ORIGINAL ARTICLE
Genome-wide association analysis of resistance to Pythium ultimum in common bean (Phaseolus vulgaris)
Isaac Onziga Dramadri,
Winnyfred Amongi,
James D. Kelly,
Clare Mugisha Mukankusi,
Corresponding Author
Isaac Onziga Dramadri
Department of Agricultural Production, Collage of Agriculture and Environmental Sciences, Makerere University Regional Centre for Crop Improvement (MaRCCI), Kampala, Uganda
Correspondence
Isaac Onziga Dramadri, Department of Agricultural Production, Collage of Agriculture and Environmental Sciences, Makerere University Regional Centre for Crop Improvement (MaRCCI), Kampala, Uganda.
Email: onzigaisaac@gmail.com; dramadri@msu.edu
Search for more papers by this authorWinnyfred Amongi
International Center for Tropical Agriculture (CIAT), Kampala, Uganda
Search for more papers by this authorJames D. Kelly
Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, MI, USA
Search for more papers by this authorClare Mugisha Mukankusi
International Center for Tropical Agriculture (CIAT), Kampala, Uganda
Search for more papers by this authorIsaac Onziga Dramadri,
Winnyfred Amongi,
James D. Kelly,
Clare Mugisha Mukankusi,
Corresponding Author
Isaac Onziga Dramadri
Department of Agricultural Production, Collage of Agriculture and Environmental Sciences, Makerere University Regional Centre for Crop Improvement (MaRCCI), Kampala, Uganda
Correspondence
Isaac Onziga Dramadri, Department of Agricultural Production, Collage of Agriculture and Environmental Sciences, Makerere University Regional Centre for Crop Improvement (MaRCCI), Kampala, Uganda.
Email: onzigaisaac@gmail.com; dramadri@msu.edu
Search for more papers by this authorWinnyfred Amongi
International Center for Tropical Agriculture (CIAT), Kampala, Uganda
Search for more papers by this authorJames D. Kelly
Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, MI, USA
Search for more papers by this authorClare Mugisha Mukankusi
International Center for Tropical Agriculture (CIAT), Kampala, Uganda
Search for more papers by this authorAbstract
Pythium root rot (PRR) caused by Pythium spp. is an important root rot disease affecting common bean productivity. The objective of this study was to conduct a genome-wide association analysis of resistance to PRR in the common bean of Andean gene pool using single nucleotide polymorphism (SNP) markers. About 260 genotypes of the Andean diversity panel (ADP) were evaluated under screen house conditions using Pythium ultimum isolate MS61 in Uganda. Sixteen significant signals for resistance to PRR were detected on chromosomes Pv01, Pv02, Pv04, Pv05 and Pv09 using 260K GBS-based and 6K Beadchip SNPs. Common significant signals were detected on Pv02 and Pv09 for PRR. Positional candidate genes associated with significant SNPs on Pv02 were Phvul.002G119700, 16.97 kb near marker S02_25507837 (25.50 Mb), encoding Subtilase family protein, and Phvul.002G278400 near marker ss715645959 (44.79 Mb) encoding Defensin-like (DEFL) protein involved in plant defence responses. Based on the relatively high heritability estimates observed for PRR in this study, significant SNP markers associated with genomic regions for resistance to PRR could be validated for marker-assisted breeding in Andean beans.
Supporting Information
| Filename | Description |
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| pbr12855-sup-0001-FigS1-S3.pdfPDF document, 218.1 KB | Fig S1-S3 |
| pbr12855-sup-0002-TableS1-S4.xlsapplication/excel, 80 KB | Table S1-S4 |
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REFERENCES
- Abawi, G. S., Pastor Corrales, M. A. (1990). Root rots of beans in Latin America and Africa: Diagnosis, research methodologies, and management strategies. Cali, Colombia: Centro Internacional de Agricultura Tropical (CIAT). p. 114. (CIAT publication no. 35).
- Abawi, G. S., Ludwig, J. W., & Gugino, B. K. (2006). Bean root rot evaluation protocols currently used in New York. Annual Report-Bean Improvement Cooperative, 49, 83.
- Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). Fitting Linear Mixed-Effects Models Usinglme4. Journal of Statistical Software, 67(1). http://dx.doi.org/10.18637/jss.v067.i01
- Beebe, S. E., Rao, I. M., Devi, M. J., & Polania, J. (2014). Common beans, biodiversity, and multiple stresses: Challenges of drought resistance in tropical soils. Crop and Pasture Science, 65(7), 667–675. https://doi.org/10.1071/CP13303
- Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal statistical society: series B (Methodological), 57(1), 289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x
- Bradbury, P. J., Zhang, Z., Kroon, D. E., Casstevens, T. M., Ramdoss, Y., & Buckler, E. S. (2007). TASSEL: Software for association mapping of complex traits in diverse samples. Bioinformatics, 23, 2633–2635. https://doi.org/10.1093/bioinformatics/btm308
- Broughton, W. J., Hernandez, G., Blair, M., Beebe, S., Gepts, P., & Vanderleyden, J. (2003). Beans (Phaseolus spp.)–Model food legumes. Plant and soil, 252(1), 55–128. https://doi.org/10.1023/A:1024146710611
- Buruchara, R. A., & Rusuku, G. (1992). Root rots in the Great lakes Region, Proceedings of the Pan-African Bean pathology working group meeting, Thika, Kenya, May 20–30, CIAT Workshop Series No. 23: 49–55.
- Cheung, F., Win, J., Lang, J. M., Hamilton, J., Vuong, H., Leach, J. E., … Buell, C. R. (2008). Analysis of the Pythium ultimum transcriptome using Sanger and Pyrosequencing approaches. BMC Genomics, 9, 542. https://doi.org/10.1186/1471-2164-9-542
- Cichy, K. A., Porch, T. G., Beaver, J. S., Cregan, P., Fourie, D., Glahn, R. P., … McClean, P. (2015). A Phaseolus vulgaris diversity panel for Andean bean improvement. Crop Science, 55, 2149–2160. https://doi.org/10.2135/cropsci2014.09.0653
- Concibido, V., Young, N., Lange, D., Denny, R., Danesh, D., & Orf, J. (1996). Targeted comparative genome analysis and qualitative mapping of a major partial-resistance gene to the soybean cyst nematode. Theoretical and Applied Genetics, 93, 234–241. https://doi.org/10.1007/BF00225751
- Devendrakumar, K. T., Li, X., & Zhang, Y. (2018). MAP kinase signalling: Interplays between plant PAMP- and effector-triggered immunity. Cellular and molecular life sciences, 75, 2981–2989. https://doi.org/10.1007/s00018-018-2839-3
- Dickson, M. H., & Abawi, G. S. (1974). Resistance to Pythium ultimum in white-seeded beans (Phaseolus vulgaris). Plant Diseases Report, 58, 77–776.
- Diniz, A. L., Giordani, W., Costa, Z. P., Margarido, G. R., Perseguini, J. M. K., Benchimol-Reis, L. L., … Vieira, M. L. C. (2019). Evidence for strong kinship influence on the extent of linkage disequilibrium in cultivated common beans. Genes, 10(1), 5. https://doi.org/10.3390/genes10010005
- Figueiredo, A., Monteiro, F., & Sebastiana, M. (2014). Subtilisin-like proteases in plant–pathogen recognition and immune priming: A perspective. Frontiers in plant science, 5, 739. https://doi.org/10.3389/fpls.2014.00739
- Gepts, P., Aragão, F. J., De Barros, E., Blair, M. W., Brondani, R., Broughton, W., … McClean, P. (2008). Genomics of Phaseolus beans, a major source of dietary protein and micronutrients in the tropics. In P. H. Moore & R. Ming (Eds.), Genomics of tropical crop plants, Plant Genetics and Genomics: Crops and Models. (Vol. 1, pp. 113–143). New York, NY: Springer. https://doi.org/10.1007/978-0-387-71219-2_5
- Gichuru, V., Buruchara, R., & Okori, P. (2016). Pathogenic and molecular characterisation of Pythium spp. inducing root rot symptoms in other crops intercropped with beans in Southwestern Uganda. Journal of Applied Biosciences, 104, 9955–9964. https://doi.org/10.4314/jab.v104i1.8
10.4314/jab.v104i1.8 Google Scholar
- Goodstein, D. M., Shu, S., Howson, R., Neupane, R., Hayes, R. D., Fazo, J., … Rokhsar, D. S. (2012). Phytozome: A comparative platform for green plant genomics. Nucleic acids research, 40(D1), D1178–D1186. https://doi.org/10.1093/nar/gkr944
- Graham, R. D., Welch, R. M., Saunders, D. A., Ortiz-Monasterio, I., Bouis, H. E., Bonierbale, M., … Meisner, C. A. (2007). Nutritious subsistence food systems. Advances in Agronomy, 92, 1–74. https://doi.org/10.1016/S0065-2113(04)92001-9
- Hagerty, C. H., Cuesta-Marcos, A., Cregan, P. B., Song, Q., McClean, P., Noffsinger, S., & Myers, J. R. (2015). Mapping Fusarium solani and Aphanomyces euteiches root rot resistance and root architecture quantitative trait loci in common bean. Crop Science, 55(5), 1969–1977. https://doi.org/10.2135/cropsci2014.11.0805
- Hoyos-Villegas, V., Song, Q., & Kelly, J. D. (2017). Genome-wide association analysis for drought tolerance and associated traits in common bean. The Plant Genome, 10, 1. https://doi.org/10.3835/plantgenome2015.12.0122
- Ingvarsson, P. K., & Street, N. R. (2011). Association genetics of complex traits in plants. New Phytologist, 189(4), 909–922. https://doi.org/10.1111/j.1469-8137.2010.03593.x
- Kamfwa, K., Cichy, K. A., & Kelly, J. D. (2015). Genome-wide association study of agronomic traits in common bean. The Plant Genome, 8, 2. https://doi.org/10.3835/plantgenome2014.09.0059
- Kamfwa, K., Mwala, M., Okori, P., Gibson, P., & Mukankusi, C. (2013). Identification of QTL for Fusarium root rot resistance in common bean. Journal of crop improvement, 27(4), 406–418. https://doi.org/10.1080/15427528.2013.786775
10.1080/15427528.2013.786775 Google Scholar
- Katuuramu, D. N., Hart, J. P., Porch, T. G., Grusak, M. A., Glahn, R. P., & Cichy, K. A. (2018). Genome-wide association analysis of nutritional composition-related traits and iron bioavailability in cooked dry beans (Phaseolus vulgaris L.). Molecular Breeding, 38(4), 44. https://doi.org/10.1007/s11032-018-0798-x
- Kelly, J. D., Gepts, P., Miklas, P. N., & Coyne, D. P. (2003). Tagging and mapping of genes and QTL and molecular marker-assisted selection for traits of economic importance in bean and cowpea. Field Crops Research, 82(2–3), 135–154. https://doi.org/10.1016/S0378-4290(03)00034-0
- Klepadlo, M., Balk, C. S., Vuong, T. D., Dorrance, A. E., & Nguyen, H. T. (2019). Molecular characterization of genomic regions for resistance to Pythium ultimum var. ultimum in the soybean cultivar Magellan. Theoretical and applied genetics, 132(2), 405–417. https://doi.org/10.1007/s00122-018-3228-x
- Lévesque, C. A., Brouwer, H., Cano, L., Hamilton, J. P., Holt, C., Huitema, E., … Buell, C. R. (2010). Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biology, 11, R73. https://doi.org/10.1186/gb-2010-11-7-r73
- Lipka, A. E., Tian, F., Wang, Q., Peiffer, J., Li, M., Bradbury, P. J., … Zhang, Z. (2012). GAPIT: Genome association and prediction integrated tool. Bioinformatics, 28(18), 2397–2399. https://doi.org/10.1093/bioinformatics/bts444
- Loiselle, B. A., Sork, V. L., Nason, J., & Graham, C. (1995). Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (RuBIACEAE). American Journal of Botany, 82, 1420–1425. https://doi.org/10.1002/j.1537-2197.1995.tb12679.x
- MacQueen, A. H., White, J. W., Lee, R., Osorno, J. M., Schmutz, J., Miklas, P. N., … Juenger, T. E. (2020). Genetic Associations in Four Decades of Multienvironment Trials Reveal Agronomic Trait Evolution in Common Bean. Genetics, 215(1), 267–284. https://doi.org/10.1534/genetics.120.303038
- Mahuku, G., Navia, M., Buruchara, R., Matta, A., & Otsyula, R. (2007). Development of PCR markers tightly linked to Pyult1, a gene that confers Pythium root rot resistance in the common bean genotype AND 1062. In Phytopathology (Vol. 97(7), p. S69). 3340 Pilot Knob Road, St Paul, Mn 55121 USA: Amer Phytopathological Soc.
- Mahuku, G. S., Buruchara, R. A., Navia, U. M., & Otsyina, R. M. (2005). A gene that confers resistance to Pythium root rot in common bean: Genetic characterization and development of molecular markers [poster] [on line]. Cali, Colombia: Centro Internacional de Agricultura Tropical (CIAT). p. 1.
- Mangin, B., Siberchicot, A., Nicolas, S., Doligez, A., This, P., & Cierco-Ayrolles, C. (2012). Novel measures of linkage disequilibrium that correct the bias due to population structure and relatedness. Heredity, 108, 285–291. https://doi.org/10.1038/hdy.2011.73
- McClean, P. E., Mamidi, S., McConnell, M., Chikara, S., & Lee, R. (2010). Synteny mapping between common bean and soybean reveals extensive blocks of shared loci. BMC Genomics, 11(1), 184. https://doi.org/10.1186/1471-2164-11-184
- Moghaddam, S. M., Mamidi, S., Osorno, J. M., Lee, R., Brick, M., Kelly, J., … McClean, P. E. (2016). Genome-wide association study identifies candidate loci underlying agronomic traits in a middle American diversity panel of common bean. Plant Genome, 9, 1–21. https://doi.org/10.3835/plantgenome2016.02.0012
- Mukalazi, J., Buruchara, R., Adipala, E., Carder, J., Opio, F., Pettitt, T., & Spence, N. (2002). Characterization of Pythium species pathogenic to common beans in Uganda. Presentation at: International Conference on Integrated Pest Management for Sub-Saharan Africa. 8-12 September 2002, Kampala, Uganda.[Poster].
- Mukalazi, J., Books, R.U.F.O.R.U.M., OER, R., SCARDA, R. and Tenders, R.U.F.O.R.U.M. (2004). Pathogen variation and quantification of Pythium species in bean fields in Uganda (Doctoral dissertation, PhD Thesis). Kampala, Uganda: Makerere University.
- Mukankusi, C. M., Amongi, W., Sebuliba, S., Musoke, S., & Acam, C. (2018). Characterization of Phaseolus coccineus interspecific germplasm accessions for disease resistance, grain market class and yield attributes. African Crop Science Journal, 26(1), 117–135. https://doi.org/10.4314/acsj.v26i1.9
10.4314/acsj.v26i1.9 Google Scholar
- Mukankusi, C., Derera, J., Melis, R., Gibson, P. T., & Buruchara, R. (2011). Genetic analysis of resistance to Fusarium root rot in common bean. Euphytica, 182(1), 11. https://doi.org/10.1007/s10681-011-0413-2
- Nakedde, T., Ibarra-Perez, F. J., Mukankusi, C., Waines, J. G., & Kelly, J. D. (2016). Mapping of QTL associated with Fusarium root rot resistance and root architecture traits in black beans. Euphytica, 212(1), 51–63. https://doi.org/10.1007/s10681-016-1755-6
- Namayanja, A., Msolla, S. N., Buruchara, R., & Namusoke, A. (2014). Genetic analysis of resistance to Pythium root rot disease in Common Bean (Phaseolus vulgaris L.) genotypes. Journal of Crop Improvement, 28(2), 184–202. https://doi.org/10.1080/15427528.2013.863815
- Navarro, F., Sass, M. E., & Nienhuis, J. (2008). Identification and confirmation of quantitative trait loci for root rot resistance in snap bean. Crop Science, 48(3), 962–972. https://doi.org/10.2135/cropsci2007.02.0113
- Nicoli, A., Zambolim, L., Paula Júnior, T. J., Vieira, R. F., Teixeira, H., & Carneiro, J. E. S. (2012). Resistance of advanced common bean lines to Fusarium root rot. Tropical Plant Pathology, 37(6), 393–398. https://doi.org/10.1590/S1982-56762012000600003
- Nzungize, J., Gepts, P., Buruchara, R., Male, A., Ragama, P., Busogoro, J. P., & Baudoin, J. P. (2011). Introgression of Pythium root rot resistance gene into Rwandan susceptible common bean cultivars. African Journal of Plant Science, 5(3), 193–200. ISSN: 1996–0824.
- Nzungize, J. R., Lyumugabe, F., Busogoro, J. P., & Baudoin, J. P. (2012). Pythium root rot of common bean: biology and control methods. A review. BASE.
- Obala, J., Mukankusi, C., Rubaihayo, P. R., Gibson, P., & Edema, R. (2012). Improvement of resistance to fusarium root rot through gene pyramiding in common bean. African Crop Science Journal, 20(1), 1–13. ISSN 1021–9730/2012.
- Oladzad, A., Porch, T., Rosas, J. C., Moghaddam, S. M., Beaver, J., Beebe, S. E., … Ratz, B. (2019). Single and multi-trait GWAS identify genetic factors associated with production traits in common bean under abiotic stress environments. G3: Genes, Genomes, Genetics, 9(6), 1881–1892. https://doi.org/10.1534/g3.119.400072
- Oladzad, A., Zitnick-Anderson, K., Jain, S., Simons, K., Osorno, J. M., McClean, P. E., & Pasche, J. (2019). Genotypes and genomic regions associated with rhizoctonia solani resistance in common bean. Frontiers in plant science, 10, 956. https://doi.org/10.3389/fpls.2019.00956
- Ongom, P. O., Nkalubo, S. T., Gibson, P. T., Mukankusi, C. M., & Rubaihayo, P. R. (2012). Evaluating genetic association between Fusarium and Pythium root rots resistances in the bean genotype RWR 719. African Crop Science Journal, 20(1), 31–39. ISSN 1021–9730/2012.
- Otsyula, R. M., Buruchara, R. A., Mahuku, G., & Rubaihayo, P. (2003). Inheritance and transfer of root rot (Pythium) resistance to bean genotypes. African Crop Science Society, 6, 295–298.
- Paparu, P., Acur, A., Kato, F., Acam, C., Nakibuule, J., Musoke, S., … Mukankusi, C. (2018). Prevalence and incidence of four common bean root rots in Uganda. Experimental Agriculture, 54(6), 888–900. https://doi.org/10.1017/S0014479717000461
- Price, A. L., Patterson, N. J., Plenge, R. M., Weinblatt, M. E., Shadick, N. A., & Reich, D. (2006). Principal components analysis corrects for stratification in genome-wide association studies. Nature Genetics, 38, 904–909. https://doi.org/10.1038/ng1847
- Qin, J., Song, Q., Shi, A., Li, S., Zhang, M., & Zhang, B. (2017). Genome-wide association mapping of resistance to Phytophthora sojae in a soybean [Glycine max (L.) Merr.] germplasm panel from maturity groups IV and V. PLoS One, 12(9), e0184613. https://doi.org/10.1371/journal.pone.0184613
- Resende, R. T., de Resende, M. D. V., Azevedo, C. F., eSilva, F. F., Melo, L. C., Pereira, H. S., … Vianello, R. P. (2018). Genome-wide association and regional heritability mapping of plant architecture, lodging and productivity in Phaseolus vulgaris. G3: Genes, Genomes, Genetics, 8(8), 2841–2854. https://doi.org/10.1534/g3.118.200493
- Richard, M. M., Pflieger, S., Sévignac, M., Thareau, V., Blanchet, S., Li, Y., … Geffroy, V. (2014). Fine mapping of Co-x, an anthracnose resistance gene to a highly virulent strain of Colletotrichum lindemuthianum in common bean. Theoretical and Applied Genetics, 127(7), 1653–1666. https://doi.org/10.1007/s00122-014-2328-5
- Román-Avilés, B., & Kelly, J. D. (2005). Identification of quantitative trait loci conditioning resistance to Fusarium root rot in common bean. Crop Science, 45(5), 1881–1890. https://doi.org/10.2135/cropsci2005.0028
- SAS Institute Inc. (2015). Base SAS 9.4 procedures guide, 5th ed. Cary, NC: SAS Institute Inc. Available: http://support.sas.com
- Schoonhoven, A. V., & Pastor-Corrales, M. A. (1987). Standard system for the evaluation of bean germplasm (p. 56). Cali, Colombia: CIAT.
- Schmutz, J., McClean, P. E., Mamidi, S., Wu, G. A., Cannon, S. B., Grimwood, J., … Jackson, S. A. (2014). A reference genome for common bean and genome-wide analysis of dual domestications. Nature Genetics, 46, 707–713. https://doi.org/10.1038/ng.3008
- Schwarz, G. (1978). Estimating the dimension of a model. The Annals of Statistics, 6, 461–464.
- Soltani, A., MafiMoghaddam, S., Oladzad-Abbasabadi, A., Walter, K., Kearns, P. J., Vasquez-Guzman, J., … Chilivers, M. I. (2018). Genetic analysis of flooding tolerance in an Andean diversity panel of dry bean (Phaseolus vulgaris L.). Frontiers in Plant Science, 9, 767. https://doi.org/10.3389/fpls.2018.00767
- Song, Q., Jia, G., Hyten, D. L., Jenkins, J., Hwang, E. Y., Schroeder, S. G., … Cregan, P. B. (2015). SNP assay development for linkage map construction, anchoring whole-genome sequence, and other genetic and genomic applications in common bean. G3: Genes, Genomes, Genetics, 5(11), 2285–2290. https://doi.org/10.1534/g3.115.020594
- Spence, N. (2009). Characterisation and epidemiology of root rot diseases caused by Fusarium and Pythium spp. in beans in Uganda. Final Technical Report.
- Sun, G., Zhu, C., Kramer, M. H., Yang, S. S., Song, W., Piepho, H. P., & Yu, J. (2010). Variation explained in mixed-model association mapping. Heredity, 105, 333–340. https://doi.org/10.1038/hdy.2010.11
- Tu, J. C., & Park, S. J. (1993). Root-rot resistance in common bean. Canadian Journal of Plant Science, 73(1), 365–367. https://doi.org/10.4141/cjps2013-416
- Tusiime, G. (2003). Variation and detection of Fusarium solani f. sp. phaseoli and quantification of soil inoculum in common bean fields (Doctoral dissertation, Dissertation). Kampala, Uganda: Makerere University.
- Vlasova, A., Capella-Gutiérrez, S., Rendón-Anaya, M., Hernández-Oñate, M., Minoche, A. E., Erb, I., … Westergaard, G. (2016). Genome and transcriptome analysis of the Mesoamerican common bean and the role of gene duplications in establishing tissue and temporal specialization of genes. Genome Biology, 17(1), 32. https://doi.org/10.1186/s13059-016-0883-6
- Wang, W., Jacobs, J. L., Chilvers, M. I., Mukankusi, C. M., Kelly, J. D., & Cichy, K. A. (2018). QTL analysis of Fusarium root rot resistance in an Andean× middle American common bean RIL population. Crop Science, 58(3), 1166–1180. https://doi.org/10.2135/cropsci2017.10.0608
- Wang, Y., Tyler, B. M., & Wang, Y. (2019). Defense and counterdefense during plant-pathogenic oomycete infection. Annual Review of Microbiology, 73, 667–696. https://doi.org/10.1146/annurev-micro-020518-120022
- Wen, L., Chang, H. X., Brown, P. J., Domier, L. L., & Hartman, G. L. (2019). Genome-wide association and genomic prediction identifies soybean cyst nematode resistance in common bean including a syntenic region to soybean Rhg1 locus. Horticulture Research, 6(1), 1–12. https://doi.org/10.1038/s41438-018-0085-3
- Wortmann, C. S. (1998). Atlas of common bean (Phaseolus vulgaris L.) production in Africa, Cali, Colombia: CIAT. (No. 297).
- York, D. W., Dickson, M. H., & Abawi, G. S. (1977). Inheritance of resistance to seed decay and pre-emergence damping-off in snap beans caused by Pythium ultimum. Plant Disease Report, 61, 285–289.
- Yu, J., Pressoir, G., Briggs, W. H., Vroh, Bi I., Yamasaki, M., Doebley, J. F., … Buckler, E. S. (2006). A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nature Genetics, 38, 203–208. https://doi.org/10.1038/ng1702
- Zhang, Z., Ersoz, E., Lai, C. Q., Todhunter, R. J., Tiwari, H. K., Gore, M. A., … Buckler, E. S. (2010). Mixed linear model approach adapted for genome-wide association studies. Nature Genetics, 42(4), 355. https://doi.org/10.1038/ng.546
- Zhu, C., Gore, M., Buckler, E. S., & Yu, J. (2008). Status and prospects of association mapping in plants. The Plant Genome, 1(1), 5–20. https://doi.org/10.3835/plantgenome2008.02.0089
