, You C, Li W, Zhao W, Zhang X, Lin Z (2017) Population structure and genetic basis of the agronomic traits of upland cotton in China revealed by a genome-wide association study using high-density SNPs. Plant Biotechnol J 15:1374–1386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang C, Shen C, Wen T, Gao B, Zhu D, Li X, Ahmed MM, Li D, Lin Z (2018) SSR-based association mapping of fiber quality in upland cotton using an 8-way MAGIC population. Mol Genet Genom 293:793–805

    Article  CAS  Google Scholar 

  • Huang C, Li X, Li D, Lin Z (2018) QTL mapping for yield, growth period and plant height traits in upland cotton using MAGIC population. Acta Agron Sin 44(9):1320–1333

    Article  Google Scholar 

  • Islam MS, Thyssen GN, Jenkins JN, Zeng L, Delhom CD, McCarty JC, Deng DD, Hinchliffe DJ, Jones DC, Fang DD (2016) A MAGIC population-based genome-wide association study reveals functional association of GhRBB1_A07 gene with superior fiber quality in cotton. BMC Genom 17:903

    Article  CAS  Google Scholar 

  • Joukhadar R, Hollaway G, Shi F, Kant S, Forrest K, Wong D, Petkowski J, Pasam R, Tibbits J, Bariana H, Bansal U, Spangenberg G, Daetwyler H, Gendall T, Hayden M (2020) Genome-wide association reveals a complex architecture for rust resistance in 2300 worldwide bread wheat accessions screened under various Australian conditions. Theor Appl Genet 133:2695–2712

    Article  CAS  PubMed  Google Scholar 

  • Letunic I, Bork P (2016) Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 44:W242-245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li XB, Fan XP, Wang XL, Cai L, Yang WC (2005) The cotton ACTIN1 gene is functionally expressed in fibers and participates in fiber elongation. Plant Cell 17:859–875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Jin X, Wang H, Zhang X, Lin Z (2016) Structure, evolution, and comparative genomics of tetraploid cotton based on a high-density genetic linkage map. DNA Res 3:283–293

    Article  CAS  Google Scholar 

  • Liu K, Muse SV (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21:2128–2129

    Article  CAS  PubMed  Google Scholar 

  • Liu ZH, Zhu L, Shi HY, Chen Y, Zhang JM, Zheng Y, Li XB (2013) Cotton GASL genes encoding putative gibberellin-regulated proteins are involved in response to GA signaling in fiber development. Mol Biol Rep 40:4561–4570

    Article  CAS  PubMed  Google Scholar 

  • Machado A, Wu Y, Yang Y, Llewellyn DJ, Dennis ES (2009) The MYB transcription factor GhMYB25 regulates early fibre and trichome development. Plant J 59:52–62

    Article  CAS  PubMed  Google Scholar 

  • Mackay I, Powell W (2007) Methods for linkage disequilibrium mapping in crops. Trends Plant Sci 12:57–63

    Article  CAS  PubMed  Google Scholar 

  • Naoumkina M, Thyssen GN, Fang DD, Jenkins JN, Mccarty JC, Florane CB (2019) Genetic and transcriptomic dissection of the fiber length trait from a cotton (Gossypium hirsutum L.) MAGIC population. BMC Genom 20(1):119

    Article  Google Scholar 

  • Nie X, Huang C, You C, Li W, Zhao W, Shen C, Zhang B, Wang H, Yan Z, Dai B, Wang M, Zhang X, Lin Z (2016) Genome-wide SSR-based association mapping for fiber quality in nation-wide upland cotton inbreed cultivars in China. BMC Genom 17:352

    Article  CAS  Google Scholar 

  • Qin H, Chen M, Yi X, Bie S, Zhang C, Zhang Y, Lan J, Meng Y, Yuan Y, Jiao C (2015) Identification of associated SSR markers for yield component and fiber quality traits based on frame map and Upland cotton collections. PLoS ONE 10:e0118073

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Su J, Pang C, Wei H, Li L, Liang B, Wang C, Song M, Wang H, Zhao S, Jia X, Mao G, Huang L, Geng D, Wang C, Fan S, Yu S (2016) Identification of favorable SNP alleles and candidate genes for traits related to early maturity via GWAS in upland cotton. BMC Genom 17:687

    Article  CAS  Google Scholar 

  • Su J, Li L, Pang C, Wei H, Wang C, Song M, Wang H, Zhao S, Zhang C, Mao G, Huang L, Wang C, Fan S, Yu S (2016) Two genomic regions associated with fiber quality traits in Chinese upland cotton under apparent breeding selection. Sci Rep 6:38496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Su J, Fan S, Li L, Wei H, Wang C, Wang H, Song M, Zhang C, Gu L, Zhao S, Mao G, Wang C, Pang C, Yu S (2016) Detection of favorable QTL alleles and candidate genes for lint percentage by GWAS in Chinese Upland Cotton. Front Plant Sci 7:1576

    PubMed  PubMed Central  Google Scholar 

  • Su X, Zhu G, Song X, Xu H, Li W, Ning X, Chen Q, Guo W (2020) Genome-wide association analysis reveals loci and candidate genes involved in fiber quality traits in sea island cotton (Gossypium barbadense). BMC Plant Biol 20:289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun X, Liu D, Zhang X, Li W, Liu H, Hong W, Jiang C, Guan N, Ma C, Zeng H, Xu C, Song J, Huang L, Wang C, Shi J, Wang R, Zheng X, Lu CY, Wang X, Zheng H (2013) SLAF-seq: An efficient method of large-scale de novo SNP discovery and genotyping using high-throughput sequencing. PLoS ONE 8:e58700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun Z, Wang X, Liu Z, Gu Q, Zhan Y, Li Z, Ke H, Yang J, Wu J, Wu L, Zhang G, Zhang C, Ma Z (2017) Genome-wide association study discovered genetic variation and candidate genes of fibre quality traits in Gossypium hirsutum L. Plant Biotech J 15:982–996

    Article  CAS  Google Scholar 

  • Tang W, Tu L, Yang X, Tan J, Deng F, Hao J, Guo K, Lindsey K, Zhang X (2014) The calcium sensor GhCaM7 promotes cotton fiber elongation by modulating reactive oxygen species (ROS) production. New Phytol 202:509–520

    Article  CAS  PubMed  Google Scholar 

  • Wang M, Yan J, Zhao J, Song W, Zhang X, Xiao Y, Zheng Y (2012) Genome-wide association study (GWAS) of resistance to head smut in maize. Plant Sci 196:125–131

    Article  CAS  PubMed  Google Scholar 

  • Wang M, Tu L, Lin M, Lin Z, Wang P, Yang Q, Ye Z, Shen C, Li J, Zhang L, Zhou X, Nie X, Li Z, Guo K, Ma Y, Huang C, Jin S, Zhu L, Yang X, Min L, Yuan D, Zhang Q, Lindsey K, Zhang X (2017) Asymmetric subgenome selection and cis-regulatory divergence during cotton domestication. Nat Genet 49:579–587

    Article  CAS  PubMed  Google Scholar 

  • Wang M, Tu L, Yuan D, Zhu D, Shen C, Li J, Liu F, Pei L, Wang P, Zhao G, Ye Z, Huang H, Yan F, Ma Y, Zhang L, Liu M, You J, Yang Y, Liu Z, Huang F, Li B, Qiu P, Zhang Q, Zhu L, Jin S, Yang X, Min L, Li G, Chen LL, Zheng H, Lindsey K, Lin Z, Udall JA, Zhang X (2019) Reference genome sequences of two cultivated allotetraploid cottons, Gossypium hirsutum and Gossypium barbadense. Nat Genet 51:224–229

    Article  CAS  PubMed  Google Scholar 

  • Wen T, Wu M, Shen C, Gao B, Zhu ZX, You C, Lin Z (2018) Linkage and association mapping reveals the genetic basis of brown fibre (Gossypium hirsutum). Plant Biotech J 16:1654–1666

    Article  CAS  Google Scholar 

  • Wendel JF, Grover CE (2015) Taxonomy and evolution of the cotton genus. John Wiley & Sons Ltd, Gossypium Cotton

    Google Scholar 

  • Wubben M, Thyssen G, Callahan F, Fang D, Jenkins J (2019) A novel variant of Gh_D02G0276 is required for root-knot nematode resistance on chromosome 14 (D02) in Upland cotton. Theor Appl Genet 132:1425–1434

    Article  CAS  PubMed  Google Scholar 

  • Xiao Y, Tong H, Yang X, Xu S, Pan Q, Qiao F, Raihan MS, Luo Y, Liu H, Zhang X, Yang N, Wang X, Deng M, Jin M, Zhao L, Luo X, Zhou Y, Li X, Liu J, Zhan W, Liu N, Wang H, Chen G, Cai Y, Xu G, Wang W, Zheng D, Yan J (2016) Genome-wide dissection of the maize ear genetic architecture using multiple populations. New Phytol 210:1095–1106

    Article  CAS  PubMed  Google Scholar 

  • Xiao Y, Liu H, Wu L, Warburton M, Yan J (2017) Genome-wide association studies in maize: praise and stargaze. Mol Plant 10:359–374

    Article  CAS  PubMed  Google Scholar 

  • Xu L, Hu K, Zhang Z, Guan C, Chen S, Hua W, Li J, Wen J, Yi B, Shen J, Ma C, Tu J, Fu T (2016) Genome-wide association study reveals the genetic architecture of flowering time in rapeseed (Brassica napus L.). DNA Res 23:43–52

    CAS  PubMed  Google Scholar 

  • Zhang HB, Li Y, Wang B, Chee PW (2008) Recent advances in cotton genomics. Int J Plant Sci 2008:742304

    Google Scholar 

  • Zhang N, Gibon Y, Wallace JG, Lepak N, Li P, Dedow L, Chen C, So YS, Kremling K, Bradbury PJ, Brutnell T, Stitt M, Buckler ES (2015) Genome-wide association of carbon and nitrogen metabolism in the maize nested association mapping population. Plant Physiol 168:575–583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Shang H, Shi Y, Huang L, Li J, Ge Q, Gong J, Liu A, Chen T, Wang D, Wang Y, Palanga KK, Muhammad J, Li W, Lu Q, Deng X, Tan Y, Song W, Cai J, Li P, Rashid HO, Gong W, Yuan Y (2016) Construction of a high-density genetic map by specific locus amplified fragment sequencing (SLAF-seq) and its application to quantitative trait loci (QTL) analysis for boll weight in upland cotton (Gossypium hirsutum.). BMC Plant biol 16(1):79

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao Y, Wang H, Chen W, Li Y, Gong H, Sang X, Huo F, Zeng F (2014) Genetic diversity and population structure of elite cotton (Gossypium hirsutum L.) germplasm revealed by SSR markers. Plant Syst Evol 301:327–336

    Article  Google Scholar 

  • Zhou Y, Li B, Li M, Li X, Zhang Z, Li Y, Li X (2013) A MADS-box gene is specifically expressed in fibers of cotton (Gossypium hirsutum) and influences plant growth of transgenic Arabidopsis in a GA-dependent manner. Plant Physiol Bioch 75:70–79

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (Grant No. 31371674). We thank the high-performance computing center at the National Key Laboratory of Crop Genetic Improvement at Huazhong Agricultural University.

Author information

Authors and Affiliations

  1. National Key Laboratory of Crop Genetic Improvement, College of Plant Sciences & Technology, Huazhong Agricultural University, Wuhan, 430070, Hubei, China

    Cong Huang, Chao Shen, Tianwang Wen, Bin Gao, De Zhu & Zhongxu Lin

  2. Institute of Crop Genetic and Breeding, Yangtze University, Jingzhou, 434025, Hubei, China

    Dingguo Li

Authors
  1. Cong Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chao Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tianwang Wen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bin Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. De Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dingguo Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhongxu Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Zhongxu Lin conceived and designed the project. Cong Huang performed the experiment and wrote the manuscript. Dingguo Li developed the MAGIC population. Tianwang Wen, De Zhu and Bing Gao carried out field experiments and investigated the phenotypic traits. Chao Shen helped with data analysis. Zhongxu Lin revised the manuscript.

Corresponding authors

Correspondence to Dingguo Li or Zhongxu Lin.

Ethics declarations

Conflict of interest

On behalf of all authors, the corresponding author states that there are no conflicts of interest.

Ethical standards

The authors state that all experiments in the study comply with the ethical standards.

Additional information

Communicated by Emma Mace.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, C., Shen, C., Wen, T. et al. Genome-wide association mapping for agronomic traits in an 8-way Upland cotton MAGIC population by SLAF-seq. Theor Appl Genet 134, 2459–2468 (2021). https://doi.org/10.1007/s00122-021-03835-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-021-03835-w

Search

Navigation