Abstract
Key message
A high-resolution GWAS detected consistent QTL for resistance to Verticillium wilt and Fusarium wilt race 4 in 376 U.S. Upland cotton accessions based on six independent replicated greenhouse tests.
Abstract
Verticillium wilt (VW, caused by Verticillium dahliae Kleb.) and Fusarium wilt (FOV, caused by Fusarium oxysporum f.sp. vasinfectum Atk. Sny & Hans) are the most important soil-borne fungal diseases in cotton. To augment and refine resistance quantitative trait loci (QTL), we conducted a genome-wide association study (GWAS) using high-density genotyping with the CottonSNP63K array. Resistance of 376 US Upland cotton accessions to a defoliating VW and virulent FOV4 was evaluated in four and two independent replicated greenhouse tests, respectively. A total of 15 and 13 QTL for VW and FOV4 resistances were anchored by 30 (on five chromosomes) and 56 (on six chromosomes) significant single nucleotide polymorphic (SNPs) markers, respectively. QTL on c8, c10, c16, and c21 were consistent in two or more tests for VW resistance, while two QTL on c8 and c14 were consistent for FOV4 resistance in two tests. Two QTL clusters on c16 and c19 were observed for both VW and FOV4 resistance, suggesting that these genomic regions may harbor genes in response to both diseases. Using BLAST search against the sequenced TM-1 genome, 30 and 35 candidate genes were identified on four QTL for VW resistance and on three QTL for FOV4 resistance, respectively. These genomic regions were rich in NBS-LRR genes presented in clusters. The results create opportunities for further studies to determine the correlations of field resistance with these QTL, molecular examinations of VW and FOV4 resistances, marker-assisted selection (MAS) and eventual cloning of QTL for disease resistance in cotton.
Similar content being viewed by others
References
Abdelraheem A, Liu F, Song M, Zhang JF (2017) A meta-analysis of quantitative trait loci for abiotic and biotic stress resistance in tetraploid cotton. Mol Genet Genomics 292:1221–1235
Abdurakhmonov IY, Buriev ZT, Shermatov SE, Abdullaev AA, Urmonov K, Kushanov F, Egamberdiev SS, Shapulatov U, Abdukarimov A, Saha S, Jenkins JN, Kohel RJ, Yu JZ, Pepper AE, Kumpatla SP, Ulloa M (2012) Genetic diversity in Gossypium genus. In: Caliskan M (ed) Genetic Diversity in Plants, ISBN: 978–953–51–0185–7, InTech, pp 313–338
Armstrong GM, Armstrong JK (1960) American, Egyptian, and Indian cotton-wilt Fusaria: Their pathogenicity and relationship to other wilt fusaria. US Dep Agric Tech Bull 219
Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21:263–265
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Statist Soc B 57:289–300
Bernardo R (2008) Molecular markers and selection for complex traits in plants: learning from the last 20 years. Crop Sci 48:1649–1664
Blasingame D, Patel MV (2011) Cotton disease loss estimate committee report. In: Proceedings of Beltwide Cotton Conference, Atlanta, GA, pp 306–308
Bowman DT, May OL, Calhoun DS (1996) Genetic base of upland cotton cultivars released between 1970 and 1990. Crop Sci 36:577–581
Bradbury PJ, Zhang Z, Kroon DE, Casstevens RM, Ramdoss Y, Buckler ES (2007) TASSEL: Software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635
Brubaker CL, Bourland FM, Wendel JF (1999) The origin and domestication of cotton. In: Smith CW, Cothren JT (eds) Cotton: Origin, History, Technology, and Production. Wiley, New York, pp 3–32
Dent AE, Bridgett MV (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361
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
Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587
Fang H, Zhou H, Sanogo S, Flynn R, Percy RG, Hughs SE, Ulloa M, Jones DC, Zhang JF (2013) Quantitative trait locus mapping for Verticillium wilt resistance in a backcross inbred line population of cotton (Gossypium hirsutum × Gossypium barbadense) based on RGA-AFLP analysis. Euphytica 194:79–91
Goicoechea N (2009) To what extent are soil amendments useful to control Verticillium wilt? Pest Manag Sci 65:831–839
Gupta PK, Rustgi S, Kulwal PL (2005) Linkage disequilibrium and association studies in higher plants: Present status and future prospects. Plant Mol Biol 57:461–485
Halpern HC, Bell AA, Wagner TA, Liu J, Nichols RL, Olvey J, Woodward JE, Sanogo S, Jones CA, Chan CT, Brewer MT (2018) First report of Fusarium wilt of cotton caused by Fusarium oxysporum f. sp. vasinfectum race 4 in Texas, U.S.A. Plant Dis 102:446
Hinze LL, Hulse-Kemp AM, Wilson IW, Zhu QH, Llewellyn DJ, Taylor JM, Spriggs A, Fang DD, Ulloa M, Burke JJ, Giband M, Lacape JM, Van Deynze A, Udall JA, Scheffler JA, Hague S, Wendel JF, Pepper AE, Frelichowski J, Lawley CT, Jones DC, Percy RG, Stelly DM (2017) Diversity analysis of cotton (Gossypium hirsutum L.) germplasm using the CottonSNP63K Array. BMC Plant Biol 17:37
Holland JB (2007) Genetic architecture of complex traits in plants. Curr Opin Plant Biol 10:156–161
Hu Y, Chen J, Fang L, Zhang Z, Ma W, Niu Y, Ju L, Deng J, Zhao T, Lian J, Baruch K, Fang D, Liu X, Ruan YL, Rahman MU, Han J, Wang K, Wang Q, Wu H, Mei G, Zang Y, Han Z, Xu C, Shen W, Yang D, Si Z, Dai F, Zou L, Huang F, Bai Y, Zhang Y, Brodt A, Ben-Hamo H, Zhu X, Zhou B, Guan X, Zhu S, Chen X, Zhang T (2019) Gossypium barbadense and Gossypium hirsutum genomes provide insights into the origin and evolution of allotetraploid cotton. Nat Genet 51:739–748
Hulse-Kemp AM, Lemm J, Plieske J, Ashrafi H, Buyyarapu R, Fang DD, Frelichowski J et al (2015) Development of a 63K SNP array for cotton and high-density mapping of intraspecific and interspecific populations of Gossypium spp. G3 Genes Genome. Genet 5:1187–1209
Hutmacher RB, Ulloa M, Wright SD, Campbell BT, Percy RG, Wallace T, Myers G, Bourland F, Weaver D, Chee P, Thaxton P, Zhang J, Smith W, Dever J, Kuraprthy V, Bowman D, Jones D, Burke JJ (2013) Elite-upland cotton germplasm-pool assessment of Fusarium wilt (FOV) resistance in California. Agron J 105:1635–1644
Ingvarsson PK, Street NR (2011) Association genetics of complex traits in plants. New Phytol 189:909–922
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
Karademir E, Karademir C, Ekinci R, Baran B, Sagir A (2012) Effect of Verticillium dahliae Kleb. on cotton yield and fiber technological properties. Int J Plant Prod 6:387–408
Kim Y, Hutmacher RB, Davis RM (2005) Characterization of California isolates of Fusarium oxysporum f. sp. vasinfectum. Plant Dis 89:366–372
Kirkpatrick TL, Rothrock CS (2011) Compendium of cotton diseases, 2nd edn. APS Press, St Paul, MN
Kochman J, Swan L, Moore N, Bentley S, O’Neill W, Mitchell A, Obst N, Lehane J, Gulino L,Salmond G (2002) The Fusarium threat-are we making the progress? In: Proceeding of 11th cotton conference, August 13–15, 2002, Brisbane, pp 643–652
Li T, Ma X, Li N, Zhou L, Liu Z, Han H, Gu Y, Bao Y, Chen J, Da X (2017) Genome-wide association study discovered candidate genes of Verticillium wilt resistance in upland cotton (Gossypium hirsutum L.). Plant Biotech J 15:1520–1532
Martinez G, Abdelraheem A, Darapuneni M, Jenkins JN, McCarty JC, Zhang JF (2018) Evaluation of a multi-parent advanced generations inter-cross (MAGIC) introgresed population for Verticillium wilt resistance in Upland cotton. Euphytica 214:197
May OL, Bowman DT, Calhoun DS (1995) Genetic diversity of U.S. upland cotton cultivars released between 1980 and 1990. Crop Sci 35:1570–1574
Mei H, Ai N, Zhang X, Ning Z, Zhang T (2014) QTLs conferring FOV 7 resistance detected by linkage and association mapping in Upland cotton. Euphytica 197:237–249
Mohamed HA (1963) Inheritance of resistance to fusarium wilt in some Egyptian cottons. Empire Cotton Grow Rev 40:292–295
Oakley SR (1998) Acala GTO Maxxa and Acala C-141; New Californian Acala varieties for the San Joaquin Valley. In: Dugger P, Richter D (eds) Proceedings of the beltwide cotton conference, vol I. San Diego, CA, USA, Jan 5–9. Memphis USA; National Cotton Council, 46–47 (En) California Planting cotton Seed Distributors, Shafter, CA, USA
Palanga KK, Jamshed M, Rashid MHO, Gong J, Li J, Iqbal MS, Liu A, Shang H, Shi Y, Chen T, Ge Q, Zhang Z, Dilnur T, Li W, Li P, Gong W, Yuan Y (2017) Quantitative trait locus mapping for Verticillium wilt resistance in an upland cotton recombinant inbred line using SNP-based high density genetic map. Front Plant Sci 8:382
Percy RG, Frelichowski JE, Arnold MD, Campbell TB, Dever JK, Fang DD, Hinze LL, Main D, Scheffler J, Sheehan MA, Ulloa M, Yu J, Yu J (2014) The U.S. national cotton germplasm collection- its contents, preservation, characterization, and evaluation. In: Abdurakhmovov I (ed.), World Cotton Germplasm Resources. Intech pp 167–201
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Rafalski JA (2010) Association genetics in crop improvements. Curr Opin Plant Biol 13:174–180
Said JI, Lin ZX, Zhang XL, Song MZ, Zhang JF (2013) A comprehensive meta QTL analysis for fiber quality, yield, yield related and morphological traits, drought tolerance, and disease resistance in tetraploid cotton. BMC Genomics 14:776
Said JI, Knapka JA, Song MZ, Zhang JF (2015a) Cotton QTLdb: a cotton QTL database for QTL analysis, visualization, and comparison between Gossypium hirsutum and G. hirsutum × G. barbadense populations. Mol Genet Genomics 290:1615–1625
Said JI, Song MZ, Wang H, Lin Z, Zhang X, Fang DD, Zhang JF (2015b) A comparative meta-analysis of QTL between intraspecific Gossypium hirsutum and interspecific G. hirsutum x G. barbadense populations. Mol Genet Genomics 290:1003–1025
Sanogo S, Zhang JF (2016) Resistance source, resistance screening techniques and disease management for Fusarium wilt in cotton. Euphytica 207:255–271
Shi Y, Zhang B, Liu A, Li W, Li J, Lu Q, Zhang Z, Li S, Gong W, Shang H, Gong J, Chen T, Ge Q, Wang T, Zhu H, Liu Z, Yuan Y (2016) Quantitative trait loci analysis of Verticillium wilt resistance in interspecific backcross populations of Gossypium hirsutum × Gossypium barbadense. BMC Genomics 17:877
Smith AL, Dick JB (1960) Inheritance of resistance to Fusarium wilt in Upland and Sea Island cotton as complicated by nematodes under field conditions. Phytopathology 50:44–48
Smith CW, Cantrell RG, Moser HS, Oakley SR (1999) History of cultivar development in the United States. In: Smith CW, Cothren JT (eds) Cotton: origin, history, technology, and production. John Wiley & Sons Inc, New York, pp 99–171
Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler ES (2001) Dwarf polymorphisms associate with variation in flowering time. Nat Genet 28:286–289
Tyagi P, Gore M, Bowman DT, Campbell B, Udall JA, Kuraparthy V (2014) Genetic diversity and population structure in the US Upland cotton (Gossypium hirsutum L.). Theor Appl Genet 127:283–295
Ulloa M, Hutmacher RB, Davis RM, Wright SD, Percy R, Marsh B (2006) Breeding for Fusarium wilt race 4 resistance in cotton under field and greenhouse conditions. J Cotton Sci 10:114–127
Ulloa M, Wang C, Hutmacher RB, Wright SD, Davis RM, Saski CA, Roberts PA (2011) Mapping Fusarium wilt race 1 resistance genes in cotton by inheritance, QTL and sequencing composition. Mol Genet Genomics 286:21–36
Ulloa M, Hutmacher RB, Roberts PA, Wright SD, Nichols RL, Davis RM (2013) Inheritance and QTL mapping of Fusarium wilt race 4 resistance in cotton. Theor Appl Genet 126:1405–1418
Ulloa M, Wang C, Saha S, Hutmacher RB, Stelly DM, Jenkins JN, Roberts P (2016) Analysis of root-knot nematode and fusarium wilt disease resistance in cotton (Gossypium spp.) using chromosome substitution lines from two alien species. Genetica 144:167–179
Van Esbroeck GA, Bowman DT (1998) Cotton improvement. Cotton germplasm diversity and its importance to cultivar development. J Cotton Sci 2:121–129
Wang C, Roberts PA (2006) A Fusarium wilt resistance gene in Gossypium barbadense and its effect on root-knot nematode-wilt disease complex. Phytopathology 96:727–734
Wang P, Su L, Qin L, Hu B, Guo W, Zhang T (2009) Identification and molecular mapping of Fusarium wilt resistant gene in upland cotton. Theor Appl Genet 119:733–739
Wang C, Ulloa M, Duong T, Roberts PA (2018) QTL mapping of multiple independent loci for resistance to Fusarium oxysporum f. sp. vasinfectum races 1 and 4 in an interspecific cotton population. Phytopathology 108:759–767
Wendel JF, Cronn RC (2003) Polyploidy and the evolutionary history of cotton. Adv Agron 78:139–186
Wendel JF, Brubaker C, Percival A (1992) Genetic diversity in Gossypium hirsutum and the origin of Upland cotton. Am J Bot 79:1291–1310
Wilhelm S, Sagen JE, Tietz H (1974) Resistance to Verticillium wilt in cotton: Sources, techniques of identification. inheritance trends, and the resistance potential of multiline cultivars. Phytopathology 64:924–931
Yu J, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208
Zhang JF, Lu Y, Adragna H, Hughs E (2005) Genetic improvement of New Mexico Acala cotton germplasm and their genetic diversity. Crop Sci. 45:2363–2373
Zhang JF, Sanogo S, Flynn R, Baral JB, Bajaj S, Hughs S, Percy RG (2012) Germplasm evaluation and transfer of Verticillium wilt resistance from Pima (Gossypium barbadense) to Upland cotton (G. hirsutum). Euphytica 187:147–160
Zhang T, Qian N, Zhu X, Chen H, Wang S, Mei H, Zhang Y (2013) Variations and transmission of QTL alleles for yield and fiber qualities in upland cotton cultivars developed in China. PLoS One 8:e57220
Zhang JF, Fang H, Zhou HP, Sanogo S, Ma ZY (2014a) Genetics, breeding, and marker-assisted selection for Verticillium wilt resistance in cotton. Crop Sci 54:1289–1303
Zhang JF, Percy RG, McCarty JC Jr (2014b) Introgression genetics and breeding between Upland and pima cotton: a review. Euphytica 198:1–12
Zhang JF, Sanogo S, Ma Z, Qu Y (2015a) Breeding, genetics, and quantitative trait locus mapping for Fusarium wilt resistance in cotton. Crop Sci 55:2435–2452
Zhang JF, Yu JW, Pei WF, Li XL, Said J, Song M, Sanogo S (2015b) Genetic analysis of Verticillium wilt resistance in a backcross inbred line population and a meta-analysis of quantitative trait loci for disease resistance in cotton. BMC Genomics 16:577
Zhang T, Hu Y, Jiang W et al (2015c) Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement. Nat Biotechnol 33:531–537
Zhang JF, Abdelraheem A, Thyssen G, Fang DD, Jenkins JN, McCarty JC, Wedegaertner T (2019) Evaluation and genome-wide association study of Verticillium wilt resistance in a MAGIC population derived from intermating of 11 Upland cotton (Gossypium hirsutum) parents. Euphytica (Submitted)
Zhao K, Tung C, Eizenga GC, Wright MK, Ali ML, Price AH, Norton GJ, Islam MR, Reynolds A, Mezey J, McClung AM, Bustamante CD, McCouch SR (2011) Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nat Comm 2:467
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
Zhou HP, Hui F, Sanogo S, Hughs SE, Jones DC, Zhang JF (2014) Evaluation of Verticillium wilt resistance in commercial cultivars and advanced breeding lines of cotton. Euphytica 196:437–448
Zhu C, Gore M, Buckler ES, Yu J (2008) Status and prospects of association mapping in plants. Plant Genome J 1:5
Zhu Y, Lujan PA, Wedegaertner T, Nichols RL, Abdelraheem A, Zhang JF, Sanogo S (2019) First report of Fusarium oxysporum f. sp. vasinfectum race 4 causing Fusarium wilt of cotton in New Mexico, USA. Plant Dis. https://doi.org/10.1094/PDIS-06-19-1170-PDN
Author information
Authors and Affiliations
Contributions
JZ and TW conceived the study. AA, HE, and YZ performed the study. VK created the diversity panel and provided the seeds for the study. LH and DS performed CottonSNP63K array for part of the diversity panel. AA analyzed the results and drafted the manuscript. All authors read, edited, and approved the manuscript.
Corresponding author
Ethics declarations
Conflict interests
The authors declare that they have no competing interests.
Ethical standards
The authors state that all experiments in the study comply with the ethical standards in the US.
Additional information
Communicated by Yunbi Xu.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Abdelraheem, A., Elassbli, H., Zhu, Y. et al. A genome-wide association study uncovers consistent quantitative trait loci for resistance to Verticillium wilt and Fusarium wilt race 4 in the US Upland cotton. Theor Appl Genet 133, 563–577 (2020). https://doi.org/10.1007/s00122-019-03487-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-019-03487-x