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A genome-wide association study uncovers novel genomic regions and candidate genes of yield-related traits in upland cotton

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A total of 62 SNPs associated with yield-related traits were identified by a GWAS. Based on significant SNPs, two candidate genes pleiotropically increase lint yield.

Abstract

Improved fibre yield is considered a constant goal of upland cotton (Gossypium hirsutum) breeding worldwide, but the understanding of the genetic basis controlling yield-related traits remains limited. To better decipher the molecular mechanism underlying these traits, we conducted a genome-wide association study to determine candidate loci associated with six yield-related traits in a population of 719 upland cotton germplasm accessions; to accomplish this, we used 10,511 single-nucleotide polymorphisms (SNPs) genotyped by an Illumina CottonSNP63K array. Six traits, including the boll number, boll weight, lint percentage, fruit branch number, seed index and lint index, were assessed in multiple environments; large variation in all phenotypes was detected across accessions. We identified 62 SNP loci that were significantly associated with different traits on chromosomes A07, D03, D05, D09, D10 and D12. A total of 689 candidate genes were screened, and 27 of them contained at least one significant SNP. Furthermore, two genes (Gh_D03G1064 and Gh_D12G2354) that pleiotropically increase lint yield were identified. These identified SNPs and candidate genes provide important insights into the genetic control underlying high yields in G. hirsutum, ultimately facilitating breeding programmes of high-yielding cotton.

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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  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  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  Google Scholar 

  • An C, Jenkins JN, Wu J, Guo Y, McCarty JC (2009) Use of fiber and fuzz mutants to detect QTL for yield components, seed, and fiber traits of upland cotton. Euphytica 172:21–34

    Article  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  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  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • George AW, Cavanagh C (2015) Genome-wide association mapping in plants. Theor Appl Genet 128:1163–1174

    Article  CAS  Google Scholar 

  • Geraldo N, Baurle I, Kidou S, Hu X, Dean C (2009) FRIGIDA delays flowering in Arabidopsis via a cotranscriptional mechanism involving direct interaction with the nuclear cap-binding complex. Plant Physiol 150:1611–1618

    Article  CAS  Google Scholar 

  • Gore MA, Fang DD, Poland JA, Zhang J, Percy RG, Cantrell RG, Thyssen G, Lipka AE (2014) Linkage map construction and quantitative trait locus analysis of agronomic and fiber quality traits in cotton. Plant Genome 7:1–10

    Article  Google Scholar 

  • Han Y, Zhao X, Liu D, Li Y, Lightfoot DA, Yang Z, Zhao L, Zhou G, Wang Z, Huang L, Zhang Z, Qiu L, Zheng H, Li W (2015) Domestication footprints anchor genomic regions of agronomic importance in soybeans. New Phytol 209:871

    Article  Google Scholar 

  • Heo JB, Rho HS, Kim SW, Hwang SM, Kwon HJ, Nahm MY, Bang WY, Bahk JD (2005) OsGAP1 functions as a positive regulator of OsRab11-mediated TGN to PM or vacuole trafficking. Plant Cell Physiol 46:2005–2018

    Article  CAS  Google Scholar 

  • Huang X, Han B (2014) Natural variations and genome-wide association studies in crop plants. Annu Rev Plant Biol 65:531–551

    Article  CAS  Google Scholar 

  • Huang X, Yang S, Gong J, Zhao Q, Feng Q, Zhan Q, Zhao Y, Li W, Cheng B, Xia J, Chen N, Huang T, Zhang L, Fan D, Chen J, Zhou C, Lu Y, Weng Q, Han B (2016) Genomic architecture of heterosis for yield traits in rice. Nature 537:629–633

    Article  CAS  Google Scholar 

  • Hulse-Kemp AM, Lemm J, Plieske J, Ashrafi H, Buyyarapu R, Fang DD, Frelichowski J, Giband M, Hague S, Hinze LL, Kochan KJ, Riggs PK, Scheffler JA, Udall JA, Ulloa M, Wang SS, Zhu QH, Bag SK, Bhardwaj A, Burke JJ, Byers RL, Claverie M, Gore MA, Harker DB, Islam MS, Jenkins JN, Jones DC, Lacape JM, Llewellyn DJ, Percy RG, Pepper AE, Poland JA, Mohan Rai K, Sawant SV, Singh SK, Spriggs A, Taylor JM, Wang F, Yourstone SM, Zheng X, Lawley CT, Ganal MW, Van Deynze A, Wilson IW, Stelly DM (2015) Development of a 63K SNP array for cotton and high-density mapping of intraspecific and interspecific populations of Gossypium spp. G3 (Bethesda) 5:1187–1209

    Article  Google Scholar 

  • Ingvarsson PK, Street NR (2011) Association genetics of complex traits in plants. New Phytol 189:909–922

    Article  Google Scholar 

  • Jia Y, Sun J, Wang X, Zhou Z, Pan Z, He S, Pang B, Wang L, Du X (2014a) Molecular diversity and association analysis of drought and salt tolerance in Gossypium hirsutum L. Germplasm. J Integr Agric 13:1845–1853

    Article  CAS  Google Scholar 

  • Jia Y, Sun X, Sun J, Pan Z, Wang X, He S, Xiao S, Shi W, Zhou Z, Pang B, Wang L, Liu J, Ma J, Du X, Zhu J (2014b) Association mapping for epistasis and environmental interaction of yield traits in 323 cotton cultivars under 9 different environments. PLoS ONE 9:e95882

    Article  Google Scholar 

  • Johanson U (2000) Molecular analysis of FRIGIDA, a major determinant of natural variation in arabidopsis flowering time. Science 290:344–347

    Article  CAS  Google Scholar 

  • Korte A, Farlow A (2013) The advantages and limitations of trait analysis with GWAS: a review. Plant Methods 9:29

    Article  CAS  Google Scholar 

  • Liu R, Wang B, Guo W, Qin Y, Wang L, Zhang Y, Zhang T (2012) Quantitative trait loci mapping for yield and its components by using two immortalized populations of a heterotic hybrid in Gossypium hirsutum L. Mol Breed 29:297–311

    Article  CAS  Google Scholar 

  • Mengistu DK, Kidane YG, Catellani M, Frascaroli E, Fadda C, Pe ME, Dell’Acqua M (2016) High-density molecular characterization and association mapping in Ethiopian durum wheat landraces reveals high diversity and potential for wheat breeding. Plant Biotechnol J 14:1800–1812

    Article  CAS  Google Scholar 

  • Meyer RS, Choi JY, Sanches M, Plessis A, Flowers JM, Amas J, Dorph K, Barretto A, Gross B, Fuller DQ, Bimpong IK, Ndjiondjop MN, Hazzouri KM, Gregorio GB, Purugganan MD (2016) Domestication history and geographical adaptation inferred from a SNP map of African rice. Nat Genet 48:1083–1088

    Article  CAS  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  Google Scholar 

  • Park MY, Kim SY (2014) The Arabidopsis J protein AtJ1 is essential for seedling growth, flowering time control and ABA response. Plant Cell Physiol 55:2152–2163

    Article  CAS  Google Scholar 

  • Paterson AH, Saranga Y, Menz M, Jiang CX, Wright RJ (2003) QTL analysis of genotype x environment interactions affecting cotton fiber quality. Theor Appl Genet 106:384–396

    Article  CAS  Google Scholar 

  • Qin H, Guo W, Zhang YM, Zhang T (2008) QTL mapping of yield and fiber traits based on a four-way cross population in Gossypium hirsutum L. Theor Appl Genet 117:883–894

    Article  Google Scholar 

  • Raman H, Raman R, Coombes N, Song J, Prangnell R, Bandaranayake C, Tahira R, Sundaramoorthi V, Killian A, Meng J, Dennis ES, Balasubramanian S (2015) Genome-wide association analyses reveal complex genetic architecture underlying natural variation for flowering time in canola. Plant Cell Environ 39:1228

    Article  Google Scholar 

  • Rothnie A, Clarke AR, Kuzmic P, Cameron A, Smith CJ (2011) A sequential mechanism for clathrin cage disassembly by 70-kDa heat-shock cognate protein (Hsc70) and auxilin. Proc Natl Acad Sci USA 108:6927–6932

    Article  CAS  Google Scholar 

  • Said JI, Song M, Wang H, Lin Z, Zhang X, Fang DD, Zhang J (2015) A comparative meta-analysis of QTL between intraspecific Gossypium hirsutum and interspecific G. hirsutum × G. barbadense populations. Mol Genet Genomics 290:1003–1025

    Article  CAS  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 (2016a) 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 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 (2016b) Two genomic regions associated with fiber quality traits in Chinese upland cotton under apparent breeding selection. Sci Rep 6:38496

    Article  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 (2016c) Identification of favorable SNP alleles and candidate genes for traits related to early maturity via GWAS in upland cotton. BMC Genom 17:687

    Article  Google Scholar 

  • Sun Z, Wang X, Liu Z, Gu Q, Zhang 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 Biotechnol J 15:982–996

    Article  CAS  Google Scholar 

  • Tafesse FG, Guimaraes CP, Maruyama T, Carette JE, Lory S, Brummelkamp TR, Ploegh HL (2014) GPR107, a G-protein-coupled receptor essential for intoxication by Pseudomonas aeruginosa exotoxin A, localizes to the Golgi and is cleaved by furin. J Biol Chem 289:24005–24018

    Article  CAS  Google Scholar 

  • Thieme CJ, Rojas-Triana M, Stecyk E, Schudoma C, Zhang W, Yang L, Minambres M, Walther D, Schulze WX, Paz-Ares J, Scheible WR, Kragler F (2015) Endogenous Arabidopsis messenger RNAs transported to distant tissues. Nat Plants 1:15025

    Article  CAS  Google Scholar 

  • Tian F, Bradbury PJ, Brown PJ, Hung H, Sun Q, Flint-Garcia S, Rocheford TR, McMullen MD, Holland JB, Buckler ES (2011) Genome-wide association study of leaf architecture in the maize nested association mapping population. Nat Genet 43:159–162

    Article  CAS  Google Scholar 

  • Turner SD (2014) qqman: an R package for visualizing GWAS results using Q–Q and manhattan plots. Biorxiv. https://doi.org/10.1101/005165

  • Vollmer AH, Youssef NN, Dewald DB (2011) Unique cell wall abnormalities in the putative phosphoinositide phosphatase mutant AtSAC9. Planta 234:993–1005

    Article  CAS  Google Scholar 

  • Wang H, Huang C, Guo H, Li X, Zhao W, Dai B, Yan Z, Lin Z (2015) QTL mapping for fiber and yield traits in upland cotton under multiple environments. PLoS ONE 10:e0130742

    Article  Google Scholar 

  • Wu J, Gutierrez OA, Jenkins JN, McCarty JC, Zhu J (2008) Quantitative analysis and QTL mapping for agronomic and fiber traits in an RI population of upland cotton. Euphytica 165:231–245

    Article  Google Scholar 

  • Würschum T, Leiser WL, Kazman E, Longin CFH (2016) Genetic control of protein content and sedimentation volume in European winter wheat cultivars. Theor Appl Genet 129:1685–1696

    Article  Google Scholar 

  • Xia Z, Zhang X, Liu Y, Jia Z, Zhao H, Li C, Wang Q (2014) Major gene identification and quantitative trait locus mapping for yield-related traits in upland cotton (Gossypium hirsutum L.). J Integr Agric 13:299–309

    Article  CAS  Google Scholar 

  • Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, Kong L, Gao G, Li CY, Wei L (2011) KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res 39:W316–W322

    Article  CAS  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 

  • Yang N, Lu Y, Yang X, Huang J, Zhou Y, Ali F, Wen W, Liu J, Li J, Yan J (2014) Genome wide association studies using a new nonparametric model reveal the genetic architecture of 17 agronomic traits in an enlarged maize association panel. PLoS Genet 10:e1004573

    Article  Google Scholar 

  • Zhang JF, Stewart JM (2000) Economical and rapid method for extracting cotton genomic DNA. J Cotton Sci 4:193–201

    CAS  Google Scholar 

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

    Google Scholar 

  • Zhang Z, Ersoz E, Lai CQ, Todhunter RJ, Tiwari HK, Gore MA, Bradbury PJ, Yu J, Arnett DK, Ordovas JM, Buckler ES (2010) Mixed linear model approach adapted for genome-wide association studies. Nat Genet 42:355–360

    Article  CAS  Google Scholar 

  • Zhang W, Liu F, Li S, Wang W, Wang C, Zhang X, Wang Y, Wang K (2011) QTL analysis on yield and its components in upland cotton RIL. Acta Agron Sin 37:433–442

    CAS  Google Scholar 

  • Zhang J, Singh A, Mueller DS, Singh AK (2015a) Genome-wide association and epistasis studies unravel the genetic architecture of sudden death syndrome resistance in soybean. Plant J 84:1124

    Article  CAS  Google Scholar 

  • Zhang T, Hu Y, Jiang W, Fang L, Guan X, Chen J, Zhang J, Saski CA, Scheffler BE, Stelly DM, Hulse-Kemp AM, Wan Q, Liu B, Liu C, Wang S, Pan M, Wang Y, Wang D, Ye W, Chang L, Zhang W, Song Q, Kirkbride RC, Chen X, Dennis E, Llewellyn DJ, Peterson DG, Thaxton P, Jones DC, Wang Q, Xu X, Zhang H, Wu H, Zhou L, Mei G, Chen S, Tian Y, Xiang D, Li X, Ding J, Zuo Q, Tao L, Liu Y, Li J, Lin Y, Hui Y, Cao Z, Cai C, Zhu X, Jiang Z, Zhou B, Guo W, Li R, Chen ZJ (2015b) Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement. Nat Biotechnol 33:531–537

    Article  CAS  Google Scholar 

  • Zhao Y, Wang H, Chen W, Li Y (2014) Genetic structure, linkage disequilibrium and association mapping of Verticillium wilt resistance in elite cotton (Gossypium hirsutum L.) germplasm population. PLoS ONE 9:e86308

    Article  Google Scholar 

  • Zhiyuan N, Chen H, Mei H, Zhang T (2014) Molecular tagging of QTLs for fiber quality and yield in the upland cotton cultivar Acala-Prema. Euphytica 195:143–156

    Article  Google Scholar 

  • Zhu T, Liang C, Meng Z, Sun G, Meng Z, Guo S, Zhang R (2017) CottonFGD: an integrated functional genomics database for cotton. BMC Plant Biol 17:101

    Article  Google Scholar 

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Acknowledgements

This work was supported by the National Key Research and Development Program (2016YFD0101405), the China Agriculture Research System (CARS-18-08), the Science and Technology Support Program of Hebei Province (16226307D) and the Top Talent Fund of Hebei Province.

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Correspondence to Caiying Zhang or Zhiying Ma.

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The experiments were performed in compliance with the current laws of China.

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Communicated by Brent Hulke.

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122_2018_3162_MOESM1_ESM.docx

Figure S1. Manhattan plots showing the GWAS results for BN per plant in different environments. Figure S2. Manhattan plots showing the GWAS results for BW in different environments. Figure S3. Manhattan plots showing the GWAS results for LP in different environments. Figure S4. Manhattan plots showing the GWAS results for FBN per plant in different environments. Figure S5. Manhattan plots showing the GWAS results for the SI in different environments. Figure S6. Manhattan plots showing the GWAS results for the LI in different environments. (DOCX 3772 kb)

122_2018_3162_MOESM2_ESM.xlsx

Table S1. Phenotypic variation for six yield-related traits in the association population. Table S2. ANOVA results for and H2 of six yield-related traits. Table S3. Summary of SNPs that are significantly associated with six yield-related traits. Table S4. List of all 689 candidate genes associated with yield-related traits. Table S5. KEGG pathway and GO analysis results of all candidate genes involved in yield-related traits. Table S6. List of candidate genes in the top five KEGG pathways. (XLSX 279 kb)

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Sun, Z., Wang, X., Liu, Z. et al. A genome-wide association study uncovers novel genomic regions and candidate genes of yield-related traits in upland cotton. Theor Appl Genet 131, 2413–2425 (2018). https://doi.org/10.1007/s00122-018-3162-y

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  • DOI: https://doi.org/10.1007/s00122-018-3162-y

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