Genome-wide association and epistasis studies unravel the genetic architecture of sudden death syndrome resistance in soybean

Plant Journal

Volumn 84, Issue 6, 2015, Pages 1124-1136

  Zhang, Jiaoping ^a   Singh, Arti ^a   Mueller, Daren S ^a   Singh, Asheesh K ^a  

^a IOWA STATE UNIVERSITY   (United States)

Author keywords

epistatic interaction; genome wide association study; Glycine max (L.) Merr.; linkage disequilibrium; plant defense; SNP SNP interaction; sudden death syndrome

Indexed keywords

AMINO ACIDS; ASSOCIATION REACTIONS; ENCODING (SYMBOLS); ENZYMES; GENES;

EPISTATIC INTERACTIONS; GENOME-WIDE ASSOCIATION STUDIES; GLYCINE MAX (L.) MERR; LINKAGE DISEQUILIBRIUM; PLANT DEFENSE; SNP-SNP INTERACTION; SUDDEN DEATH SYNDROMES;

NITROGEN FIXATION;

GENETIC MARKER; PLANT PROTEIN;

EPISTASIS; FUSARIUM; GENE LINKAGE DISEQUILIBRIUM; GENETIC MARKER; GENETIC VARIATION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; SOYBEAN;

EPISTASIS, GENETIC; FUSARIUM; GENETIC MARKERS; GENETIC VARIATION; GENOME-WIDE ASSOCIATION STUDY; LINKAGE DISEQUILIBRIUM; PLANT DISEASES; PLANT PROTEINS; SOYBEANS;

EID: 84961302171     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.13069     Document Type: Article

References (66)

1. Abdelmajid, K.M., Ramos, L., Leandro, L., Mbofung, G., Hyten, D.L., Kantartzi, S.K., Grier, R.L., Njiti, V.N., Cianzio, S., and, Meksem, K., (2012) The 'PI 438489B' by 'Hamilton' SNP-based genetic linkage map of soybean [Glycine max (L.) Merr.] identified quantitative trait loci that underlie seedling SDS resistance. J. Plant Genome Sci. 1, 18-30.
2. Abeysekara, N.S., and, Bhattacharyya, M.K., (2014) Analyses of the xylem sap proteomes identified candidate Fusarium virguliforme proteinacious toxins. PLoS ONE, 9, e93667.
3. Abouzeid, H., Boisset, G., Favez, T., et al. (2011) Mutations in the SPARC-related modular calcium-binding protein 1 gene, SMOC1, cause Waardenburg anophthalmia syndrome. Am. J. Hum. Genet. 88, 92-98.
4. Arahana, V.S., Graef, G.L., Specht, J.E., Steadman, J.R., and, Eskridge, K.M., (2001) Identification of QTLs for resistance to Sclerotinia sclerotiorum in soybean. Crop Sci. 41, 180-188.
5. Bastien, M., Sonah, H., and, Belzile, F., (2014) Genome-wide association mapping of Sclerotinia sclerotiorum resistance in soybean with a genotyping-by-sequencing approach. Plant Genome, 7 (10), 3835.
6. Bates, D., Maechler, M., and, Bolker, B., (2012) lme4: linear mixed-effects models using using 'Eigen' and S4 [WWW document]. URL http://CRAN.R-project.org/package#x003D;lme4 [accessed on 13 November 2015].
7. Browning, B.L., and, Browning, S.R., (2007) Efficient multilocus association testing for whole genome association studies using localized haplotype clustering. Genet. Epidemiol. 31, 365-375.
8. Browning, B.L., and, Browning, S.R., (2009) A unified approach to genotype imputation and haplotype-phase inference for large data sets of trios and unrelated individuals. Am. J. Hum. Genet. 84, 210-223.
9. Brzostowski, L., Schapaugh, W., Rzodkiewicz, P., Todd, T., and, Little, C., (2014) Effect of host resistance to Fusarium virguliforme and Heterodera glycines on sudden death syndrome disease severity and soybean yield. Plant Health Prog. 15, 1.
10. Chang, S.J.C., Doubler, T.W., Kilo, V., Suttner, R., Klein, J., Schmidt, M.E., Gibson, P.T., and, Lightfoot, D.A., (1996) Two additional loci underlying durable field resistance to soybean sudden death syndrome (SDS). Crop Sci. 36, 1684-1688.
11. Cianzio, S.R., Bhattacharyya, M.K., Swaminathan, S., Westgate, G.M., Gebhart, G., Rivera-Velez, N., Lundeen, P., Van der Molen, K., and, Pruski, T.I., (2014) Registration of AR10SDS soybean germplasm partially resistant to sudden death syndrome and resistant to soybean cyst nematode. J. Plant Regist. 8, 200-210.
12. De Coninck, B., Timmermans, P., Vos, C., Cammue, B.P.A., and, Kazan, K., (2015) What lies beneath: belowground defense strategies in plants. Trends Plant Sci. 20, 91-101.
13. Farm, P.P.S., (1995) Occurrence of soybean sudden death syndrome in east-central Illinois and associated yield losses. Plant Dis. 79, 315.
14. Gou, X., He, K., Yang, H., Yuan, T., Lin, H., Clouse, S.D., and, Li, J., (2010) Genome-wide cloning and sequence analysis of leucine-rich repeat receptor-like protein kinase genes in Arabidopsis thaliana. BMC Genom. 11, 19.
15. Graham, M.A., Marek, L.F., and, Shoemaker, R.C., (2002) Organization, expression and evolution of a disease resistance gene cluster in soybean. Genetics, 162, 1961-1977.
16. Hartman, G., Huang, Y., Nelson, R., and, Noel, G., (1997) Germplasm evaluation of Glycine max for resistance to Fusarium solani, the causal organism of sudden death syndrome. Plant Dis. 81, 515-518.
17. Hartman, G., Chang, H.-X., and, Leandro, L., (2015) Research advances and management of soybean sudden death syndrome. Crop Prot. 73, 60-66.
18. Hayes, A.J., Jeong, S.C., Gore, M.A., Yu, Y.G., Buss, G.R., Tolin, S.A., and, Maroof, M.A.S., (2004) Recombination within a nucleotide-binding-site/leucine-rich-repeat gene cluster produces new variants conditioning resistance to soybean mosaic virus in soybeans. Genetics, 166, 493-503.
19. Heil, M., and, Bostock, R.M., (2002) Induced systemic resistance (ISR) against pathogens in the context of induced plant defences. Ann. Bot. 89, 503-512.
20. Hnetkovsky, N., Chang, S.J.C., Doubler, T.W., Gibson, P.T., and, Lightfoot, D.A., (1996) Genetic mapping of loci underlying field resistance to soybean sudden death syndrome (SDS). Crop Sci. 36, 393-400.
21. Hu, X., Liu, Q., Zhang, Z., Li, Z., Wang, S., He, L., and, Shi, Y., (2010) SHEsisEpi, a GPU-enhanced genome-wide SNP-SNP interaction scanning algorithm, efficiently reveals the risk genetic epistasis in bipolar disorder. Cell Res. 20, 854-857.
22. Huang, X.H., Wei, X.H., Sang, T., et al. (2010) Genome-wide association studies of 14 agronomic traits in rice landraces. Nat. Genet. 42, 961-976.
23. Hwang, E.Y., Song, Q., Jia, G., Specht, J.E., Hyten, D.L., Costa, J., and, Cregan, P.B., (2014) A genome-wide association study of seed protein and oil content in soybean. BMC Genom. 15, 1.
24. Jones, D.A., and, Jones, J., (1997) The role of leucine-rich repeat proteins in plant defences. Adv. Bot. Res. 24, 89-167.
25. Kang, Y., Kim, K., Shim, S., Yoon, M., Sun, S., Kim, M., Van, K., and, Lee, S.-H., (2012) Genome-wide mapping of NBS-LRR genes and their association with disease resistance in soybean. BMC Plant Biol. 12, 139.
26. Koenning, S.R., and, Wrather, J.A., (2010) Suppression of soybean yield potential in the continental United States by plant diseases from 2006 to 2009. Plant Health Prog. doi: 10.1094/PHP-2010-1122-01-RS.
27. Kump, K.L., Bradbury, P.J., Wisser, R.J., et al. (2011) Genome-wide association study of quantitative resistance to southern leaf blight in the maize nested association mapping population. Nat. Genet. 43, 163-168.
28. Lee, S., Mian, M.R., McHale, L.K., Wang, H., Wijeratne, A.J., Sneller, C.H., and, Dorrance, A.E., (2013) Novel quantitative trait loci for partial resistance to Phytophthora sojae in soybean PI 398841. Theor. Appl. Genet. 126, 1121-1132.
29. Leon, J., Rojo, E., and, Sanchez-Serrano, J.J., (2001) Wound signalling in plants. J. Exp. Bot. 52, 1-9.
30. Li, Y.H., Li, W., Zhang, C., Yang, L., Chang, R.Z., Gaut, B.S., and, Qiu, L.J., (2010) Genetic diversity in domesticated soybean (Glycine max) and its wild progenitor (Glycine soja) for simple sequence repeat and single-nucleotide polymorphism loci. New Phytol. 188, 242-253.
31. Lipka, A.E., Tian, F., Wang, Q.S., Peiffer, J., Li, M., Bradbury, P.J., Gore, M.A., Buckler, E.S., and, Zhang, Z.W., (2012) GAPIT: genome association and prediction integrated tool. Bioinformatics, 28, 2397-2399.
32. Liu, W.D., Liu, J.L., Triplett, L., Leach, J.E., and, Wang, G.L., (2014) Novel insights into rice innate immunity against bacterial and fungal pathogens. Annu. Rev. Phytopathol. 52, 213-241.
33. Mamidi, S., Lee, R.K., Goos, J.R., and, McClean, P.E., (2014) Genome-wide association studies identifies seven major regions responsible for iron deficiency chlorosis in soybean (Glycine max). PLoS ONE, 9, e107469.
34. Manolio, T.A., Collins, F.S., Cox, N.J., et al. (2009) Finding the missing heritability of complex diseases. Nature, 461, 747-753.
35. Mueller, D., Hartman, G., Nelson, R., and, Pedersen, W., (2002) Evaluation of Glycine max germ plasm for resistance to Fusarium solani f. sp. glycines. Plant Dis. 86, 741-746.
36. Mueller, D., Nelson, R., Hartman, G., and, Pedersen, W., (2003) Response of commercially developed soybean cultivars and the ancestral soybean lines to Fusarium solani f. sp. glycines. Plant Dis. 87, 827-831.
37. Nagy, S., Poczai, P., Cernak, I., Gorji, A.M., Hegedus, G., and, Taller, J., (2012) PICcalc: an online program to calculate polymorphic information content for molecular genetic studies. Biochem. Genet. 50, 670-672.
38. Njiti, V., Suttner, R., Gray, L., Gibson, P., and, Lightfoot, D., (1997) Rate-reducing resistance to Fusarium solani f. sp. phaseoli underlies field resistance to soybean sudden death syndrome. Crop Sci. 37, 132-138.
39. Njiti, V.N., Meksem, K., Iqbal, M.J., Johnson, J.E., Kassem, M.A., Zobrist, K.F., Kilo, V.Y., and, Lightfoot, D.A., (2002) Common loci underlie field resistance to soybean sudden death syndrome in Forrest, Pyramid, Essex, and Douglas. Theor. Appl. Genet. 104, 294-300.
40. Ouyang, S.Q., Liu, Y.F., Liu, P., Lei, G., He, S.J., Ma, B., Zhang, W.K., Zhang, J.S., and, Chen, S.Y., (2010) Receptor-like kinase OsSIK1 improves drought and salt stress tolerance in rice (Oryza sativa) plants. Plant J. 62, 316-329.
41. Park, K.Y., Jung, J.Y., Park, J., Hwang, J.U., Kim, Y.W., Hwang, I., and, Lee, Y., (2003) A role for phosphatidylinositol 3-phosphate in abscisic acid-induced reactive oxygen species generation in guard cells. Plant Physiol. 132, 92-98.
42. Pennell, R.I., and, Lamb, C., (1997) Programmed cell death in plants. Plant Cell, 9, 1157-1168.
43. Poland, J.A., Bradbury, P.J., Buckler, E.S., and, Nelson, R.J., (2011) Genome-wide nested association mapping of quantitative resistance to northern leaf blight in maize. Proc. Natl Acad. Sci. USA, 108, 6893-6898.
44. Prabhu, S., and, Pe'er, I., (2012) Ultrafast genome-wide scan for SNP-SNP interactions in common complex disease. Genome Res. 22, 2230-2240.
45. Purcell, S., Neale, B., Todd-Brown, K., et al. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559-575.
46. Remington, D.L., Thornsberry, J.M., Matsuoka, Y., Wilson, L.M., Whitt, S.R., Doebley, J., Kresovich, S., Goodman, M.M., and, Buckler, E.S.t., (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc. Natl Acad. Sci. USA, 98, 11479-11484.
47. Roy, K.W., Rupe, J.C., Hershman, D.E., and, Abney, T.S., (1997) Sudden death syndrome of soybean. Plant Dis. 81, 1100-1111.
48. Rupe, J., Gbur, E., and, Marx, D., (1991) Cultivar responses to sudden death syndrome of soybean. Plant Dis. 75, 47-50.
49. Schmutz, J., Cannon, S.B., Schlueter, J., et al. (2010) Genome sequence of the palaeopolyploid soybean. Nature, 463, 178-183.
50. Singh, A., Knox, R.E., DePauw, R.M., Singh, A.K., Cuthbert, R.D., Campbell, H.L., Singh, D., Bhavani, S., Fetch, T., and, Clarke, F., (2013) Identification and mapping in spring wheat of genetic factors controlling stem rust resistance and the study of their epistatic interactions across multiple environments. Theor. Appl. Genet. 126, 1951-1964.
51. Sonah, H., O'Donoughue, L., Cober, E., Rajcan, I., and, Belzile, F., (2015) Identification of loci governing eight agronomic traits using a GBS-GWAS approach and validation by QTL mapping in soya bean. Plant Biotechnol. J. 13, 211-221.
52. Song, Q.J., Hyten, D.L., Jia, G.F., Quigley, C.V., Fickus, E.W., Nelson, R.L., and, Cregan, P.B., (2013) Development and evaluation of SoySNP50K, a high-density genotyping array for soybean. PLoS ONE, 8, e54985.
53. Srour, A., Afzal, A.J., Blahut-Beatty, L,. et al. (2012) The receptor like kinase at Rhg1-a/Rfs2 caused pleiotropic resistance to sudden death syndrome and soybean cyst nematode as a transgene by altering signaling responses. BMC Genom. 13, 368.
54. Staskawicz, B.J., Ausubel, F.M., Baker, B.J., Ellis, J.G., and, Jones, J.D.G., (1995) Molecular genetics of plant disease resistance. Science, 268, 661-667.
55. Van Loon, L.C., and, Van Strien, E.A., (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol. Mol. Plant Pathol. 55, 85-97.
56. Vorwerk, S., Somerville, S., and, Somerville, C., (2004) The role of plant cell wall polysaccharide composition in disease resistance. Trends Plant Sci. 9, 203-209.
57. Wang, H., Waller, L., Tripathy, S., St Martin, S.K., Zhou, L., Krampis, K., Tucker, D.M., Mao, Y., Hoeschele, I., and, Maroof, S., (2010) Analysis of genes underlying soybean quantitative trait loci conferring partial resistance to Phytophthora sojae. Plant Genome, 3, 23-40.
58. Wang, D., Salah El-Basyoni, I., Stephen Baenziger, P., Crossa, J., Eskridge, K.M., and, Dweikat, I., (2012a) Prediction of genetic values of quantitative traits with epistatic effects in plant breeding populations. Heredity, 109, 313-319.
59. Wang, H., St Martin, S.K., and, Dorrance, A.E., (2012b) Comparison of phenotypic methods and yield contributions of quantitative trait loci for partial resistance to Phytophthora sojae in soybean. Crop Sci. 52, 609-622.
60. Wen, Z., Tan, R., Yuan, J., et al. (2014) Genome-wide association mapping of quantitative resistance to sudden death syndrome in soybean. BMC Genom. 15, 809.
61. Wimmer, V., Albrecht, T., Auinger, H.J., and, Schon, C.C., (2012) synbreed: a framework for the analysis of genomic prediction data using R. Bioinformatics, 28, 2086-2087.
62. Woody, J.L., Severin, A.J., Bolon, Y.T., et al. (2011) Gene expression patterns are correlated with genomic and genic structure in soybean. Genome, 54, 10-18.
63. Wywial, E., and, Singh, S.M., (2010) Identification and structural characterization of FYVE domain-containing proteins of Arabidopsis thaliana. BMC Plant Biol. 10, 157.
64. Xu, S.Z., and, Jia, Z.Y., (2007) Genome-wide analysis of epistatic effects for quantitative traits in barley. Genetics, 175, 1955-1963.
65. Zhang, Z.W., Ersoz, E., Lai, C.Q., et al. (2010) Mixed linear model approach adapted for genome-wide association studies. Nat. Genet. 42, 355-360.
66. Zhang, J., Song, Q., Cregan, P.B., Nelson, R.L., Wang, X., Wu, J., and, Jiang, G.-L., (2015) Genome-wide association study for flowering time, maturity dates and plant height in early maturing soybean (Glycine max) germplasm. BMC Genom. 16, 217.