Abstract
Key message
Four QTLs and an epistatic interaction were associated with disease severity in response to inoculation with Fusarium oxysporum f. sp. melonis race 1 in a recombinant inbred line population of melon.
Abstract
The USDA Cucumis melo inbred line, MR-1, harbors a wealth of alleles associated with resistance to several major diseases of melon, including powdery mildew, downy mildew, Alternaria leaf blight, and Fusarium wilt. MR-1 was crossed to an Israeli cultivar, Ananas Yok’neam, which is susceptible to all of these diseases, to generate a recombinant inbred line (RIL) population of 172 lines. In this study, the RIL population was genotyped to construct an ultra-dense genetic linkage map with 5663 binned SNPs anchored to the C. melo genome and exhibits the overall high quality of the assembly. The utility of the densely genotyped population was demonstrated through QTL mapping of a well-studied trait, resistance to Fusarium wilt caused by Fusarium oxysporum f. sp. melonis (Fom) race 1. A major QTL co-located with the previously validated resistance gene Fom-2. In addition, three minor QTLs and an epistatic interaction contributing to Fom race 1 resistance were identified. The MR-1 × AY RIL population provides a valuable resource for future QTL mapping studies and marker-assisted selection of disease resistance in melon.
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References
Altschul SF, Gish W, Miller W et al (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
Argyris JM, Ruiz-Herrera A, Madriz-Masis P et al (2015) Use of targeted SNP selection for an improved anchoring of the melon (Cucumis melo L.) scaffold genome assembly. BMC Genom 16:4. https://doi.org/10.1186/s12864-014-1196-3
Belisario A, Luongo L, Corazza L, et al (2000) Studies on Fusarium oxysporum f. sp. melonis Italian populations [Cucumis melo L.]. Colture Protette 29(3):87–89
Berrocal-Lobo M, Molina A (2004) Ethylene response factor 1 mediates arabidopsis resistance to the soilborne fungus Fusarium oxysporum. Mol Plant Microbe Interact 17:763–770. https://doi.org/10.1094/MPMI.2004.17.7.763
Brien C (2016) asremlPlus: augments the use of ‘asreml’ in fitting mixed models. R package version 2.0-9. https://CRAN.R-project.org/package=asremlPlus. Accessed 10 Feb 2017
Broman KW, Sen S (2009) A guide to QTL mapping with R/qtl, vol 46. Springer, New York
Broman KW, Speed T (2002) A model selection approach for the identification of quantitative trait loci in experimental crosses. J R Stat Soc B 64(641–656):731–775
Broman KW, Wu H, Sen S, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890. https://doi.org/10.1093/bioinformatics/btg112
Browning BL, Browning SR (2016) Genotype imputation with millions of reference samples. Am J Hum Genet 98:116–126. https://doi.org/10.1016/j.ajhg.2015.11.020
Catanzariti A-M, Lim GTT, Jones DA (2015) The tomato I-3 gene: a novel gene for resistance to fusarium wilt disease. New Phytol 207:106–118. https://doi.org/10.1111/nph.13348
Chang C, Wang Y, Tung C (2017) Genome-wide single nucleotide polymorphism discovery and the construction of a high-density genetic map for melon (Cucumis melo L.) using genotyping-by-sequencing. Front Plant Sci 8:1–11. https://doi.org/10.3389/fpls.2017.00125
Cole SJ, Diener AC (2013) Diversity in receptor-like kinase genes is a major determinant of quantitative resistance to Fusarium oxysporum f. sp. matthioli. New Phytol 200:172–184. https://doi.org/10.1111/nph.12368
Daley J, Branham S, Levi A et al (2017) Mapping resistance to Alternaria cucumerina in Cucumis melo. Phytopathology 107:427–432
Danecek P, Auton A, Abecasis G et al (2011) The variant call format and VCFtools. Bioinformatics 27:2156–2158
Diaz A, Fergany M, Formisano G et al (2011) A consensus linkage map for molecular markers and quantitative trait loci associated with economically important traits in melon (Cucumis melo L.). BMC Plant Biol 11:111. https://doi.org/10.1186/1471-2229-11-111
Elshire RJ, Glaubitz JC, Sun Q et al (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6:e19379. https://doi.org/10.1371/journal.pone.0019379
Erzurum K, Taner Y, Secer E et al (1999) Occurrence of races of Fusarium oxysporum f. sp. melonis causing wilt on melon in Central Anatolia. J Turk Phytopathol 28:87–97
Ficcadenti N, Sestili S, Annibali S, Campanelli G (2002) Resistance to Fusarium oxysporum f. sp. melonis Race 1,2 in melon lines Nad-1 and Nad-2. Plant Dis 86:897–900. https://doi.org/10.1007/s10681-013-0971-6
Garcia-Mas J, Benjak A, Sanseverino W et al (2012) The genome of melon (Cucumis melo L.). Proc Natl Acad Sci USA 109:11872–11877. https://doi.org/10.1073/pnas.1205415109
Gilmour AR, Gogel BJ, Cullis BR et al (2009) ASReml user guide release 3.0. VSN International Ltd, Hemel Hempstead
Giri MK, Singh N, Banday ZZ et al (2017) GBF1 differentially regulates CAT2 and PAD4 transcription to promote pathogen defense in Arabidopsis thaliana. Plant J 91:802–815. https://doi.org/10.1111/tpj.13608
Glaubitz JC, Casstevens TM, Lu F et al (2014) TASSEL-GBS: a high capacity genotyping by sequencing analysis pipeline. PLoS One 9:e90346. https://doi.org/10.1371/journal.pone.0090346
Joobeur T, King JJ, Nolin SJ et al (2004) The fusarium wilt resistance locus Fom-2 of melon contains a single resistance gene with complex features. Plant J 39:283–297. https://doi.org/10.1111/j.1365-313X.2004.02134.x
Kosambi DD (1943) the estimation of map distances from recombination values. Ann Eugen 12:172–175. https://doi.org/10.1111/j.1469-1809.1943.tb02321.x
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760. https://doi.org/10.1093/bioinformatics/btp324
Manichaikul A, Moon JY, Sen Ś et al (2009) A model selection approach for the identification of quantitative trait loci in experimental crosses, allowing epistasis. Genetics 181:1077–1086. https://doi.org/10.1534/genetics.108.094565
Marchler-Bauer A, Bryant SH (2004) CD-search: protein domain annotations on the fly. Nucleic Acids Res 32:327–331. https://doi.org/10.1093/nar/gkh454
Marchler-Bauer A, Bo Y, Han L et al (2017) CDD/SPARCLE: Functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 45:D200–D203. https://doi.org/10.1093/nar/gkw1129
Namiki F, Shimizu K, Satoh K et al (2000) Occurrence of Fusarium oxysporum f. sp. melonis Race 1 in Japan. J Gen Plant Pathol 66:12–17
Nimmakayala P, Tomason YR, Abburi VL et al (2016) Genome-wide differentiation of various melon horticultural groups for use in GWAS for fruit firmness and construction of a high resolution genetic map. Front Plant Sci 7:1–15. https://doi.org/10.3389/fpls.2016.01437
R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Risser G, Banihashemi Z, Davis DW (1976) A proposed nomenclature of Fusarium oxysporum f. sp. melonis races and resistance genes in Cucumis melo. Phytopathology 66:1105–1106
Schreuder W, Lamprecht SC, Holz G (2000) Race determination and vegetative compatibility grouping of Fusarium oxysporum f. sp. melonis from South Africa. Plant Dis 84:231–234. https://doi.org/10.1094/pdis.2000.84.3.231
Sekhwal M, Li P, Lam I et al (2015) Disease resistance gene analogs (RGAs) in plants. Int J Mol Sci 16:19248–19290. https://doi.org/10.3390/ijms160819248
Sen S, Churchill GA (2001) A statistical framework for quantitative trait mapping. Genetics 159:371–387. https://doi.org/10.1126/science.1242429
Tezuka T, Waki K, Yashiro K et al (2009) Construction of a linkage map and identification of DNA markers linked to Fom-1, a gene conferring resistance to Fusarium oxysporum f. sp. melonis race 2 in melon. Euphytica 168:177–188. https://doi.org/10.1007/s10681-009-9881-z
Thomas CE (1982) Resistance to downy mildew in Cucumis melo plant introductions and American cultivars [Pseudoperonospora cubensis]. Plant Dis 66:500–502
Thomas CE (1986) Downy and powdery mildew resistant melon breeding line MR-1. HortScience 21:329
Thomas CE, McCreight JD, Jourdain EL (1990) Inheritance of resistance to Alternaria cucumerina in Cucumis melo line MR-1. Plant Dis 74:868–870
Wang Y, Thomas CE, Dean RA (2000) Genetic mapping of a fusarium wilt resistance gene (Fom-2) in melon (Cucumis melo L.). Mol Breed 6:379–389. https://doi.org/10.1023/A:1009671925793
Wang S, Yang J, Zhang M (2011) Developments of functional markers for Fom-2-mediated fusarium wilt resistance based on single nucleotide polymorphism in melon (Cucumis melo L.). Mol Breeding 27:385–393. https://doi.org/10.1007/s11032-010-9439-8
Wechter WP, Whitehead MP, Thomas CE, Dean RA (1995) Identification of a randomly amplified polymorphic DNA marker linked to the fom2 fusarium wilt resistance gene in melon MR-1. Phytopathology 85:1245–1249
Wechter WP, Dean RA, Thomas CE (1998) Development of sequence-specific primers that amplify a 1.5-kb DNA marker for race 1 fusarium wilt resistance in Cucumis melo L. HortScience 33:291–292
Wechter WP, Kousik C, McMillan M, Levi A (2012) Identification of resistance to fusarium oxysporum f. sp. niveum race 2 in citrullus lanatus var. citroides plant introductions. HortScience 47:334–338. https://doi.org/10.1002/ird.1717
Zeng ZB, Kao CH, Basten CJ (1999) Estimating the genetic architecture of quantitative traits. Genet Res 74:279–289. https://doi.org/10.1017/S0016672399004255
Zheng XY, Wolff DW, Baudracco-Arnas S, Pitrat M (1999) Development and utility of cleaved amplified polymorphic sequences (CAPS) and restriction fragment length polymorphisms (RFLPs) linked to the Fom-2 fusarium wilt resistance gene in melon (Cucumis melo L.). Theor Appl Genet 99:453–463. https://doi.org/10.1007/s001220051257
Zink FW (1992) Genetics of resistance to Fusarium oxysporum f. sp. melonis races 0 and 2 in melon cultivars Honey Dew, Iroquois, and Delicious 51. Plant Dis 76:162–166
Zink FW, Thomas CE (1990) Genetics of resistance to Fusarium oxysporum f. sp. melonis races 0, 1, and 2 in melon line MR-1. Phytopathology 80:1230–1232
Zuniga TL, Zitter TA, Gordon TR et al (1997) Characterization of pathogenic races of Fusarium oxysporum f.sp. melonis causing fusarium wilt of melon in New York. Plant Dis 81:592–596. https://doi.org/10.1094/pdis.1997.81.6.592
Acknowledgements
This research used resources provided by the SCINet project of the USDA Agricultural Research Service, ARS project number 0500-00093-001-00-D.
Funding
This study was funded, in part, by the United States Department of Agriculture (USDA) project number 6080-22000-028-00 and the National Institute of Food and Agriculture, Specialty Crops Research Initiative project number 6080-21000-018-08.
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The experiment conducted complies with the laws of the United States.
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Communicated by Sanwen Huang.
Electronic supplementary material
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122_2017_3039_MOESM1_ESM.csv
Supplementary material 1 (CSV 4 kb) Online resource 1 Disease severity line means (dsLineMeans), best linear unbiased predictors of disease severity (dsBLUPs), and line means within each test (dsTest1 and dsTest2) for the MR-1 x AY RIL population and parents
122_2017_3039_MOESM2_ESM.csv
Supplementary material 2 (CSV 150 kb) Online resource 2 Linkage groups (LG) and genetic positions (cM) of 5,747 binned SNPs (named as “S”chromosome”_“physical position in base pairs) prior to the removal of misaligned SNPs
122_2017_3039_MOESM3_ESM.csv
Supplementary material 3 (CSV 2180 kb) Online resource 3 Genotypes (AA indicates alleles contributed by MR-1 and BB by AY), linkage group (LG), genetic position (cM), chromosome (CS), physical position (Mb), and p value from a χ2 test of deviations from expected segregation ratios (P value) for the 5,663 binned SNPs used to generate the MR-1 x AY genetic linkage map
122_2017_3039_MOESM4_ESM.csv
Supplementary material 4 (CSV 58 kb) Online resource 4 Chromosome (cs), start and stop position (in bp), strand designation, and functional descriptors for genes found within the 1.5-LOD intervals of Fusarium oxysporum f.sp. melonis race 1 resistance QTLs
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Branham, S.E., Levi, A., Katawczik, M. et al. Construction of a genome-anchored, high-density genetic map for melon (Cucumis melo L.) and identification of Fusarium oxysporum f. sp. melonis race 1 resistance QTL. Theor Appl Genet 131, 829–837 (2018). https://doi.org/10.1007/s00122-017-3039-5
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DOI: https://doi.org/10.1007/s00122-017-3039-5