Theoretical and Applied Genetics

, Volume 131, Issue 4, pp 757–773 | Cite as

Integration of sudden death syndrome resistance loci in the soybean genome

  • Hao-Xun Chang
  • Mitchell G. Roth
  • Dechun Wang
  • Silvia R. Cianzio
  • David A. Lightfoot
  • Glen L. Hartman
  • Martin I. Chilvers


Key message

Complexity and inconsistencies in resistance mapping publications of soybean sudden death syndrome (SDS) result in interpretation difficulty. This review integrates SDS mapping literature and proposes a new nomenclature system for reproducible SDS resistance loci.


Soybean resistance to sudden death syndrome (SDS) is composed of foliar resistance to phytotoxins and root resistance to pathogen invasion. There are more than 80 quantitative trait loci (QTL) and dozens of single nucleotide polymorphisms (SNPs) associated with soybean resistance to SDS. The validity of these QTL and SNPs is questionable because of the complexity in phenotyping methodologies, the disease synergism between SDS and soybean cyst nematode (SCN), the variability from the interactions between soybean genotypes and environments, and the inconsistencies in the QTL nomenclature. This review organizes SDS mapping results and proposes the Rfv (resistance to Fusarium virguliforme) nomenclature based on supporting criteria described in the text. Among ten reproducible loci receiving our Rfv nomenclature, Rfv18-01 is mostly supported by field studies and it co-localizes to the SCN resistance locus rhg1. The possibility that Rfv18-01 is a pleiotropic resistance locus and the concern about Rfv18-01 being confounded with Rhg1 is discussed. On the other hand, Rfv06-01, Rfv06-02, Rfv09-01, Rfv13-01, and Rfv16-01 were identified both by screening soybean leaves against phytotoxic culture filtrates and by evaluating SDS severity in fields. Future phenotyping using leaf- and root-specific resistance screening methodologies may improve the precision of SDS resistance, and advanced genetic studies may further clarify the interactions among soybean genotypes, F. virguliforme, SCN, and environments. The review provides a summary of the SDS resistance literature and proposes a framework for communicating SDS resistance loci for future research considering molecular interactions and genetic breeding for soybean SDS resistance.





Genome-wide association study


Leucine-repeat rich


Quantitative trait loci


Resistance to Fusarium virguliforme


Resistance to Heterodera glycine


Soybean cyst nematode


Sudden death syndrome


Single nucleotide polymorphisms


Simple sequence repeat



Funding was provide by North Central Soybean Research Program and Michigan Soybean Promotion Committee.

Compliance with ethical standards

Conflict of interest

The authors claim no conflict of interest.

Supplementary material

122_2018_3063_MOESM1_ESM.xlsx (66 kb)
Supplementary material 1 (XLSX 65kb)
122_2018_3063_MOESM2_ESM.pdf (45 kb)
Supplementary material 2 (PDF 44kb) Supplemental Fig.1. Pedigrees of ‘Forrest’, ‘Hartwig’, and ‘Pyramid’


  1. Abdelmajid KM, Meksem K, Wood AJ, Lightfoot DA (2007) Loci underlying SDS and SCN resistance mapped in the ‘Essex’ by ‘Forrest’ soybean recombinant inbred lines. Rev Biol Biotechnol 6:2–10Google Scholar
  2. Abdelmajid KM, Ramos L, Leandro LF, Mbofung G, Hyten DL, Kantartzi SK et al (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 1:18–30CrossRefGoogle Scholar
  3. Abdelsamad NA, Baumbach J, Bhattacharyya MK, Leandro LF (2017) Soybean sudden death syndrome caused by Fusarium virguliforme is impaired by prolonged flooding and anaerobic conditions. Plant Dis 101:712–719CrossRefGoogle Scholar
  4. Adee E, Ruiz Diaz DA, Little CR (2016) Effect of soil-test phosphorus and phosphorus fertilization on the severity of soybean sudden death syndrome. Crop Forage Turfgrass Manag. Google Scholar
  5. Afzal AJ, Srour A, Goil A, Vasudaven S, Liu T, Samudrala R et al (2013) Homo-dimerization and ligand binding by the leucine-rich repeat domain at RHG1/RFS2 underlying resistance to two soybean pathogens. BMC Plant Biol 13:43CrossRefPubMedPubMedCentralGoogle Scholar
  6. Allen TW, Bradley CA, Sisson AJ, ByamukamaE Chilvers MI, Coker CM et al (2017) Soybean yield loss estimates due to diseases in the United States, and Ontario, Canada, from 2010 to 2014. Plant Health Progress 18:19–27Google Scholar
  7. Anderson J, Akond M, Kassem MA, Meksem K, Kantartzi SK (2015) Quantitative trait loci underlying resistance to sudden death syndrome (SDS) in MD96-5722 by ‘Spencer’ recombinant inbred line population of soybean. 3 Biotech 5:203–210CrossRefPubMedGoogle Scholar
  8. Ballini E, Morel JB, Droc G, Price A, Courtois B, Notteghem JL et al (2008) A genome-wide meta-analysis of rice blast resistance genes and quantitative trait loci provides new insights into partial and complete resistance. Mol Plant Microbe Interact 21:859–868CrossRefPubMedGoogle Scholar
  9. Bao Y, Kurle JE, Anderson G, Young ND (2015) Association mapping and genomic prediction for resistance to sudden death syndrome in early maturing soybean germplasm. Mol Breed 35:128CrossRefPubMedPubMedCentralGoogle Scholar
  10. Brar HK, Swaminathan S, Bhattacharyya MK (2011) The Fusarium virguliforme toxin FvTox1 causes foliar sudden death syndrome-like symptoms in soybean. Mol Plant Microbe Interact 24:1179–1188CrossRefPubMedGoogle Scholar
  11. Brzostowski LF, Schapaugh WT, Rzodkiewicz PA, Todd TC, Little CR (2014) Effect of host resistance to Fusarium virguiliforme and Heterodera glycines on sudden death syndrome disease severity and soybean yield. Plant Health Progress 15:1–8Google Scholar
  12. Caldwell BE, Brim CA, Ross JP (1960) Inheritance of resistance of soybeans to the cyst nematode, Heterodera glycines. Agron J 52:635–636CrossRefGoogle Scholar
  13. Chang SJC, Doubler TW, Kilo V, Suttner R, Klein J, Schmidt ME et al (1996) Two additional loci underlying durable field resistance to soybean sudden death syndrome (SDS). Crop Sci 36:1684–1688CrossRefGoogle Scholar
  14. Chang SJC, Doubler TW, Kilo V, Abu-Thredeih J, Pradhu R, Freire V et al (1997) Association of loci underlying field resistance to soybean sudden death syndrome (SDS) and cyst nematode (SCN) race 3. Crop Sci 37:965–971CrossRefGoogle Scholar
  15. Chang HX, Domier LL, Radwan O, Yendrek CR, Hudson ME, Hartman GL (2016a) Identification of multiple phytotoxins produced by Fusarium virguliforme including a phytotoxic effector (FvNIS1) associated with sudden death syndrome foliar symptoms. Mol Plant Microbe Interact 29:96–108CrossRefPubMedGoogle Scholar
  16. Chang HX, Lipka AE, Domier LL, Hartman GL (2016b) Characterization of disease resistance loci in the USDA Soybean germplasm collection using genome-wide association studies. Phytopathology 106:1139–1151CrossRefPubMedGoogle Scholar
  17. Chong SK, Hildebrand KK, Luo Y, Myers O, Indorante SJ, Kazakevicius A et al (2005) Mapping soybean sudden death syndrome as related to yield and soil/site properties. Soil Tillage Res 84:101–107CrossRefGoogle Scholar
  18. Cook DE, Lee TG, Guo XL, Melito S, Wang K, Bayless AM et al (2012) Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science 338:1206–1209CrossRefPubMedGoogle Scholar
  19. Farias Neto AL, Hartman GL, Pedersen WL, Li S, Diers BW (2006) Irrigation and inoculation methods that increase the severity of soybean sudden death syndrome in the field. Crop Sci 46:2547–2554CrossRefGoogle Scholar
  20. Farias Neto AL, Hashmi R, Schmidt M, Carlson SR, Hartman GL, Li SX et al (2007) Mapping and confirmation of a new sudden death syndrome resistance QTL on linkage group D2 from the soybean genotypes PI 567374 and ‘Ripley’. Mol Breed 20:53–62CrossRefGoogle Scholar
  21. Farias Neto AL, Schmidt M, Hartman GL, Li S, Diers BW (2008) Inoculation methods under greenhouse conditions for evaluating soybean resistance to sudden death syndrome. Pesquisa Agropecuária Brasileira 43:1475–1482CrossRefGoogle Scholar
  22. Flor HH (1942) Inheritance of pathogenicity in Melampsora lini. Phytopathology 32:653–669Google Scholar
  23. Gao X, Jackson TA, Hartman GL, Niblack TL (2006) Interactions between the soybean cyst nematode and Fusarium solani f. sp. glycines based on greenhouse factorial experiments. Phytopathology 96:1409–1415CrossRefPubMedGoogle Scholar
  24. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogen. Annu Rev Pythopathol 43:205–227CrossRefGoogle Scholar
  25. Goffinet B, Gerber S (2000) Quantitative trait loci: a meta-analysis. Genetics 155:463–473PubMedPubMedCentralGoogle Scholar
  26. Gongora-Canul CC, Leandro LF (2011) Effect of soil temperature and plant age at time of inoculation on progress of root rot and foliar symptoms of soybean sudden death syndrome. Plant Dis 95:436–440CrossRefGoogle Scholar
  27. Gongora-Canul CC, Nutter FW, Leandro LF (2012) Temporal dynamics of root and foliar severity of soybean sudden death syndrome at different inoculum densities. Eur J Plant Pathol 132:71–79CrossRefGoogle Scholar
  28. Grant D, Nelson RT, Cannon SB, Shoemaker RC (2010) SoyBase, the USDA-ARS soybean genetics and genomics database. Nucleic Acids Res 38:D843–D846CrossRefPubMedGoogle Scholar
  29. Hartman GL, Huang YH, Nelson RL, Noel GR (1997) Germplasm evaluation of Glycine max for resistance to Fusarium solani, the causal organism of sudden death syndrome. Plant Dis 81:515–518CrossRefGoogle Scholar
  30. Hartman GL, Huang YH, Li S (2004) Phytotoxicity ofFusarium solaniculture filtrates from soybeans and other hosts assayed by stem cuttings. Aust Plant Pathol 33:9–15CrossRefGoogle Scholar
  31. Hartman GL, Chang HX, Leandro LF (2015) Research advances and management of soybean sudden death syndrome. Crop Prot 73:60–66CrossRefGoogle Scholar
  32. Hnetkovsky N, Chang SJC, Doubler TW, Gibson PT, Lightfoot DA (1996) Genetic mapping of loci underlying field resistance to soybean sudden death syndrome (SDS). Crop Sci 36:393–400CrossRefGoogle Scholar
  33. Iqbal MJ, Meksem K, Njiti VN, Kassem MA, Lightfoot DA (2001) Microsatellite markers identify three additional quantitative trait loci for resistance to soybean sudden-death syndrome (SDS) in Essex × Forrest RILs. Theor Appl Genet 102:187–192CrossRefGoogle Scholar
  34. Iqbal MJ, Ahsan R, Afzal AJ, Jamal A, Meksem K, El-Shemy HA et al (2008) Multigenetic QTL: the laccase encoded within the soybean Rfs2/rhg1 locus inferred to underlie part of the dual resistance to cyst nematode and sudden death syndrome. Curr Issues Mol Biol 11:11–19Google Scholar
  35. Kandel YR, Bradley CA, Wise KA, Chilvers MI, Tenuta AU, Davis VM et al (2015) Effect of glyphosate application on sudden death syndrome of glyphosate-resistant soybean under field conditions. Plant Dis 99:347–354CrossRefGoogle Scholar
  36. Kandel YR, Wise KA, Bradley CA, Chilvers MI, Tenuta AU, Mueller DS (2016a) Fungicide and cultivar effects on sudden death syndrome and yield of soybean. Plant Dis 100:1339–1350CrossRefGoogle Scholar
  37. Kandel YR, Wise KA, Bradley CA, Tenuta AU, Mueller DS (2016b) Effect of planting date, seed treatment, and cultivar on plant population, sudden death syndrome, and yield of soybean. Plant Dis 100:1735–1743CrossRefGoogle Scholar
  38. Kandel YR, Wise KA, Bradley CA, Chilvers MI, Byrne AM, Tenuta AU et al (2017) Effect of soybean cyst nematode resistance source and seed treatment on population densities of Heterodera glycines, sudden death syndrome, and yield of soybean. Plant Dis 101(12):2137–2143CrossRefGoogle Scholar
  39. Kassem MA, Shultz J, Meksem K, Cho Y, Wood AJ, Iqbal MJ et al (2006) An updated ‘Essex’ by ‘Forrest’ linkage map and first composite interval map of QTL underlying six soybean traits. Theor Appl Genet 113:1015–1026CrossRefPubMedGoogle Scholar
  40. Kazi S, Shultz J, Afzal J, Johnson J, Njiti VN, Lightfoot DA (2008) Separate loci underlie resistance to root infection and leaf scorch during soybean sudden death syndrome. Theor Appl Genet 116:967–977CrossRefPubMedGoogle Scholar
  41. Kazi S, Shultz J, Afzal J, Hashmi R, Jasim M, Bond J et al (2010) Iso-lines and inbred-lines confirmed loci that underlie resistance from cultivar ‘Hartwig’ to three soybean cyst nematode populations. Theor Appl Genet 120:633–644CrossRefPubMedGoogle Scholar
  42. Koenning SR, Wrather JA (2010) Suppression of soybean yield potential in the continental United States by plant diseases from 2006 to 2009. Plant Health Progress. (online) Google Scholar
  43. Kushalappa AC, Yogendra KN, Karre S (2016) Plant innate immune response: qualitative and quantitative resistance. Crit Rev Plant Sci 35:38–55CrossRefGoogle Scholar
  44. Li S, Hartman GL, Widholm JM (1999) Viability staining of soybean suspension-cultured cells and a seedling stem cutting assay to evaluate phytotoxicity of Fusarium solani f. sp. glycines culture filtrates. Plant Cell Rep 18:375–380CrossRefGoogle Scholar
  45. Lightfoot DA (2015) Two decades of molecular marker-assisted breeding for resistance to soybean sudden death syndrome. Crop Sci 55:1460–1484CrossRefGoogle Scholar
  46. Liu SM, Kandoth PK, Lakhssassi N, Kang JW, Colantonio V, Heinz R et al (2017) The soybean GmSNAP18 gene underlies two types of resistance to soybean cyst nematode. Nat Commun 8:14822CrossRefPubMedPubMedCentralGoogle Scholar
  47. Luckew AS, Leandro LF, Bhattacharyya MK, Nordman DJ, Lightfoot DA, Cianzio SR (2013) Usefulness of 10 genomic regions in soybean associated with sudden death syndrome resistance. Theor Appl Genet 126:2391–2403CrossRefPubMedGoogle Scholar
  48. Luckew AS, Swaminathan S, Leandro LF, Orf JH, Cianzio SR (2017) ‘MN1606SP’ by ‘Spencer’ filial soybean population reveals novel quantitative trait loci and interactions among loci conditioning SDS resistance. Theor Appl Genet 130:2139–2149CrossRefPubMedGoogle Scholar
  49. Marburger D, Conley S, Esker P, MacGuidwin A, Smith D (2014) Relationship Between Fusarium virguliforme and Heterodera glycines in Commercial Soybean Fields in Wisconsin. Plant Health Progress 15:11–18Google Scholar
  50. Meksem K, Doubler TW, Chancharoenchai K, Njiti VN, Chang SJC, Arelli APR et al (1999) Clustering among loci underlying soybean resistance to Fusarium solani, SDS and SCN in near-isogenic lines. Theor Appl Genet 99:1131–1142CrossRefGoogle Scholar
  51. Meksem K, Pantazopoulos P, Njiti VN, Hyten LD, Arelli PR, Lightfoot DA (2001) ’Forrest’ resistance to the soybean cyst nematode is bigenic: saturation mapping of the Rhg1 and Rhg4 loci. Theor Appl Genet 103:710–717CrossRefGoogle Scholar
  52. Mueller DS, Hartman GL, Nelson RL, Pedersen WL (2002) Evaluation of Glycine max germplasm for resistance to Fusarium solani f. sp. glycines. Plant Dis 86:741–746CrossRefGoogle Scholar
  53. Navi SS, Yang XB (2016) Sudden death syndrome—a growing threat of losses in soybeans. CAB Rev 11:1–13CrossRefGoogle Scholar
  54. Njiti VN, Lightfoot DA (2006) Genetic analysis infers Dt loci underlie resistance to Fusarium solani f. sp. glycines in indeterminate soybeans. Can J Plant Sci 86:83–90CrossRefGoogle Scholar
  55. Njiti VN, Shenaut MA, Suttner RJ, Schmidt ME, Gibson PT (1996) Soybean reponse to soybean sudden death syndrome: inheritance influenced by cyst nematode resistance in Pyramid × Douglas progenies. Crop Sci 36:1165–1170CrossRefGoogle Scholar
  56. Njiti VN, Doubler TW, Suttner RJ, Gary LE, Gilson PT, Lightfoot DA (1998) Resistance to soybean sudden death syndrome and root colonization by Fusarium solani f. sp. glycine in near-isogenic lines. Crop Sci 38:472–477CrossRefGoogle Scholar
  57. Njiti VN, Johnson JE, Torto TA, Gray LE, Lightfoot DA (2001) Inoculum rate influences selection for field resistance to soybean sudden death syndrome in the greenhouse. Crop Sci 41:1726–1731CrossRefGoogle Scholar
  58. Njiti VN, Meksem K, Iqbal MJ, Johnson JE, Kassem MA, Zobrist KF et al (2002) Common loci underlie field resistance to soybean sudden death syndrome in ‘Forrest’, ‘Pyramid’, ‘Essex’, and ‘Douglas’. Theor Appl Genet 104:294–300CrossRefPubMedGoogle Scholar
  59. Ortiz-Ribbing LM, Eastburn DM (2004) Soybean root systems and sudden death syndrome severity: taproot and lateral root infection. Plant Dis 88:1011–1016CrossRefGoogle Scholar
  60. Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ (2009) Shades of gray: the world of quantitative disease resistance. Trends Plant Sci 14:21–29CrossRefPubMedGoogle Scholar
  61. Prabhu RR, Njiti VN, Bell-Johnson B, Johnson JE, Schmidt ME, Klein JH et al (1999) Selecting soybean cultivars for dual resistance to soybean cyst nematode and sudden death syndrome using two DNA markers. Crop Sci 39:982–987CrossRefGoogle Scholar
  62. Radwan O, Liu Y, Clough SL (2011) Transcriptional analysis of soybean root response to Fusarium virguliforme, the causal agent of sudden death syndrome. Mol Plant Microbe Interact 24:958–972CrossRefPubMedGoogle Scholar
  63. Radwan O, Li M, Calla B, Li S, Hartman GL, Clough SJ (2013) Effect of Fusarium virguliforme phytotoxin on soybean gene expression suggests a role in multidimensional defense. Mol Plant Pathol 14:293–307CrossRefPubMedGoogle Scholar
  64. Rogovska N, Laird D, Leandro LF, Aller D (2017) Biochar effect on severity of soybean root disease caused byFusarium virguliforme. Plant Soil 413:111–126CrossRefGoogle Scholar
  65. Roy KW, Hershman DE, Rupe JC, Abney TS (1997) Sudden death syndrome of soybean. Plant Dis 81:1100–1111CrossRefGoogle Scholar
  66. Rupe JC, Robbins RT, Gbur EE Jr (1997) Effects of crop rotation on soil population densities of Fusarium solani and Heterodera glycines and on the development of sudden death syndrome of soybean. Crop Prot 16:575–580CrossRefGoogle Scholar
  67. Rupe JC, Robbins RT, Becton CB, Sabbe WA, Gbur EE Jr (1999) Vertical and temporal distribution of Fusarium solani and Heterodera glycines in fields with sudden death syndrome of soybean. Soil Biol Biochem 31:245–251CrossRefGoogle Scholar
  68. Rupe JC, Widick JD, Sabbe WE, Robbins RT, Becton CB (2000) Effect of chloride and soybean cultivar on yield and development of sudden death syndrome, soybean cyst nematode, and southern blight. Plant Dis 84:669–674CrossRefGoogle Scholar
  69. Rupe JC, Sabbe WE, Robbins RT, Gbur EE Jr (2013) Soil and plant factors associated with sudden death syndrome of soybean. J Prod Agric 6:218–221CrossRefGoogle Scholar
  70. Sanogo G, Yang XB, Lundeen P (2001) Field response of glyphosate-tolerant soybean to herbicides and sudden death syndrome. Plant Dis 85:773–779CrossRefGoogle Scholar
  71. Scandiani MM, Ruberti DS, Giorda LM, Pioli RN, Luque AG, Bottai H et al (2011) Comparisons of inoculation methods for characterizing relative aggressiveness of two soybean sudden death syndrome pathogens, Fusarium virguliforme and F. tucumaniae. Tropic Plant Pathol 36:133–140CrossRefGoogle Scholar
  72. Scherm H, Yang XB (1996) Development of sudden death syndrome of soybean in relation to soil temperature and soil water matric potential. Phytopathology 86:642–649CrossRefGoogle Scholar
  73. Scherm H, Yang XB (2010) Relation of sand content, pH, and potassium and phosphorus nutrition to the development of sudden death syndrome in soybean. Can J Plant Path 23:174–180Google Scholar
  74. Scherm H, Yang XB, Lundeen P (1998) Soil variables associated with sudden death syndrome in soybean fields in Iowa. Plant Dis 82:1152–1157CrossRefGoogle Scholar
  75. Schweizer P, Stein N (2011) Large-scale data integration reveals colocalization of gene functional groups with meta-QTL for multiple disease resistance in barley. Mol Plant Microbe Interact 24:1492–1501CrossRefPubMedGoogle Scholar
  76. Soriano JM, Royo C (2015) Dissecting the genetic architecture of leaf rust resistance in wheat by QTL meta-analysis. Phytopathology 105:1585–1593CrossRefPubMedGoogle Scholar
  77. Sosnowski O, Charcosset A, Joets J (2012) BioMercator V3: an upgrade of genetic map compilation and quantitative trait loci meta-analysis algorithms. Bioinformatics 28:2082–2083CrossRefPubMedPubMedCentralGoogle Scholar
  78. Srour A, Afzal AJ, Blahut-Beatty L, Hemmati N, Simmonds DH, Li WB 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 13:368CrossRefGoogle Scholar
  79. Srour A, Gibson DJ, Leandro LFS, Malvick DK, Bond JP, Fakhoury AM (2017) Unraveling microbial and edaphic factors affecting the development of sudden death syndrome in soybean. Phytobiome 1:91–101CrossRefGoogle Scholar
  80. St. Clair DA (2010) Quantitative disease resistance and quantitative resistance loci in breeding. Annu Rev Phytopathol 48:247–268CrossRefPubMedGoogle Scholar
  81. 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 129:495–506CrossRefPubMedGoogle Scholar
  82. Triwitayakorn K, Njiti VN, Iqbal MJ, Yaegashi S, Town C, Lightfoot DA (2005) Genomic analysis of a region encompassing QRfs1 and QRfs2: genes that underlie soybean resistance to sudden death syndrome. Genome 48:125–138CrossRefPubMedGoogle Scholar
  83. Vasconcellos RCC, Oraguzie OB, Soler A, Arkwazee H, Myers JR, Ferreira JJ et al (2017) Meta-QTL for resistance to white mold in common bean. PLoS One 12:e0171685CrossRefPubMedPubMedCentralGoogle Scholar
  84. Veyrieras JB, Goffinet B, Charcosset A (2007) MetaQTL: a package of new computational methods for meta-analysis of QTL mapping experiments. BMC Bioinform 8:49CrossRefGoogle Scholar
  85. Vick CM, Chong SK, Bond JP, Russin JS (2003) Response of soybean sudden death syndrome to subsoil tillage. Plant Dis 87:629–632CrossRefGoogle Scholar
  86. Vick CM, Bond JP, Chong SK, Russin JS (2006) Response of soybean sudden death syndrome to tillage and cultivar. Can J Plant Pathol 28:77–83CrossRefGoogle Scholar
  87. Vosberg SK, Marburger DA, Smith DL, Conley SP (2017) Planting date and fluopyram seed treatment effect on soybean sudden death syndrome and seed yield. Agron J 109:2570–2578CrossRefGoogle Scholar
  88. Wang YJ, Xu J, Deng DX, Ding HD, Bian YL, Yin ZT et al (2016) A comprehensive meta-analysis of plant morphology, yield, stay-green, and virus disease resistance QTL in maize (Zea mays L.). Planta 243:459–471CrossRefPubMedGoogle Scholar
  89. Weems JD, Haudenshield JS, Bond JP, Hartman GL, Ames KA, Bradley CA (2015) Effect of fungicide seed treatments on Fusarium virguliforme infection of soybean and development of sudden death syndrome. Can J Plant Pathol 37:435–447CrossRefGoogle Scholar
  90. Wen ZX, Tan RJ, Yuan JZ, Bales C, Du WY, Zhang SC et al (2014) Genome-wide association mapping of quantitative resistance to sudden death syndrome in soybean. BMC Genom 15:809CrossRefGoogle Scholar
  91. Westphal A, Li CG, Xing LJ, McKay A, Malvick D (2014) Contributions of Fusarium virguliforme and Heterodera glycines to the disease complex of sudden death syndrome of soybean. PLoS One 9:e99529CrossRefPubMedPubMedCentralGoogle Scholar
  92. Xiang Y, Scandiani MM, Herman TK, Hartman GL (2015) Optimizing conditions of a cell-free toxic filtrate stem cutting assay to evaluate soybean genotype responses to Fusarium species that cause sudden death syndrome. Plant Dis 99:502–507CrossRefGoogle Scholar
  93. Xing L, Westphal A (2006) Interaction ofFusarium solanif.sp.glycines andHeterodera glycinesin sudden death syndrome of soybean. Phytopathology 96:763–770CrossRefPubMedGoogle Scholar
  94. Xing L, Westphal A (2009) Effects of crop rotation of soybean with corn on severity of sudden death syndrome and population densities ofHeterodera glycinesin naturally infested soil. Field Crops Res 112:107–117CrossRefGoogle Scholar
  95. Yuan J, Bashir R, Salas G, Sharma H, Srour A, Lightfoot DA (2012) New approaches to selecting resistance or tolerance to SDS and Fusarium root rot. J Plant Genome Sci 1:10–17CrossRefGoogle Scholar
  96. Zhang JP, Singh A, Mueller DS, Singh AK (2015) Genome-wide association and epistasis studies unravel the genetic architecture of sudden death syndrome resistance in soybean. Plant J 84:1124–1136CrossRefPubMedGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Department of Plant, Soil and Microbial SciencesMichigan State UniversityEast LansingUSA
  2. 2.Genetics ProgramMichigan State UniversityEast LansingUSA
  3. 3.Department of AgronomyIowa State UniversityAmesUSA
  4. 4.Department of Plant, Soil and Agricultural SystemsSouthern Illinois UniversityCarbondaleUSA
  5. 5.Department of Crop SciencesUniversity of Illinois at Urbana-ChampaignUrbanaUSA
  6. 6.USDA-Agricultural Research ServiceUrbanaUSA

Personalised recommendations