Abstract
Fusarium wilt caused by the soil-borne fungus Fusarium oxysporum f. sp. vasinfectum (FOV) race 4 (FOV4) has become one of the most important emerging diseases in US cotton production. Numerous QTLs have been reported for resistance to FOV; however, no major FOV4-resistance QTL or gene has been identified and used in breeding Upland cotton (Gossypium hirsutum) for FOV4 resistance. In this study, a panel of 223 Chinese Upland cotton accessions was evaluated for FOV4 resistance based on seedling mortality rate (MR) and stem and root vascular discoloration (SVD and RVD). SNP markers were developed based on targeted genome sequencing using AgriPlex Genomics. The chromosome region at 2.130–2.292 Mb on D03 was significantly correlated with both SVD and RVD but not with MR. Based on the two most significant SNP markers, accessions homozygous for AA or TT SNP genotype averaged significantly lower SVD (0.88 vs. 2.54) and RVD (1.46 vs. 3.02) than those homozygous for CC or GG SNP genotype. The results suggested that a gene or genes within the region conferred resistance to vascular discoloration caused by FOV4. The Chinese Upland accessions had 37.22% homozygous AA or TT SNP genotype and 11.66% heterozygous AC or TG SNP genotype, while 32 US elite public breeding lines all had the CC or GG SNP genotype. Among 463 obsolete US Upland accessions, only 0.86% possessed the AA or TT SNP genotype. This study, for the first time, has developed diagnostic SNPs for marker-assisted selection and identified FOV4-resistant Upland germplasms with the SNPs.
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 Genom 292:1221–1235
Abdelraheem A, Kuraparthy V, Hinze L, Stelly D, Zhang JF (2020) A genome-wide association study uncovers consistent quantitative trait loci for resistance to Verticillium wilt and Fusarium wilt in the U.S. Upland Cotton. Theor Appl Genet 133:563–577
Abdelraheem A, Zhu Y, Dever JK, Wheeler TA, Wedegaertner T, Hake K, Zhang JF (2021) Identification of resistance sources to Fusarium wilt race 4 in Gossypium barbadense and cultivated Asiatic diploid species. Euphytica 217:153
Abdelraheem A, Zhu Y, Zhang JF (2022) Quantitative trait locus mapping for fusarium wilt race 4 resistance in a recombinant inbred line population of Pima cotton (Gossypium barbadense). Pathogens 11:1143
Armstrong GM, Armstrong JK (1960) American, Egyptian, and Indian cotton-wilt fusaria: their pathogenicity and relationship to other wilt fusaria (No. 1219). US Dep Agric Tech Bull 1219:1–19
Bell AA, Gu A, Olvey J, Wagner TA, Tashpulatov JJ, Prom S, Quintana J, Nichols RL, Liu J (2019) Detection and characterization of Fusarium oxysporum f. sp. vasinfectum VCG0114 (Race 4) isolates of diverse geographic origins. Plant Dis 103:1998–2009
Blasingame D, Patel MV (2013) Cotton disease loss estimate committee report. In: Proceedings of the Beltwide cotton conference, National Cotton Council, Memphis, TN, pp 1242–1245
Broccanello B, Chiodi C, Funk A, McGrath M, Panella L, Stevanato P (2018) Comparison of three PCR-based assays for SNP genotyping in plants. Plant Methods 14:28
Cianchetta AN, Davis RM (2015) Fusarium wilt of cotton: management strategies. Crop Prot 73:40–44
Cianchetta AN, Allen TW, Hutmacher RB, Kemerait RC, Kirkpatrick TL, Lawrence GW, Lawrence KS, Mueller JD, Nichols RL, Olsen MW, Overstreet C, Woodward JE, Davis RM (2015) Survey of Fusarium oxysporum f. sp. vasinfectum in the United States. J Cotton Sci 19:328–336
Davis RM, Colyer PD, Rothrock CS, Kochman JK (2006) Fusarium wilt of cotton: population diversity and implications for management. Plant Dis 90:692–703
Diaz J, Garcia J, Lara C, Hutmacher RB, Ulloa M, Nichols RL, Ellis ML (2021) Characterization of current Fusarium oxysporum f. sp. vasinfectum isolates from cotton in the San Joaquin Valley of California and Lower Valley El Paso. Texas Plant Dis 105:1898–1911
Du X, Huang G, He S, Yang Z, Sun G, Ma X, Li N, Zhang X, Sun J, Liu M, Jia Y, Pan Z, Gong W, Liu Z, Zhu H, Ma L, Liu F, Yang D, Wang F, Fan W, Gong Q, Peng Z, Wang L, Wang X, Xu S, Shang H, Lu C, Zheng H, Huang S, Lin T, Zhu Y, Li F (2018) Resequencing of 243 diploid cotton accessions based on an updated A genome identifies the genetic basis of key agronomic traits. Nat Genet 50:796–802
Feng CD, Zhang JF, Liu JL, Wu ZB, Guo JH, Sun JZ (1998) Allelism and linkage test of Upland cotton genes resistant to Fusarium wilt. Hereditas 20:33–36
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, USA. Plant Dis 102:446
Han W, Zhao J, Deng X, Gu A, Li D, Wang Y, Lu X, Zu Q, Chen Q, Chen QJ, Zhang JF, Qu Y (2022) QTL mapping and identification of candidate genes for resistance to Fusarium wilt race 7 using a resequencing-based high density genetic bin map in a recombinant inbred line population of Gossypium barbadense. Front Plant Sci 13:815643
Holmes EA, Bennett RS, Spurgeon DW, Colyer PD, Davis RM (2009) New genotypes of Fusarium oxysporum f. sp. vasinfectum from the southeastern United States. Plant Dis 93:1298–1304
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
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, Kuraparthy V, Bowman D, Jones D, Burke J (2013) Elite-Upland cotton germplasm-pool assessment of Fusarium wilt resistance in California. Agron J 105:1635–1644
Kim Y, Hutmacher RB, Davis RM (2005) Characterization of California isolates of Fusarium oxysporum f. sp. vasinfectum. Plant Dis 89:366–372
Liu S, Zhang X, Xiao S, Ma J, Shi W, Qin T, Xi H, Nie X, You C, Xu Z, Wang T, Wang Y, Zhang Z, Li J, Kong J, Aierxi A, Yu Y, Lindsey K, Klosterman SJ, Zhang X, Zhu L (2021) A single-nucleotide mutation in a glutamate receptor-like gene confers resistance to Fusarium wilt in Gossypium hirsutum. Adv Sci 8:2002723
Lawrence K, Strayer-Scherer A, Norton R, Hu J, Faske T, Hutmacher R, Mueller J, Small I, Grabau Z, Kemerait B, Jardine D, Price P, Watson T, Allen T, Meeks C, Idowu J, Thiessen L, Byrd S, Goodson J, Kelly H (2021) Cotton disease loss estimate committee report, 2020. In: Proceedings of the Beltwide Cotton Conference, National Cotton Council, Memphis, TN, pp 3–4
Said JI, Knapka JA, Song M, Zhang JF (2015) Cotton QTLdb: a cotton QTL database for QTL analysis, visualization, and comparison between Gossypium hirsutum and G. hirsutum × G. barbadense populations. Mol Genet Genom 290:1615–1625
Sanogo S, Zhang JF (2016) Resistance sources, resistance screening techniques and disease management for Fusarium wilt in cotton. Euphytica 207:255–271
Smith AL, Dick JB (1960) Inheritance of resistance to Fusarium wilt in Upland and Sea Island Cottons as complicated by nematodes under field conditions. Phytopathology 50:44–48
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, Percy R, Zhang JF, Hutmacher RB, Wright SD, Davis RM (2009) Registration of four Pima cotton germplasm lines having good levels of Fusarium wilt race 4 resistance with moderate yields and good fibers. J Plant Reg 3:198–202
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, Hutmacher RB, Percy RG, Wright SD, Burke JJ (2016) Registration of five Pima cotton germplasm lines (SJ-FR05–FR09) with improved resistance to Fusarium wilt race 4 and good lint yield and fiber quality. J Plant Reg 10:154–158
Ulloa M, Hutmacher RB, Schramm T, Ellis ML, Nichols R, Roberts PA, Wright SD (2020) Sources, selection and breeding of Fusarium wilt (Fusarium oxysporum f. sp. vasinfectum) race 4 (FOV4) resistance in Upland (Gossypium hirsutum L.) cotton. Euphytica 216:109
Ulloa M, Abdurakhmonov I, Hutmacher R, Schramm T, Shermatov S, Buriev Z, Roberts P, Ellis M, Payton P (2022) Registration of three Gossypium barbadense L. American Pima-like germplasm lines (PSSJ-FRP01, PSSJ-FRP02, and PSSJ-FRP03) with improved resistance to Fusarium wilt race 4 and good fiber quality. J Plant Reg 16:626–634
Ulloa M, Hutmacher RB, Zhang JF, Schramm T, Roberts PA, Ellis M, Dever JK, Wheeler TA, Witt TW, Sanogo S, Hague S, Keely M, Arce J, Angeles J, Hake K, Payton P (2023) Registration of 17 upland germplasm lines (PSSJ-FRU01 to PSSJ-FRU17) with improved resistance to Fusarium wilt race 4 and good fiber quality. J Plant Reg 17:152–163
Wagner TA, Bell AA, Castles ZA, Ali A, Flores O, Liu J (2022) Detection, genotyping, and virulence characterization of Fusarium wilt race 4 (VCG0114) causing cotton wilt in three Texas fields. J Phytopath 170:492–503
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
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
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
Zhang JF (2018) Fighting Fusarium wilt through breeding in cotton: a successful story in China. In: Proceedings of the Beltwide Cotton Conference, National Cotton Council, Memphis, TN, pp 877–879
Zhang JF, Stewart JM (2000) Economical and rapid method for extracting cotton genomic DNA. J Cotton Sci 4:193–201
Zhang JF, Sanogo S, Ma ZY, Qu YY (2015) Breeding, genetics, and quantitative trait locus mapping for Fusarium wilt resistance in cotton. Crop Sci 55:2435–2453
Zhang J, Wedegaertner T, Idowu OJ, Flynn R, Hughs SE, Jones DC (2016) Registration of ‘NuMex COT 15 GLS’ glandless cotton. J Plant Reg 10:223–227
Zhang J, Idowu OJ, Wedegaertner T (2020a) Registration of glandless ‘NuMex COT 17 GLS’ Upland cotton cultivar with Fusarium wilt race 4 resistance. J Plant Reg 14:1–9
Zhang JF, Abdelraheem A, Zhu Y, Wheeler TA, Dever JK, Frelichowski J, Love J, Ulloa M, Jenkins JN, McCarty JC Jr, Nichols R, Wedegaertner T (2020b) Assessing genetic variation for Fusarium wilt race 4 resistance in tetraploid cotton by screening over three thousand germplasm lines under greenhouse or controlled conditions. Euphytica 216:106
Zhang JF, Abdelraheem A, Zhu Y, Wheeler TA, Dever JK, Elkins-Arc EH, Nichols R, Wedegaertner T (2020c) Pedigree selection under field conditions within Acala 1517-08 and its glandless derivatives for development of cotton resistant to Fusarium wilt caused by Fusarium oxysporum f. sp. vasinfectum race 4. Euphytica 216:155
Zhang JF, Zhu Y, Abdelraheem A, Lujan P, Idowu J, Nichols R, Wedegaertner T (2020d) Field survey, detection and characterization of Fusarium wilt race 4 in cotton in New Mexico. In: Proceedings of the Beltwide Cotton Conferences. p 84
Zhang JF, Abdelraheem A, Zhu Y, Wheeler TA, Dever JK, Nichols R, Wedegaertner T (2021) Importance of temperature in evaluating cotton for resistance to Fusarium wilt caused by Fusarium oxysporum f. sp. vasinfectum race 4. Crop Sci 61:1783–1796
Zhang J, Abdelraheem A, Zhu Y, Elkins-Arce H, Dever J, Whitelock D, Hake K, Wedegaertner W, Wheeler TA (2022a) Studies of evaluation methods for resistance to Fusarium wilt race 4 (Fusarium oxysporum f. sp. vasinfectum) in cotton: effects of cultivar, planting date, and inoculum density on disease progression. Front Plant Sci 13:900131
Zhang J, Zhu Y, Abdelraheem A, Elkins-Arce HD, Wheeler T, Dever J, Ulloa WD, Hake K, Wedegaertner T (2022b) Studies of evaluation parameters for resistance to Fusarium wilt in cotton caused by Fusarium wilt race 4 (Fusarium oxysporum f. sp. vasinfectum). Crop Sci 62:1115–1132
Zhang J, Zhu Y, Abdelraheem A, Elkins-Arce HD, Dever J, Wheeler T, Isakeit T, Hake K, Wedegaertner T (2022c) Use of a Latin square design to assess experimental errors in field evaluation of cotton for resistance to Fusarium wilt race 4. Crop Sci 62:575–591
Zhang JF, Abdelraheem A, Ma J, Zhu Y, Dever J, Wheeler TA, Hake K, Wedegaertner T, Yu J (2022d) Mapping of dynamic QTLs for resistance to Fusarium wilt (Fusarium oxysporum f. sp. vasinfectum) race 4 in a backcross inbred line population of Upland cotton. Mol Genet Genom 297:319–332
Zhang JF, Zhu Y, Abdelraheem A, Arce H, Dever JK, Wheeler TA, Hake K, Wedegaertner T (2022e) Evaluation methods, germplasm evaluation, genetics, and breeding for resistance to Fusarium wilt race 4 in cotton: personal knowledge and experiences. In: Proceedings of the Beltwide Cotton Conferences, pp 110–120
Zhang JF, Zhu Y, Elkins-Arce H, Wheeler T, Dever JK, Whitelock D, Wedegaertner T, Hake K, Bissonnette K (2022f) Efficiency of selection for resistance to Fusarium wilt race 4 in cotton when conducted in the field versus greenhouse. Euphytica 218:165
Zhao N, Wang W, Grover CE, Jiang K, Pan Z, Guo B, Zhu J, Su Y, Wang M, Nie H, Xiao L, Guo A, Yang J, Cheng C, Ning X, Li B, Xu H, Adjibolosoo D, Aierxi A, Li P, Geng J, Wendel JF, Kong J, Hua J (2021) Genomic and GWAS analyses demonstrate phylogenomic relationships of Gossypium barbadense in China and selection for fibre length, lint percentage and Fusarium wilt resistance. Plant Biotech J 20:691–710
Zhu Y, Abdelraheem A, Teng ZH, Sanogo S, Wheeler T, Wedegaertner T, and Zhang JF (2019) Pathogenicity test of Fusarium wilt and screening germplasm lines for Fusarium wilt resistance in cotton. In: Proceedings of the Beltwide Cotton Conference, p 15
Zhu Y, Lujan PA, Wedegaertner T, Nichols R, Abdelraheem A, Zhang JF, Sanogo S (2020) First report of Fusarium oxysporum f. sp. vasinfectum race 4 causing Fusarium wilt of cotton in New Mexico, USA. Plant Dis 104:588
Zhu Y, Abdelraheem A, Lujan P, Idowu OJ, Sullivan P, Nichols R, Wedegaertner T, Zhang JF (2021a) Detection and characterization of Fusarium wilt (Fusarium oxysporum f. sp. vasinfectum) race 4 causing Fusarium wilt of cotton seedlings in New Mexico, USA. Plant Dis 105:3353–3367
Zhu Y, Abdelraheem A, Wheeler TA, Dever JK, Wedegaertner T, Hake KD, Zhang JF (2021b) Interactions between cotton genotypes and Fusarium wilt race 4 isolates from Texas and resistance evaluation in cotton. Crop Sci 61:1809–1825
Zhu Y, Abdelraheem A, Thyssen GN, Teng Z, Fang DD, Jenkins JN, McCarty JC Jr, Wedegaertner T, Zhang JF (2022) A GWAS identified a major QTL for resistance to Fusarium wilt (Fusarium oxysporum f. sp. vasinfectum) race 4 in a MAGIC population derived from intermating of eleven Upland cotton (Gossypium hirsutum) parents. Theor Appl Genet 135:2297–2312
Zhu Y, Elkins-Arce H, Wheeler T, Dever J, Whitelock D, Hake K, Wedegaertner T, Zhang J (2023a) Effect of growth stage, cultivar, and root wounding on disease development in cotton caused by Fusarium wilt race 4 (Fusarium oxysporum f. sp. vasinfectum). Crop Sci 63:101–114
Zhu Y, Elkins-Arce H, Wheeler T, Dever JK, Whitelock D, Hake K, Bissonnette K, Zhang JF (2023b) Pre- and post- emergence damping-off in cotton caused by Fusarium wilt (Fusarium oxysporum f. sp. vasinfectum) race 4: Genotypic difference and implications. Phytopathology, accepted upon revision, February 21, 2023b.
Funding
This study was funded by Cotton Incorporated (21-076).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Communicated by Bing Yang.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zhang, J., Zhu, Y., Wheeler, T. et al. Targeted development of diagnostic SNP markers for resistance to Fusarium wilt race 4 in Upland cotton (Gossypium hirsutum). Mol Genet Genomics 298, 895–903 (2023). https://doi.org/10.1007/s00438-023-02024-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-023-02024-2