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Theoretical and Applied Genetics

, Volume 132, Issue 2, pp 405–417 | Cite as

Molecular characterization of genomic regions for resistance to Pythium ultimum var. ultimum in the soybean cultivar Magellan

  • Mariola Klepadlo
  • Christine S. Balk
  • Tri D. Vuong
  • Anne E. Dorrance
  • Henry T. NguyenEmail author
Original Article

Abstract

Key message

Two novel QTL for resistance to Pythium ultimum var. ultimum were identified in soybean using an Illumina SNP Chip and whole genome re-sequencing.

Abstract

Pythium ultimum var. ultimum is one of numerous Pythium spp. that causes severe pre- and post-emergence damping-off of seedlings and root rot of soybean [Glycine max (L.) Merr.]. The objective of this research was to identify quantitative trait loci (QTL) for resistance to P. ultimum var. ultimum in a recombinant inbred line population derived from a cross of ‘Magellan’ (moderately resistant) and PI 438489B (susceptible). Two different mapping approaches were utilized: the universal soybean linkage panel (USLP 1.0) and the bin map constructed from whole genome re-sequencing (WGRS) technology. Two genomic regions associated with variation in three disease-related parameters were detected using both approaches, with the bin map providing higher resolution. Using WGRS, the first QTL were mapped within a 350-kbp region on Chr. 6 and explained 7.5–13.5% of the phenotypic variance. The second QTL were positioned in a 260-kbp confidence interval on Chr. 8 and explained 6.3–16.8% of the phenotypic variation. Candidate genes potentially associated with disease resistance were proposed. High-resolution genetic linkage maps with a number of significant SNP markers could benefit marker-assisted breeding and dissection of the molecular mechanisms underlying soybean resistance to Pythium damping-off in ‘Magellan.’ Additionally, the outputs of this study may encourage more screening of diverse soybean germplasm and utilization of genome-wide association studies to understand the genetic basis of quantitative disease resistance.

Abbreviations

ANOVA

Analysis of variance

BLUP

Best linear unbiased predictor

DAI

Days after inoculation

LOD

Logarithm of odds

MAS

Marker-assisted selection

LG

Linkage group

LSD

Least significant difference

MDR

Multiple disease resistance

MQM

Multiple-QTL modeling

QTL

Quantitative trait locus

PS

Plant stand

RIL

Recombinant inbred line

RRS

Root rot score

RW

Fresh root weight

SNP

Single nucleotide polymorphism

SSR

Simple sequence repeat

USLP

Universal soybean linkage panel

WGRS

Whole genome re-sequencing

Notes

Acknowledgements

The authors would like to thank Dennis C. Yungbluth and Dr. Peng Cheng for their technical assistance with seed delivery, and Deloris Veney for technical assistance with phenotypic assay. Funding was provided through the soybean check-off dollars from United Soybean Board. This project was also funded in part through check-off dollars provided by the Ohio Soybean Council, and funds appropriated to the Ohio Agricultural Research and Development Center, The Ohio State University, and the National Institute of Food and Agriculture, United States Department of Agriculture (USDA), Hatch project for Development of Disease Management Strategies for Soybean Pathogens in Ohio OHO01303.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

122_2018_3228_MOESM1_ESM.docx (19 kb)
Supplementary Table 1. Summary of candidate genes identified in confidence intervals of QTL detected on Chrs. 6 and 8 conferring resistance to Pythium ultimum var. ultimum in Magellan. (DOCX 19 kb)

References

  1. Acharya B, Lee S, Mian MR, Jun TH, McHale LK, Michel AP, Dorrance AE (2015) Identification and mapping of quantitative trait loci (QTL) conferring resistance to Fusarium graminearum from soybean PI 567301B. Theor Appl Genet 128(5):827–838CrossRefGoogle Scholar
  2. Allen TW, Bradley CA, Sisson AJ, Byamukama E, Chilvers MI, Coker CM, Collins AA, Damicone JP, Dorrance AE, Dufault NS, Esker PD, Fraske TR, Giesler LJ, Grybauskas AP, Hershman DE, Hollier CA, Isakeit T, Jardine DJ, Kelly HM, Kemerait RC, Kleczewski NM, Koenning SR, Kurle JE, Malvick DK, Markell SG, Mehl HL, Mueller DS, Mueller JD, Mulrooney RP, Nelson BD, Newman MA, Osborne L, Overstreet C, Padgett GB, Phipps PM, Price PP, Sikora EJ, Smith DL, Spurlock TN, Tande CA, Tenuta AU, Wise KA, Wrather JA (2017) Soybean yield loss estimates due to diseases in the United States and Ontario, Canada, from 2010 to 2014. Plant Health Prog 18:19–27CrossRefGoogle Scholar
  3. Allen TW, Bissonnette K, Bradley CA, Damicone JP, Dufault NS, Faske TR, Hollier CA, Isakeit T, Kemerait RC, Kleczewski NM, Mehl HL, Mueller JD, Overstreet C, Price PP, Sikora EJ, Spurlock TN, Thiessen L, Young H (2018) Southern United States soybean disease loss estimates for 2017. In: Proceedings of the 45th annual meeting of the southern soybean disease workers. 7–8 March, Pensacola Beach, FLGoogle Scholar
  4. Balk C, Fitzgibbon T, Novakowiski JH, Erye M, Dorrance AE (2014) Assessment of resistance in soybean towards Pythium ultimum var. ultimum and Pythium ultimum var. sporangiiferum. Phytopathology 104(S3):166Google Scholar
  5. Bates GD, Rothrock CS, Rupe JC (2008) Resistance of the soybean cultivar Archer to Pythium damping-off and root rot caused by several Pythium spp. Plant Dis 92(5):763–766CrossRefGoogle Scholar
  6. Bernard RL, Cremeens CR, Cooper RL, Collins FI, Krober OA, Athow KL, Laviolette FA, Coble CJ, Nelson RL. (1998) Evaluation of the USDA soybean germplasm collection: maturity groups 000–IV. USDA Tech. Bull. 1871. US Gov. Print. Office, Washington, DCGoogle Scholar
  7. Broders KD, Lipps PE, Paul PA, Dorrance AE (2007) Characterization of Pythium spp. associated with corn and soybean seed and seedling disease in Ohio. Plant Dis 91(6):727–735CrossRefGoogle Scholar
  8. Broders KD, Wallhead MW, Austin GD, Lipps PE, Paul PA, Mullen RW, Dorrance AE (2009) Association of soil chemical and physical properties with Pythium species diversity, community composition, and disease incidence. Phytopathology 99(8):957–967CrossRefGoogle Scholar
  9. Broman KW, Sen S (2009) A guide to QTL mapping with R/qtl. Springer, New YorkCrossRefGoogle Scholar
  10. Brown GE, Kennedy BW (1965) Pythium pre-emergence damping-off of soybean in Minnesota. Plant Dis Rep 49:646–647Google Scholar
  11. Campa A, Pérez-Vega E, Pascual A, Ferreira JJ (2010) Genetic analysis and molecular mapping of quantitative trait loci in common bean against Pythium ultimum. Phytopathology 100(12):1315–1320CrossRefGoogle Scholar
  12. Cheng P, Gedling CR, Patil G, Vuong TD, Shannon JG, Dorrance AE, Nguyen HT (2017a) Genetic mapping and haplotype analysis of a locus for quantitative resistance to Fusarium graminearum in soybean accession PI 567516C. Theor Appl Genet 130(5):999–1010CrossRefGoogle Scholar
  13. Cheng Y, Ma Q, Ren H, Xia Q, Song E, Tan Z, Li S, Zhang G, Nian H (2017b) Fine mapping of a Phytophthora resistance gene RpsWY in soybean (Glycine max L.) by high-throughput genome-wide sequencing. Theor Appl Genet 130(5):1041–1051CrossRefGoogle Scholar
  14. Cianzio SR, Shultz SP, Fehr WR, Tachibana H (1991) Registration of ‘Archer’ soybean. Crop Sci 31:1707–1712CrossRefGoogle Scholar
  15. Dorrance AE, Schmitthenner AF (2000) New sources of resistance to Phytophthora sojae in the soybean plant introductions. Plant Dis 84(12):1303–1308CrossRefGoogle Scholar
  16. Dorrance AE, Berry SA, Lipps PE (2004) Characterization of Pythium spp. from three Ohio fields for pathogenicity on corn and soybean and metalaxyl sensitivity. Plant Health Prog 5(1):10–16CrossRefGoogle Scholar
  17. Ellis ML, McHale LK, Paul PA, St Martin SK, Dorrance AE (2013) Soybean germplasm resistant to and molecular mapping of resistance quantitative trait loci derived from the soybean accession PI 424354. Crop Sci 53(3):1008–1021CrossRefGoogle Scholar
  18. Empig L, Fehr WR (1971) Evaluation of methods for generation advance in bulk hybrid soybean populations 1. Crop Sci 11(1):51–54CrossRefGoogle Scholar
  19. Fehr WR, Caviness CE, Burmood DT, Pennington JS (1971) Stage of development descriptions for soybeans, Glycine Max (L.) Merrill 1. Crop Sci 11(6):929–931CrossRefGoogle Scholar
  20. Gillman JD, Kim WS, Song B, Oehrle NW, Tawari NR, Liu S, Krishnan HB (2017) Whole-genome resequencing identifies the molecular genetic cause for the absence of a Gy5 glycinin protein in soybean PI 603408. G3 7(7):2345–2352CrossRefGoogle Scholar
  21. Griffin GJ (1990) Importance of Pythium ultimum in a disease syndrome of cv. Essex soybean. Can J Plant Pathol 12(2):135–140CrossRefGoogle Scholar
  22. Hyten DL, Choi IY, Song Q, 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(3):960–968CrossRefGoogle Scholar
  23. Iquira E, Humira S, François B (2015) Association mapping of QTLs for Sclerotinia stem rot resistance in a collection of soybean plant introductions using a genotyping by sequencing (GBS) approach. BMC Plant Biol 15(1):5–11CrossRefGoogle Scholar
  24. Jiang YN, Haudenshield JS, Hartman GL (2012) Characterization of Pythium spp. from soil samples in Illinois. Can J Plant Pathol 34(3):448–454CrossRefGoogle Scholar
  25. Keeling BL (1974) Soybean seed rot and the relation of seed exudate to host susceptibility. Phytopathology 64:1445–1447CrossRefGoogle Scholar
  26. Kirkpatrick MT, Rothrock CS, Rupe JC, Gbur EE (2006) The effect of Pythium ultimum and soil flooding on two soybean cultivars. Plant Dis 90(5):597–602CrossRefGoogle Scholar
  27. Koenning SR, Wrather JA (2010) Suppression of soybean yield potential in the continental United States by plant diseases from 2006 to 2009. Plant Health Prog 11:10–13CrossRefGoogle Scholar
  28. Lamichhane JR, Dürr C, Schwanck AA, Robin MH, Sarthou JP, Cellier V, Messéan A, Aubertot JN (2017) Integrated management of damping-off diseases: a review. Agron Sustain Dev 37(2):10–20CrossRefGoogle Scholar
  29. Levesque CA, De Cock AW (2004) Molecular phylogeny and taxonomy of the genus Pythium. Mycol Res 108(12):1363–1383CrossRefGoogle Scholar
  30. Li X, Han Y, Teng W, Zhang S, Yu K, Poysa V, Anderson T, Ding J, Li W (2010) Pyramided QTL underlying tolerance to Phytophthora root rot in mega-environments from soybean cultivars ‘Conrad’ and ‘Hefeng 25’. Theor Appl Genet 121(4):651–658CrossRefGoogle Scholar
  31. Liu S, Kandoth PK, Warren SD, Yeckel G, Heinz R, Alden J, Yang C, Jamai A, El-Mellouki T, Juvale PS, Hill J (2012) A soybean cyst nematode resistance gene points to a new mechanism of plant resistance to pathogens. Nature 492(7428):256–257Google Scholar
  32. Mahuku GS, Buruchara R, Navia U, Otsyula RM (2005) A gene that confers resistance to Pythium root rot in common bean: genetic characterization and development of molecular markers. Repos Agric Res OutputsGoogle Scholar
  33. Marchand G, Chen Y, Berhane NA, Wei L, Lévesque CA, Xue AG (2014) Identification of Pythium spp. from the rhizosphere of soybeans in Ontario, Canada. Can J Plant Pathol 36(2):246–251CrossRefGoogle Scholar
  34. Matthiesen RL, Ahmad AA, Robertson AE (2016) Temperature affects aggressiveness and fungicide sensitivity of four Pythium spp. that cause soybean and corn damping off in Iowa. Plant Dis 100(3):583–591CrossRefGoogle Scholar
  35. McLachlan KS (2016) Evaluation of Pythium root rot and damping off resistance in the ancestral lines of North American soybean cultivars and chemical control of the active ingredient ethaboxam in seed treatments. Master thesis. University of IllinoisGoogle Scholar
  36. Navarro F, Sass ME, Nienhuis J (2008) Identification and confirmation of quantitative trait loci for root rot resistance in snap bean. Crop Sci 48(3):962–972CrossRefGoogle Scholar
  37. Niks RE, Qi X, Marcel TC (2015) Quantitative resistance to biotrophic filamentous plant pathogens: concepts, misconceptions, and mechanisms. Annu Rev Phytopathol 4(53):445–470CrossRefGoogle Scholar
  38. Otsyula R, Rubaihayo P, Buruchara R (2003) Inheritance of resistance to Pythium root rot in beans (Phaseolus vulgaris) genotypes. Afr Crop Sci Conf Proc 6:295–298Google Scholar
  39. Patil G, Do T, Vuong TD, Valliyodan B, Lee JD, Chaudhary J, Shannon JG, Nguyen HT (2016) Genomic-assisted haplotype analysis and the development of high-throughput SNP markers for salinity tolerance in soybean. Sci Rep 6:19199–19206CrossRefGoogle Scholar
  40. Radmer L, Anderson G, Malvick DM, Kurle JE, Rendahl A, Mallik A (2017) Pythium, Phytophthora, and Phytopythium spp. associated with soybean in Minnesota, their relative aggressiveness on soybean and corn, and their sensitivity to seed treatment fungicides. Plant Dis 101(1):62–72CrossRefGoogle Scholar
  41. Rod KS, Walker DR, Bradley C (2018) Evaluation of major ancestors of North American soybean cultivars for resistance to three Pythium species that cause seedling blight. Plant Dis 102(11):2241–2252CrossRefGoogle Scholar
  42. Rojas JA, Jacobs JL, Napieralski S, Karaj B, Bradley CA, Chase T, Esker PD, Giesler LJ, Jardine DJ, Malvick DK, Markell SG, Nelson BD, Robertson AE, Rupe JC, Smith DL, Sweets LE, Tenuta AU, Wise KA, Chilvers MI (2017a) Oomycete species associated with soybean seedlings in North America—part I: identification and pathogenicity characterization. Phytopathology 107(3):280–292CrossRefGoogle Scholar
  43. Rojas JA, Jacobs JL, Napieralski S, Karaj B, Bradley CA, Chase T, Esker PD, Giesler LJ, Jardine DJ, Malvick DK, Markell SG (2017b) Oomycete species associated with soybean seedlings in North America—part II: diversity and ecology in relation to environmental and edaphic factors. Phytopathology 107(3):293–304CrossRefGoogle Scholar
  44. Rosso ML, Rupe JC, Chen P, Mozzoni LA (2008) Inheritance and genetic mapping of resistance to damping-off caused by Pythium aphanidermatum in ‘Archer’ soybean. Crop Sci 48(6):2215–2222CrossRefGoogle Scholar
  45. Rupe JC, Rothrock CS, Rosso L, Gbur E (2017) Effect of planting date, seed treatment, seed quality, flooding and Pythium resistance to soybean emergence. Phytopathology 107(3):10–11Google Scholar
  46. Stroup WW (1989) Why mixed models. Applications of mixed models in agriculture and related disciplines. South Coop Serv Bull 343:1–8Google Scholar
  47. Swaminathan S, Abeysekara NS, Liu M, Cianzio SR, Bhattacharyya MK (2016) Quantitative trait loci underlying host responses of soybean to Fusarium virguliforme toxins that cause foliar sudden death syndrome. Theor Appl Genet 129(3):495–506CrossRefGoogle Scholar
  48. Urrea K, Rupe J, Chen P, Rothrock CS (2017) Characterization of seed rot resistance to Pythium aphanidermatum in soybean. Crop Sci 57(3):1394–1403CrossRefGoogle Scholar
  49. Van Ooijen JW, Voorrips RE (2006) Joinmap 4.0 manual. Kyazma, WageningenGoogle Scholar
  50. Van Ooijen JW, Boer MP, Jansen RC, Maliepaard CA (2000) MapQTL 4.0: software for the calculation of QTL positions on genetic maps (user manual). Plant Res InternatGoogle Scholar
  51. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93(1):77–78CrossRefGoogle Scholar
  52. Vuong TD, Sleper DA, Shannon JG, Wu X, Nguyen HT (2011) Confirmation of quantitative trait loci for resistance to multiple-HG types of soybean cyst nematode (Heterodera glycines Ichinohe). Euphytica 181(1):101–111CrossRefGoogle Scholar
  53. Wang J, Li H, Zhang L, Li C, Meng L (2010) Users’ manual of QTL IciMapping V3. 0. Chinese Academy of Agricultural Sciences, BeijingGoogle Scholar
  54. Wiener-Hanks T, Nelson R (2016) Multiple disease resistance in plants. Annu Rev Phytopathol 54:229–252CrossRefGoogle Scholar
  55. Xu X, Zeng L, Tao Y, Vuong T, Wan J, Boerma R, Noe J, Li Z, Finnerty S, Pathan SM, Shannon JG (2013) Pinpointing genes underlying the quantitative trait loci for root-knot nematode resistance in palaeopolyploid soybean by whole genome resequencing. Proc Natl Acad Sci USA 110(33):13469–13474CrossRefGoogle Scholar
  56. Yang XB (1999) Pythium damping-off and root rot. Compendium of soybean diseases, 4th edn. APS Press, St. Paul, MN, pp 42–44Google Scholar
  57. Yang SS, Chen TY, Tzeng DS (2005) The role of ChiF gene expression in relating to mycoparasitism of Streptomyces griseobrunneus S3 on Rhizoctonia solani AG4 and Pythium aphanidermatum. Plant Pathol Bull 14(2):147–158Google Scholar
  58. Yuan J, Wen Z, Gu C, Wang D (2017) Introduction of high throughput and cost effective SNP genotyping platforms in soybean. Plant Genet Genom Biotech 2(1):90–94CrossRefGoogle Scholar
  59. Yue P, Arelli PR, Sleper DA (2001) Molecular characterization of resistance to Heterodera glycines in soybean PI 438489B. Theor Appl Genet 102(6–7):921–928CrossRefGoogle Scholar
  60. Zhang BQ, Yang XB (2000) Pathogenicity of Pythium populations from corn-soybean rotation fields. Plant Dis 84(1):94–99CrossRefGoogle Scholar
  61. Zitnick-Anderson KK, Nelson BD Jr (2015) Identification and pathogenicity of Pythium on soybean in North Dakota. Plant Dis 99(1):31–38CrossRefGoogle Scholar
  62. Zitnick-Anderson KK, Norland JE, Luis E, Fortuna AM, Nelson BD (2017) Probability models based on soil properties for predicting presence-absence of Pythium in soybean roots. Microb Ecol 6:1Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Division of Plant ScienceUniversity of MissouriColumbiaUSA
  2. 2.Department of Plant PathologyThe Ohio State UniversityWoosterUSA
  3. 3.Davey TreeKentUSA

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