Abstract
Partial resistance to Phytophthora sojae in soybean is controlled by multiple quantitative trait loci (QTL). With traditional QTL mapping approaches, power to detect such QTL, frequently of small effect, can be limited by population size. Joint linkage QTL analysis of nested recombinant inbred line (RIL) populations provides improved power to detect QTL through increased population size, recombination, and allelic diversity. However, uniform development and phenotyping of multiple RIL populations can prove difficult. In this study, the effectiveness of joint linkage QTL analysis was evaluated on combinations of two to six nested RIL populations differing in inbreeding generation, phenotypic assay method, and/or marker set used in genotyping. In comparison to linkage analysis in a single population, identification of QTL by joint linkage analysis was only minimally affected by different phenotypic methods used among populations once phenotypic data were standardized. In contrast, genotyping of populations with only partially overlapping sets of markers had a marked negative effect on QTL detection by joint linkage analysis. In total, 16 genetic regions with QTL for partial resistance against P. sojae were identified, including four novel QTL on chromosomes 4, 9, 12, and 16, as well as significant genotype-by-isolate interactions. Resistance alleles from PI 427106 or PI 427105B contributed to a major QTL on chromosome 18, explaining 10–45 % of the phenotypic variance. This case study provides guidance on the application of joint linkage QTL analysis of data collected from populations with heterogeneous assay conditions and a genetic framework for partial resistance to P. sojae.
Similar content being viewed by others
References
Aarts N, Metz M, Holub E, Staskawicz BJ, Daniels MJ, Parker JE (1998) Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proc Natl Acad Sci USA 95:10306–10311
Bachman MS, Tamulonis JP, Nickell CD, Bent AF (2001) Molecular markers linked to brown stem rot resistance genes, Rbs1 and Rbs2, in soybean. Crop Sci 41:527–535
Beavis WD (1998) QTL analyses: power, precision, and accuracy. In: Patterson A (ed) Molecular dissection of complex traits. CRC Press, Boca Raton, pp 250–266
Blanc G, Charcosset A, Mangin B, Gallais A, Moreau L (2006) Connected populations for detecting quantitative trait loci and testing for epistasis: an application in maize. Theor Appl Genet 113:206–224
Buckler ES, Holland JB, Bradbury PJ, Acharya CB, Brown PJ, Browne C, Ersoz E, Flint-Garcia S, Garcia A, Glaubitz JC, Goodman MM, Harjes C, Guill K, Kroon DE, Larsson S, Lepak NK, Li HH, Mitchell SE, Pressoir G, Peiffer JA, Rosas MO, Rocheford TR, Romay MC, Romero S, Salvo S, Villeda HS, da Silva HS, Sun Q, Tian F, Upadyayula N, Ware D, Yates H, Yu JM, Zhang ZW, Kresovich S, McMullen MD (2009) The genetic architecture of maize flowering time. Science 325:714–718
Burnham KD, Dorrance AE, VanToai TT, Martin SKS (2003) Quantitative trait loci for partial resistance to Phytophthora sojae in soybean. Crop Sci 43:1610–1617
Buzzell RI, Anderson TR (1982) Plant loss response of soybean cultivars to Phytophthora megasperma f. sp. glycinea under field conditions. Plant Dis 66:1146–1148
Calenge F, Faure A, Goerre M, Gebhardt C, Van de Weg WE, Parisi L, Durel CE (2004) Quantitative trait loci (QTL) analysis reveals both broad-spectrum and isolate-specific QTL for scab resistance in an apple progeny challenged with eight isolates of Venturia inaequalis. Phytopathology 94:370–379
Chandler K, Lipka AE, Owens BF, Li HH, Buckler ES, Rocheford T, Gore MA (2013) Genetic analysis of visually scored orange kernel color in maize. Crop Sci 53:189–200
Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971
Cook DE, Lee TG, Guo X, Melito S, Wang K, Bayless AM, Wang J, Hughes TJ, Willis DK, Clemente TE, Diers BW, Jiang J, Hudson ME, Bent AF (2012a) Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science 338:1206–1209
Cook JP, McMullen MD, Holland JB, Tian F, Bradbury P, Ross-Ibarra J, Buckler ES, Flint-Garcia SA (2012b) Genetic architecture of maize kernel composition in the nested association mapping and inbred association panels. Plant Physiol 158:824–834
Darvishzadeh R, Kiani SP, Dechamp-Guillaume G, Gentzbittel L, Sarrafi A (2007) Quantitative trait loci associated with isolate specific and isolate nonspecific partial resistance to Phoma macdonaldii in sunflower. Plant Pathol 56:855–861
Dorrance AE, Schmitthenner AF (2000) New sources of resistance to Phytophthora sojae in the soybean plant introductions. Plant Dis 84:1303–1308
Dorrance AE, Berry SA, Anderson TR, Meharg C (2008) Isolation, storage, pathotype characterization, and evaluation of resistance for Phytophthora sojae in soybean. Plant Health Prog. doi:10.1094/PHP-2008-0118-01-DG
Flor HH (1956) The complementary genic systems in flax and flax rust. Adv Genet 8:29–54
Gaudet M, Fara AG, Sabatti M, Kuztninsky E, Mugnozza GS (2007) Single-reaction for SNP genotyping on agarose gel by allele-specific PCR in black poplar (Populus nigra L.). Plant Mol Biol Rep 25:1–9
Gonzalez AM, Marcel TC, Niks RE (2012) Evidence for a minor gene-for-minor gene interaction explaining nonhypersensitive polygenic partial disease resistance. Phytopathology 102:1086–1093
Grau CR, Dorrance AE, Bond J, Russin JS (2004) Fungal diseases. In: Boerma HR, Specht JE (eds) Soybeans: improvement, production, and uses, 3rd edn. American Society of Agronomy, Crop Science Society of America, Soil Science Society of America, Madison, pp 679–763
Guo B, Sleper DA, Arelli PR, Shannon JG, Nguyen HT (2005) Identification of QTLs associated with resistance to soybean cyst nematode races 2, 3 and 5 in soybean PI 90763. Theor Appl Genet 111:965–971
Han YP, Teng WL, Yu KF, Poysa V, Anderson T, Qiu LJ, Lightfoot DA, Li WB (2008) Mapping QTL tolerance to Phytophthora root rot in soybean using microsatellite and RAPD/SCAR derived markers. Euphytica 162:231–239
Holland JB (2007) Genetic architecture of complex traits in plants. Curr Opin Plant Biol 10:156–161
Hyten DL, Choi IY, Song QJ, Specht JE, Carter TE, Shoemaker RC, Hwang EY, Matukumalli LK, Cregan PB (2010) A high density integrated genetic linkage map of soybean and the development of a 1536 universal soy linkage panel for quantitative trait locus mapping. Crop Sci 50:960–968
Johnson R (1984) A critical analysis of durable resistance. Annu Rev Phytopathol 22:309–330
Kim HS, Diers BW (2000) Inheritance of partial resistance to Sclerotinia stem rot in soybean. Crop Sci 40:55–61
Kou YJ, Wang SP (2010) Broad-spectrum and durability: understanding of quantitative disease resistance. Curr Opin Plant Biol 13:181–185
Kou YJ, Wang SP (2012) Toward an understanding of the molecular basis of quantitative disease resistance in rice. J Biotechnol 159:283–290
Kump KL, Holland JB, Jung MT, Wolters P, Balint-Kurti PJ (2010) Joint analysis of near-isogenic and recombinant inbred line populations yields precise positional estimates for quantitative trait loci. Plant Genome 3:142–153
Kump KL, Bradbury PJ, Wisser RJ, Buckler ES, Belcher AR, Oropeza-Rosas MA, Zwonitzer JC, Kresovich S, McMullen MD, Ware D, Balint-Kurti PJ, Holland JB (2011) Genome-wide association study of quantitative resistance to southern leaf blight in the maize nested association mapping population. Nat Genet 43:163–168
Lander E, Kruglyak L (1995) Genetic dissection of complex traits—guidelines for interpreting and reporting linkage results. Nat Genet 11:241–247
Lee S, Mian MAR, McHale L, Wang H, Wijeratne A, Sneller C, Dorrance A (2013a) Novel quantitative trait loci for partial resi stance to Phytophthora sojae in soybean PI 398841. Theor Appl Genet 126:1121–1132
Lee S, Mian MAR, McHale LK, Sneller CH, Dorrance AE (2013b) Identification of quantitative trait loci conditioning partial resistance to Phytophthora sojae in soybean PI 407861A. Crop Sci 53:1022–1031
Levene H (1960) Robust tests for the equality of variance. In: Olkin I (ed) Contributions to probability and statistics. Stanford University Press, Palo Alto, pp 278–292
Li HH, Ye GY, Wang JK (2007) A modified algorithm for the improvement of composite interval mapping. Genetics 175:361–374
Li XP, Han YP, Teng WL, Zhang SZ, Yu KF, Poysa V, Anderson T, Ding JJ, Li WB (2010) Pyramided QTL underlying tolerance to Phytophthora root rot in mega-environments from soybean cultivars ‘Conrad’ and ‘Hefeng 25’. Theor Appl Genet 121:651–658
Li H, Bradbury P, Ersoz E, Buckler ES, Wang J (2011) Joint QTL linkage mapping for multiple-cross mating design sharing one common parent. PLoS One 6:e17573
Marcel TC, Gorguet B, Ta MT, Kohutova Z, Vels A, Niks RE (2008) Isolate specificity of quantitative trait loci for partial resistance of barley to Puccinia hordei confirmed in mapping populations and near-isogenic lines. New Phytol 177:743–755
McHale LK, Haun WJ, Xu WW, Bhaskar PB, Anderson JE, Hyten DL, Gerhardt DJ, Jeddeloh JA, Stupar RM (2012) Structural variants in the soybean genome localize to clusters of biotic stress-response genes. Plant Physiol 159:1295–1308
Mideros S, Nita M, Dorrance AE (2007) Characterization of components of partial resistance, Rps2, and root resistance to Phytophthora sojae in soybean. Phytopathology 97:655–662
Negeri AT, Coles ND, Holland JB, Balint-Kurti PJ (2011) Mapping QTL controlling southern leaf blight resistance by joint analysis of three related recombinant inbred line populations. Crop Sci 51:1571–1579
Nguyen VT, Vuong TD, VanToai T, Lee JD, Wu X, Mian MAR, Dorrance AE, Shannon JG, Nguyen HT (2012) Mapping of quantitative trait loci associated with resistance to Phytophthora sojae and flooding tolerance in soybean. Crop Sci 52:2481–2493
Parlevliet JE, Zadoks JC (1977) Integrated concept of disease resistance—new view including horizontal and vertical resistance in plants. Euphytica 26:5–21
Patterson HD, Thompson R (1971) Recovery of inter-block information when block sizes are unequal. Biometrika 58:545–554
Poland JA, Nelson RJ (2011) In the eye of the beholder: the effect of rater variability and different rating scales on QTL mapping. Phytopathology 101:290–298
Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ (2009) Shades of gray: the world of quantitative disease resistance. Trends Plant Sci 14:21–29
Poland JA, Bradbury PJ, Buckler ES, Nelson RJ (2011) Genome-wide nested association mapping of quantitative resistance to northern leaf blight in maize. Proc Natl Acad Sci USA 108:6893–6898
SAS Institute Inc (2011) SAS/STAT® 9.3 user’s guide. SAS Institute Inc., Cary
Schmitthenner AF (1985) Problems and progress in control of Phytophthora root rot of soybean. Plant Dis 69:362–368
Schon CC, Utz HF, Groh S, Truberg B, Openshaw S, Melchinger AE (2004) Quantitative trait locus mapping based on resampling in a vast maize testcross experiment and its relevance to quantitative genetics for complex traits. Genetics 167:485–498
Song QJ, Jia GF, Zhu YL, Grant D, Nelson RT, Hwang EY, Hyten DL, Cregan PB (2010) Abundance of SSR motifs and development of candidate polymorphic SSR markers (BARCSOYSSR_1.0) in soybean. Crop Sci 50:1950–1960
St Clair DA (2010) Quantitative disease resistance and quantitative resistance loci in breeding. Annu Rev Phytopathol 48:247–268
Stroup WW (1989) Why mixed models. Applications of mixed models in agriculture and related disciplines. South Coop Ser Bull 343:1–8 (Louisiana Agricultural Experiment Station, Baton Rouge)
Terry LI, Chase K, Jarvik T, Orf JH, Mansur LM, Lark KG (2000) Soybean quantitative trait loci for resistance to insects. Crop Sci 40:375–382
Thomison PR, Thomas CA, Kenworthy WJ (1991) Tolerant and root-resistant soybean cultivars: reactions to Phytophthora rot in inoculum-layer tests. Crop Sci 31:73–75
Tian F, Bradbury PJ, Brown PJ, Hung H, Sun Q, Flint-Garcia S, Rocheford TR, McMullen MD, Holland JB, Buckler ES (2011) Genome-wide association study of leaf architecture in the maize nested association mapping population. Nat Genet 43:159–162
Tucker DM, Saghai Maroof MA, Mideros S, Skoneczka JA, Nabati DA, Buss GR, Hoeschele I, Tyler BM, St. Martin SK, Dorrance AE (2010) Mapping quantitative trait loci for partial resistance to Phytophthora sojae in a soybean interspecific cross. Crop Sci 50:628–635
Vales MI, Schon CC, Capettini F, Chen XM, Corey AE, Mather DE, Mundt CC, Richardson KL, Sandoval-Islas JS, Utz HF, Hayes PM (2005) Effect of population size on the estimation of QTL: a test using resistance to barley stripe rust. Theor Appl Genet 111:1260–1270
Van Ooijen JW (2006) JoinMap® 4, software for the calculation of genetic linkage maps in experimental populations. Kyazma B.V., Wageningen
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
Walling GA, Visscher PM, Andersson L, Rothschild MF, Wang LZ, Moser G, Groenen MAM, Bidanel JP, Cepica S, Archibald AL, Geldermann H, de Koning DJ, Milan D, Haley CS (2000) Combined analyses of data from quantitative trait loci mapping studies: chromosome 4 effects on porcine growth and fatness. Genetics 155:1369–1378
Wang H, Waller L, Tripathy S, St. Martin SK, Zhou L, Krampis K, Tucker DM, Mao Y, Hoeschele I, Saghai Maroof MA, Tyler BM, Dorrance AE (2010) Analysis of genes underlying soybean quantitative trait loci conferring partial resistance to Phytophthora sojae. Plant Genome 3:23–40
Wang H, St Martin SK, Dorrance AE (2012) Comparison of phenotypic methods and yield contributions of quantitative trait loci for partial resistance to Phytophthora sojae in soybean. Crop Sci 52:609–622
Weng C, Yu K, Anderson TR, Poysa V (2007) A quantitative trait locus influencing tolerance to Phytophthora root rot in the soybean cultivar ‘Conrad’. Euphytica 158:81–86
White JW, Andrade-Sanchez P, Gore MA, Bronson KF, Coffelt TA, Conley MM, Feldmann KA, French AN, Heun JT, Hunsaker DJ, Jenks MA, Kimball BA, Roth RL, Strand RJ, Thorp KR, Wall GW, Wang GY (2012) Field-based phenomics for plant genetics research. Field Crop Res 133:101–112
Wu X, Zhou B, Zhao J, Guo N, Zhang B, Yang F, Chen S, Gai J, Xing H (2011) Identification of quantitative trait loci for partial resistance to Phytophthora sojae in soybean. Plant Breed 130:144–149
Yang G, Dong Y, Li Y, Wang Q, Shi Q, Zhou Q (2013) Verification of QTL for grain starch content and its genetic correlation with oil content using two connected RIL populations in high-oil maize. PLoS One 8:e53770
Zeng ZB (1994) Precision mapping of quantitative trait loci. Genetics 136:1457–1468
Acknowledgments
This study was funded in part by United Soybean Board and Ohio Soybean Council through soybean producer’s check-off dollars. We would like to acknowledge Dr. Perry Cregan’s laboratory (USDA-ARS, Beltsville, MA) for the preliminary SNP genotyping of parental genotypes with 1,536 SNPs. We thank Dr. Steve St. Martin for advice on statistical analysis, and Dr. Huihui Li (Chinese Academy of Agricultural Science, Beijing, China) for helpful discussion of JICIM and provision of scripts for permutation analysis. We also thank T. Mendiola, L. Wallace, A. Bhupendra, A. Gunadi, A. Stasko, C. Phelan, C. Balk, C. Smith, D. Plewa, D. Veney, D. Wickramasinghe, and R. Schneider for technical assistance, and J. Whittier for conducting Illumina’s GoldenGate® SNP genotyping at the MCIC/OARDC.
Conflict of interest
The authors declare that they have no conflict of interests.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by A. E. Melchinger.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Lee, S., Mian, M.A.R., Sneller, C.H. et al. Joint linkage QTL analyses for partial resistance to Phytophthora sojae in soybean using six nested inbred populations with heterogeneous conditions. Theor Appl Genet 127, 429–444 (2014). https://doi.org/10.1007/s00122-013-2229-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-013-2229-z