Theoretical and Applied Genetics

, Volume 129, Issue 12, pp 2295–2311 | Cite as

Advancements in breeding, genetics, and genomics for resistance to three nematode species in soybean

  • Ki-Seung Kim
  • Tri D. Vuong
  • Dan Qiu
  • Robert T. Robbins
  • J. Grover Shannon
  • Zenglu Li
  • Henry T. Nguyen
Review
Part of the following topical collections:
  1. From phenotype to genotype - Celebrating 150 years of Mendelian genetics in plant breeding research

Abstract

Key message

Integration of genetic analysis, molecular biology, and genomic approaches drastically enhanced our understanding of genetic control of nematode resistance and provided effective breeding strategies in soybeans.

Abstract

Three nematode species, including soybean cyst (SCN, Heterodera glycine), root-knot (RKN, Meloidogyne incognita), and reniform (RN, Rotylenchulus reniformis), are the most destructive pests and have spread to soybean growing areas worldwide. Host plant resistance has played an important role in their control. This review focuses on genetic, genomic studies, and breeding efforts over the past two decades to identify and improve host resistance to these three nematode species. Advancements in genetics, genomics, and bioinformatics have improved our understanding of the molecular and genetic mechanisms of nematode resistance and enabled researchers to generate large-scale genomic resources and marker-trait associations. Whole-genome resequencing, genotyping-by-sequencing, genome-wide association studies, and haplotype analyses have been employed to map and dissect genomic locations for nematode resistance. Recently, two major SCN-resistant loci, Rhg1 and Rhg4, were cloned and other novel resistance quantitative trait loci (QTL) have been discovered. Based on these discoveries, gene-specific DNA markers have been developed for both Rhg1 and Rhg4 loci, which were useful for marker-assisted selection. With RKN resistance QTL being mapped, candidate genes responsible for RKN resistance were identified, leading to the development of functional single nucleotide polymorphism markers. So far, three resistances QTL have been genetically mapped for RN resistance. With nematode species overcoming the host plant resistance, continuous efforts in the identification and deployment of new resistance genes are required to support the development of soybean cultivars with multiple and durable resistance to these pests.

Abbreviations

LG

Linkage group

PI

Plant introduction

SCN

Soybean cyst nematode

RKN

Root-knot nematode

RN

Reniform nematode

SNP

Single nucleotide polymorphism

QTL

Quantitative trait loci

References

  1. Abdelmajid K, Ramos L, Hyten D, Kantartzi S, Bond J, Grier R et al (2014) Quantitative trait loci (QTL) that underlie SCN resistance in the soybean [Glycine max (L.) Merr.] ‘PI438489B’ by ‘Hamilton’ recombinant inbred line population. Atlas J Plant Biol 1:29–38CrossRefGoogle Scholar
  2. Anand SC, Rao-Arelli AP (1989) Genetic analyses of soybean genotypes resistant to soybean cyst nematode race 5. Crop Sci 29:1181–1184CrossRefGoogle Scholar
  3. Anderson TR, Welacky TW, Olechowski HT, Ablett G, Ebsary BA (1988) First report of Heterodera glycines on soybeans in Ontario, Canada. Plant Dis 72:453CrossRefGoogle Scholar
  4. Arelli A, Wilcox J, Myers O, Gibson P (1997) Soybean germplasm resistant to races 1 and 2 of Heterodera glycines. Crop Sci 37:1367–1369CrossRefGoogle Scholar
  5. Arelli PR, Young LD, Concibido VC (2009) Inheritance of resistance in soybean PI 567516C to LY1 nematode population infecting cv. Hartwig. Euphytica 165:1–4CrossRefGoogle Scholar
  6. Arriagada O, Mora F, Dellarossa JC, Ferreira MF, Cervigni GD, Schuster I (2012) Bayesian mapping of quantitative trait loci (QTL) controlling soybean cyst nematode resistant. Euphytica 186:907–917CrossRefGoogle Scholar
  7. Bao Y, Vuong T, Meinhardt C, Tiffin P, Denny R et al (2014) Potential of association mapping and genomic selection to explore PI 88788 derived soybean cyst nematode resistance. Plant Genome 7:1–13CrossRefGoogle Scholar
  8. Barabaschia D, Tondellia A, Desiderioa F, Volanteb A, Vaccinoc P, Valèb G et al (2016) Next generation breeding. Plant Sci 242:3–13CrossRefGoogle Scholar
  9. Bassuner R, Clayton K, Lewers KS, Mackenzie S, Shoemaker RC, Vaghchhipawala Z (2001) Modulations in gene expression and mapping of genes associated with cyst nematode infection of soybean. Mol Plant Microbe Interact 14:42–54PubMedCrossRefGoogle Scholar
  10. Bernardo R (2016) Bandwagons I, too, have known. Theor Appl Genet. doi:10.1007/s00122-016-2772-5 Google Scholar
  11. Boerma HR, Hussey RS (1992) Breeding plants for resistance to nematodes. J Nematol 24:242–252PubMedPubMedCentralGoogle Scholar
  12. Borevitz JO, Nordborg M (2003) The impact of genomics on the study of natural variation in Arabidopsis. Plant Physiol 132:718–725PubMedPubMedCentralCrossRefGoogle Scholar
  13. Brucker E, Carlson S, Wright E, Niblack TL, Diers BW (2005) Rhg1 alleles from soybean PI 437654 and PI 88788 respond differentially to isolates of Heterodera glycines in the greenhouse. Theor Appl Genet 111:44–49PubMedCrossRefGoogle Scholar
  14. Caldwell BE, Brim CA, Ross JP (1960) Inheritance of resistance of soybeans to the cyst nematode, Heterodera glycines. Agron J 52:635–636CrossRefGoogle Scholar
  15. Carter TE, Nelson RL, Sneller CH, Cui Z (2004) Genetic diversity in Soybean. In: Boerma HR, Specht JE (eds) Soybeans: improvement, production and uses, 3rd edn. American Society for Agronomy, Madison, pp 303–416Google Scholar
  16. Caviness CE, Riggs RD (1976) Breeding for nematode resistance. In: Hill LD (ed) World soybean research. In: Proceeding of the World Soybean Research Conf., Champaign, IL. 3–8 Aug. 1975, The Interstate Printers & Publishers, Danville, IL, pp 594–601Google Scholar
  17. Chang SJ, Doubler TW, Kilo VY, Abu-Thredeih J, Prabhu R, Freire V, Suttner R, Klein J, Schmidt ME, Gibson PT, Lightfoot DA (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
  18. Chang W, Dong L, Wang Z, Hu H, Han Y, Teng W, Zhang H, Guo M, Li W (2011) QTL underlying resistance to two HG Types of Heterodera glycines found in soybean cultivar ‘L-10’. BMC Genom 12:1CrossRefGoogle Scholar
  19. Chang HX, Lipka AE, Domier LL, Hartman GL (2016) Characterization of disease resistance loci in the USDA Soybean Germplasm Collection using genome-wide association studies. Phytopathology 106:1139–1151PubMedCrossRefGoogle Scholar
  20. Chen Y, Wang D, Arelli P, Ebrahimi M, Nelson RL (2006) Molecular marker diversity of SCN-resistant sources in soybean. Genome 49:938–949PubMedCrossRefGoogle Scholar
  21. Chung WH, Jeong N, Kim J, Lee WK, Lee YG, Lee SH et al (2014) Population structure and domestication revealed by high-depth resequencing of Korean cultivated and wild soybean genomes. DNA Res 21:153–167PubMedCrossRefGoogle Scholar
  22. Colgrove AL, Niblack TL (2008) Correlation of female indices from virulence assays on inbred lines and field populations of Heterodera glycines. J Nematol 40:39PubMedPubMedCentralGoogle Scholar
  23. Concibido VC, Denny RL, Boutin SR, Hautea R, Orf JH, Young ND (1994) DNA marker analysis of loci underlying resistance to soybean cyst nematode (Heterodera glycines Ichinohe). Crop Sci 34:240–246CrossRefGoogle Scholar
  24. Concibido VC, Lange DA, Denny RL, Orf JH, Young ND (1997) Genome mapping of soybean cyst nematode resistance genes in Peking, PI 90763, and PI 88788 using DNA markers. Crop Sci 37:258–264CrossRefGoogle Scholar
  25. Concibido VC, Diers BW, Arelli PR (2004) A decade of QTL mapping for cyst nematode resistance in soybean. Crop Sci 44:1121–1131CrossRefGoogle Scholar
  26. Cook R, Evans K (1987) Resistance and tolerance. In: Brown RH, Kerry BR (eds) Principles and practice of nematode control in crops. Academic Press, Orlando, pp 179–231Google Scholar
  27. Cook DE, Lee TG, Guo X, Melito S et al (2012) Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science 338:1206–1209PubMedCrossRefGoogle Scholar
  28. Cook DE, Bayless AM, Wang K, Guo X, Song Q, Jiang J, Bent AF (2014) Distinct copy number, coding sequence and locus methylation patterns underlie Rhg1-mediated soybean resistance to soybean cyst nematode. Plant Phys 165:630–647CrossRefGoogle Scholar
  29. Cornu M (1879) E´tudes sur le Phylloxera vastatrix. Me´m. Pre´s. Acad Sci Paris 26:164–174Google Scholar
  30. Cregan PB, Jarvik T, Bush AL, Shoemaker RC, Lark KG, Kahler AL, Kaya N, VanToai TT, Lohnes DG, Chung L, Specht JE (1999) An integrated genetic linkage map of the soybean genome. Crop Sci 39:1464–1490CrossRefGoogle Scholar
  31. Davis E, Koenning SR, Burton JW, Barker KR (1996) Greenhouse evaluation of selected soybean germplasm for resistance to North Carolina populations of Heterodera glycines, Rotylenchulus reniformis, and Meloidogyne species. J Nematol 28:590–598PubMedPubMedCentralGoogle Scholar
  32. Dickson SP, Wang K, Krantz I, Hakonarson H, Goldstein DB (2010) Rare variants create synthetic genome-wide associations. PLoS Biol 8:e1000294PubMedPubMedCentralCrossRefGoogle Scholar
  33. Diers BW, Arelli PR (1999) Management of parasite nematodes of soybean through genetic resistance. In: Kauffman HE (ed) Proceeding The 6th world soybean res. Conf., Chicago, IL. 4–7 Aug 1999. Superior Printing, Champaign IL, pp 300–306Google Scholar
  34. Donald P, Young L (2004) Characterization of two soybean cyst nematode populations that reproduce on PI 437654 source of resistance. J Nematol 36:315–316Google Scholar
  35. Faghihi J (2012) Field Crops; Soybean Nematodes. Purdue Extension. Purdue University. E-210-W. https://extension.entm.purdue.edu/publications/E-210.pdf. Accessed 29 April 2016
  36. Ferdous SA, Watanabe S, Suzuki C, Tanaka Y, Kamiya M, Yamanaka N, Harada K (2006) QTL analysis of resistance to soybean cyst nematode race 3 in soybean cultivar Toyomusume. Breed Sci 56:155–163CrossRefGoogle Scholar
  37. Fourie H, Mienie C, Mc Donald AH, De Waele D (2008) Identification and validation of genetic markers associated with Meloidogyne incognita race 2 resistance in soybean, Glycine max (L.) Merr. Nematol 10:651–661CrossRefGoogle Scholar
  38. Gaur HS, Perry RN (1991) The biology and control of the plant parasitic nematode Rotylenchulus reniformis. Agr Zool Rev 4:177–211Google Scholar
  39. Glover KD, Wang D, Arelli PR, Carlson SR, Cianzio SR, Diers BW (2004) Near-isogenic lines confirm a soybean cyst nematode resistance gene from PI 88788 on linkage group. J. Crop Sci 44:936–941CrossRefGoogle Scholar
  40. Goswami BK, Agrawal DK (1978) Interrelationships between species of Fusarium and root-knot nematode, Meloidogyne incognita, in soybean. Nematol Mediterr 6:125–128Google Scholar
  41. 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 111:965–971PubMedCrossRefGoogle Scholar
  42. Guo B, Sleper DA, Nguyen HT, Arelli PR, Shannon JG (2006) Quantitative trait loci underlying resistance to three soybean cyst nematode populations in soybean PI 404198A. Crop Sci 46:224–233CrossRefGoogle Scholar
  43. Ha BK, Bennett JB, Hussey RS, Finnerty SL, Boerma HR (2004) Pedigree analysis of a major QTL conditioning soybean resistance to southern root-knot nematode. Crop Sci 44:758–763CrossRefGoogle Scholar
  44. Ha BK, Robbins RT, Han F, Hussey RS, Soper JF, Boerma HR (2007) SSR mapping and confirmation of soybean QTL from PI 437654 conditioning resistance to reniform nematode. Crop Sci 47:1336–1343CrossRefGoogle Scholar
  45. Han Y, Zhao X, Cao G, Wang Y, Li Y, Liu D, Teng W, Zhang Z et al (2015) Genetic characteristics of soybean resistance to HG type 0 and HG type 1.2.3.5.7 of the cyst nematode analyzed by genome-wide association mapping. BMC Genom 16:598CrossRefGoogle Scholar
  46. Harris DK, Boerma HR, Hussey RS, Finnerty SL (2003) Additional sources of soybean germplasm resistant to two species of root-knot nematode. Crop Sci 43:1848–1851CrossRefGoogle Scholar
  47. Hartman GL, Sinclair JB, Rupe JC (1999) Compendium of soybean diseases. APS Press, St. PaulGoogle Scholar
  48. Hartman GL, West E, Herman T (2011) Crops that feed the world 2. Soybean-worldwide production, use, and constraints caused by pathogens and pests. Food Secur 3:5–17CrossRefGoogle Scholar
  49. Hartwig EE, Epps JM (1973) Registration of ‘Forrest’ soybeans. Crop Sci 13:287CrossRefGoogle Scholar
  50. Harville BG, Green A, Birchfield W (1985) Genetic resistance to reniform nematodes in soybeans. Plant Dis 69:587–589Google Scholar
  51. Heer JA, Knap HT, Mahalingam R, Shipe ER, Arelli PR, Matthews BF (1998) Molecular markers for resistance to Heterodera glycines in advanced soybean germplasm. Mol Breed 4:359–367CrossRefGoogle Scholar
  52. Herald CM, Robinson AF (1990) Survey of current distribution of Rotylenchulus reniformis in the United States. Suppt J Nematol 22:695–699Google Scholar
  53. Herald CM, Thames WH (1982) The reniform nematode, Rotylenchulus reniformis. In: Riggs RD (ed) Nematology in the southern region of the United States, Southern Cooperative Series Bulletin 276. Arkansas Agricultural Experiment Station, Fayetteville, pp 139–143Google Scholar
  54. Hinson K, Hartwig EE (1964) Bragg and Hardee soybeans. Crop Sci 4:664CrossRefGoogle Scholar
  55. Hussey RS, Janssen GJW (2002) Root-knot nematodes: Meloidogyne species. In: Starr JL et al (eds) Plant resistance to parasitic nematodes. CAB Int, New York, pp 43–70CrossRefGoogle Scholar
  56. Hussey RS, Boerma HR, Raymer PL, Luzzi BM (1991) Resistance in maturity groups V-VIII soybean cultivars to soybean cyst and root-knot nematodes. J Nematol 23:576–583PubMedPubMedCentralGoogle Scholar
  57. Hymowitz T, Singh RJ (1987) Taxonomy and speciation. In: Wilcox JR (ed) Soybeans: improvement, production, and uses, 2nd edn. ASA-CSSA-SSSA, Madison, pp 23–45Google Scholar
  58. Hyten DL, Cannon SB, Song Q, Weeks N, Fickus EW et al (2010) High-throughput SNP discovery through deep resequencing of a reduced representation library to anchor and orient scaffolds in the soybean whole genome sequence. BMC Genom 11:38CrossRefGoogle Scholar
  59. Islam S (2015) Molecular characterization of genetic resistance to soybean cyst nematode in soybean line SS97-6946. J Animal Plant Sci 25:243–253Google Scholar
  60. Jiao Y, Vuong TD, Liu Y, Li Z, Noe J, Robbins RT, Joshi T, Xu D, Shannon JG, Nguyen HT (2015) Identification of quantitative trait loci underlying resistance to southern root-knot and reniform nematodes in soybean accession PI 567516C. Mol Breed 35:131PubMedPubMedCentralCrossRefGoogle Scholar
  61. Joshi T, Valliyodan B, Wu JH, Lee SH, Xu D, Nguyen HT (2013) Genomic differences between cultivated soybean, G. max and its wild relative G. soja. BMC Genom 14(1):1CrossRefGoogle Scholar
  62. Kadam S, Vuong TD, Qiu D et al (2016) Genomic-assisted phylogenetic analysis and marker development for next generation soybean cyst nematode resistance breeding. Plant Sci 242:342–350PubMedCrossRefGoogle Scholar
  63. Kandoth PK, Mitchum MG (2013) War of the worms: how plants fight under attacks. Curr Opin Plant Biol 16:457–463PubMedCrossRefGoogle Scholar
  64. Kazi S, Shultz J, Afzal J, Hashmi R, Jasim M, Bond J, Arelli PR, Lightfoot DA (2010) Iso-lines and inbred-lines confirmed loci that underlie resistance from cultivar ‘Hartwig’ to three soybean cyst nematode populations. Theor Appl Genet 120:633–644PubMedCrossRefGoogle Scholar
  65. Keim P, Shoemaker RC, Palmer RG (1989) Restriction fragment length polymorphism diversity in soybean. Theor Appl Genet 77:786–792PubMedCrossRefGoogle Scholar
  66. Khan MR (2005) Hosts and non-hosts of reniform nematode, Rotylenchulus reniformis Linford & Oliveira, 1940–a critical review. Environ and Ecolo 23:124–140Google Scholar
  67. Kim KS, Hill CB, Hartman GL, Mian MA, Diers BW (2008) Discovery of soybean aphid biotypes. Crop Sci 48:923–928CrossRefGoogle Scholar
  68. Kim MY, Lee S, Van K et al (2010) Whole-genome sequencing and intensive analysis of the undomesticated soybean (Glycine soja Sieb. and Zucc.) genome. Proc Natl Acad Sci USA 107:22032–22037PubMedPubMedCentralCrossRefGoogle Scholar
  69. Kim M, Hyten DL, Niblack TL, Diers BW (2011) Stacking resistance alleles from wild and domestic soybean sources improves soybean cyst nematode resistance. Crop Sci 51:934–943CrossRefGoogle Scholar
  70. Kim C, Guo H, Kong W, Chandnani R, Shuang LS, Paterson AH (2016) Application of genotyping by sequencing technology to a variety of crop breeding programs. Plant Sci 242:14–22PubMedCrossRefGoogle Scholar
  71. Kinloch RA (1974) Response of soybean cultivars to nematicidal treatments of soil infested with Meloidogyne incognita. J Nematol 6:7–11PubMedPubMedCentralGoogle Scholar
  72. Kness A, Kleczewski N (2015) Root-knot nematode on soybean. University of Delaware. http://cdn.extension.udel.edu/wp-content/uploads/2015/10/15124841/RKN-on-soybean.pdf. Accessed 05 May 2016
  73. Koenning SR, Wrather JA (2010) Suppression of soybean yield potential in the continental United States from plant diseases from 2006 to 2009. Plant Health Prog. http://www.plantmanagementnetwork.org/pub/php/research/2010/yield/. Accessed 28 Apr 2016
  74. Korte A, Farlow A (2013) The advantages and limitations of trait analysis with GWAS: a review. Plant Methods 9:29–37PubMedPubMedCentralCrossRefGoogle Scholar
  75. Lam HM, Xu X, Liu X et al (2011) Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat Genet 43(4):387CrossRefGoogle Scholar
  76. Lee JD, Kim HK, Robbins RT, Wrather JA, Bond J, Nguyen HT, Shannon JG (2015a) Reaction of soybean cyst nematode resistant plant introductions to root-knot and reniform nematodes. Plant Breed Biotech 3:346–354CrossRefGoogle Scholar
  77. Lee TG, Kumar I, Diers BW, Hudson ME (2015b) Evolution and selection of Rhg1, a copy-number variant nematode-resistance locus. Mol Ecology 24:1774–1791CrossRefGoogle Scholar
  78. Lee TG, Brian WD, Hudson ME (2016) An efficient method for measuring copy number variation applied to improvement of nematode resistance in soybean. Plant J. doi:10.1111/tpj.13240 Google Scholar
  79. Li Z, Jakkula L, Hussey RS, Tamulonis JP, Boerma HR (2001) SSR mapping and confirmation of the QTL from PI 96354 conditioning soybean resistance to southern root-knot nematode. Theor Appl Genet 103:1167–1173CrossRefGoogle Scholar
  80. Lightfoot DA (2015) Two decades of molecular marker-assisted breeding for resistance to soybean sudden death syndrome. Crop Sci 55:1460–1484CrossRefGoogle Scholar
  81. Linford MB, Oliveira JM (1940) Rotylenchulus reniformis, nov. gen., n. sp., a nematode parasite of roots. Proc Helminthol Soc Washington 7:35–42Google Scholar
  82. Liu S, Kandoth PK, Warren SD et al (2012) A soybean cyst nematode resistance gene points to a new mechanism of plant resistance to pathogens. Nature 492:256–260PubMedGoogle Scholar
  83. Lusas EW (2004) Soybean processing and utilization. In: Boerma HR, Specht JE (eds) Soybeans: improvement, production, and uses, 3rd edn. ASA-CSSA-SSSA, Madison, pp 949–1036Google Scholar
  84. Luzzi BM, Boerma HR, Hussey RS (1987) Resistance to three species of root-knot nematode in soybean. Crop Sci 27:258–262CrossRefGoogle Scholar
  85. Luzzi BM, Boerma HR, Hussey RS (1994) A gene for resistance to the southern root-knot nematode in soybean. J Hered 85:484–486Google Scholar
  86. Mahalingam R, Skorupska HT (1995) DNA markers for resistance to Heterodera glycines I. Race 3 in soybean cultivar Peking. Breed Sci 45:435–443Google Scholar
  87. Mansur LM, Carriquiry AL, Rao-Arelli AP (1993) Generation mean analysis of resistance to race 3 of soybean cyst nematode. Crop Sci 33:1249–1253CrossRefGoogle Scholar
  88. Matson AL, Williams LF (1965) Evidence of a fourth gene for resistance to the soybean cyst nematode. Crop Sci 5:477CrossRefGoogle Scholar
  89. Maughan PJ, Saghai Maroof MA, Buss GR (1995) Microsatellite and amplified sequence length polymorphisms in cultivated and wild soybean. Genome 38:715–723PubMedCrossRefGoogle Scholar
  90. McGawley EC, Overstreet C (1999) Reniform nematode. In: Hartman GL, Sinclair J, Rupe JC (eds) Compendium of soybean diseases, 4th edn. APS Press, St. Paul, pp 54–55Google Scholar
  91. 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
  92. Mimee B, Peng H, Popovic V, Yu Q, Duceppe MO, Tétreault MP, Belair G (2015) First report of soybean cyst nematode (Heterodera glycines Ichinohe) on soybean in the Province of Quebec, Canada. Nematol 17:523–530CrossRefGoogle Scholar
  93. Moura RM, Davis EL, Luzzi BM, Boerma HR, Hussey RS (1993) Postinfectional development of Meloidogyne incognita on susceptible and resistant soybean genotypes. Nematropica 23:7–13Google Scholar
  94. Niblack TL (2005) Soybean cyst nematode management reconsidered. Plant Dis 89:1020–1026CrossRefGoogle Scholar
  95. Niblack TL, Arelli PR, Noel GR, Opperman CH, Orf JH, Schmitt DP, Shannon JG, Tylka GL (2002) A revised classification scheme for genetically diverse populations of Heterodera glycines. J Nematol 34:279–288PubMedPubMedCentralGoogle Scholar
  96. Niblack TL, Colgrove AL, Colgrove K, Bond JP (2008) Shift in virulence of soybean cyst nematode is associated with use of resistance from PI 88788. Plant Health Prog. https://www.plantmanagementnetwork.org/pub/php/research/2008/virulence/. Accessed 29 March 2016
  97. O’Neal M, Johnson K (2010) Insect pests of soybean and their management. In: Singh G (ed) The soybean. CABI, Cambridge, pp 300–325Google Scholar
  98. Peng DL, Peng H, Wu DQ, Huang WK, Ye WX, Cui JK (2016) First report of soybean cyst nematode (Heterodera glycines) on soybean from Gansu and Ningxia China. Plant Dis 100:229CrossRefGoogle Scholar
  99. Pham AT, McNally K, Abdel-Haleem H, Boerma RH, Li Z (2013) Fine mapping and identification of candidate genes controlling the resistance to southern root-knot nematode in PI 96354. Theor Appl Genet 126:1825–1838PubMedCrossRefGoogle Scholar
  100. Platt A, Vilhjálmsson BJ, Nordborg M (2010) Conditions under which genome-wide association studies will be positively misleading. Genetics 186:1045–1052PubMedPubMedCentralCrossRefGoogle Scholar
  101. Prabhu RR, Njiti VN, Bell-Johnson B, Johnson JE, Schmidt ME, Klein JH, Lightfoot DA (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
  102. Pratt PW, Wrather JA (1998) Soybean disease loss estimates for the southern United States, 1994 to 1996. Plant Dis 82:114–116CrossRefGoogle Scholar
  103. Qiu BX, Arelli PR, Sleper DA (1999) RFLP markers associated with soybean cyst nematode resistance and seed composition in a ‘Peking’ × ‘Essex’ population. Theor Appl Genet 98:356–364CrossRefGoogle Scholar
  104. Rao-Arelli AP (1994) Inheritance of resistance to Heterodera glycines race 3 in soybean accessions. Plant Dis 78:898–900CrossRefGoogle Scholar
  105. Rao-Arelli AP, Anand SC, Wrather AJ (1992) Soybean resistance to soybean cyst nematode race 3 is conditioned by an additional dominant gene. Crop Sci 32:862–864CrossRefGoogle Scholar
  106. Rebois RV, Johnson WC, Cairns EJ (1968) Resistance in soybeans, Glycine max (L.) Merr. to the reniform nematode. Crop Sci 8:394–395CrossRefGoogle Scholar
  107. Rebois RV, Epps JM, Hartwig EE (1970) Correlation of resistance in soybeans to Heterodera glycines and Rotylenchulus reniformis. Phytopathology 60:695–700CrossRefGoogle Scholar
  108. Riggs RD (2004) History and distribution. Biology and management of soybean cyst nematode, 2nd edn. Walsworth Publishing Company, Marceline, pp 9–39Google Scholar
  109. Riggs RD, Schmitt DP (1988) Complete characterization of the race scheme for Heterodera glycines. J Nematol 20:392–395PubMedPubMedCentralGoogle Scholar
  110. Rincker K, Nelson R, Specht J, Sleper D, Cary T et al (2014) Genetic improvement of soybean in maturity groups II, III, and IV. Crop Sci 54:1419–1432Google Scholar
  111. Robbins RT, Rakes L (1996) Resistance to the reniform nematode in selected soybean cultivars and germplasm lines. J Nematol 28:612–615PubMedPubMedCentralGoogle Scholar
  112. Robbins RT, Rakes L, Elkins CR (1994a) Reniform nematode reproduction and soybean yield of four soybean cultivars in Arkansas. J Nematol 26:656–658PubMedPubMedCentralGoogle Scholar
  113. Robbins RT, Rakes L, Elkins CR (1994b) Reproduction of the reniform nematode on thirty soybean cultivars. J Nematol 26:659–664PubMedPubMedCentralGoogle Scholar
  114. Robinson AF, Inserra RN, Caswell-Chen EP, Vovlas N, Troccoli A (1997) Rotylenchus species: identification, distribution, host ranges, and crop plant resistance. Nematropica 27:127–180Google Scholar
  115. Ross JP, Brim CA (1957) Resistance of soybeans to the soybean cyst nematode as determined by a double-row method. Plant Dis Rept 41:923–924Google Scholar
  116. Ruben E, Jamai A, Afzal J, Njiti VN, Triwitayakorn K, Iqbal MJ, Yaegashi S, Bashir R, Kazi S, Arelli P (2006) Genomic analysis of the rhg1 locus: candidate genes that underlie soybean resistance to the cyst nematode. Mol Genet Genomics 276:503–516PubMedCrossRefGoogle Scholar
  117. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J et al (2010) Genome sequence of the paleopolyploid soybean. Nature 463:178–183PubMedCrossRefGoogle Scholar
  118. Sciumbato GL (1993) Soybean disease loss estimates for the southern United States during 1988–1991. Plant Dis 77:954–956Google Scholar
  119. Shannon JG, Arelli PR, Young LD (2004) Breeding soybeans for resistance and tolerance. In: Schmitt DP, Wrather JA, Riggs RD (eds) Biology and management of soybean cyst nematode, 2nd edn. Schmidt & Associates of Marceline, Mareline, pp 155–180Google Scholar
  120. Shannon JG, Wrather JA, Sleper DA, Robbins RT, Nguyen HT, Anand S (2007a) Registration of Jake soybean. J Crop Reg 1:29–30Google Scholar
  121. Shannon JG, Wrather JA, Sleper DA, Nguyen HT, Anand SC (2007b) Registration of Stoddard soybean. J Crop Reg 1:28–29Google Scholar
  122. Shi Z, Liu S, Noe J, Arelli P, Meksem K, Li Z (2015) SNP identification and marker assay development for high-throughput selection of soybean cyst nematode resistance. BMC Genom 16:314CrossRefGoogle Scholar
  123. Silva MFD, Schuster I, Silva JFVD, Ferreira A, Barros EGD, Moreira MA (2007) Validation of microsatellite markers for assisted selection of soybean resistance to cyst nematode races 3 and 14. Pesquisa Agropecuária Brasileira 42:1143–1150CrossRefGoogle Scholar
  124. Smith AL (1940) Distribution and relation of meadow nematode, Pratylenchus pratensis to Fusarium wilt of cotton in Georgia. Phytopathology 30:710Google Scholar
  125. Song Q, Hyten DL, Jia G, Quigley CV, Fickus EW et al (2013) Development and evaluation of SoySNP50 K, a high-density genotyping array for soybean. PLoS One 8(1):e54985PubMedPubMedCentralCrossRefGoogle Scholar
  126. Specht JE, Diers BW, Nelson RL, Toledo JFF, Torrion JA, Grassini P (2014) In: Smith S, Diers B, Specht J, Carver B (eds) Yield gains in major US field crops. CSSA, Madison, pp 311–356Google Scholar
  127. Stetina SR, Smith JR, Ray JD (2014) Identification of Rotylenchulus reniformis resistant Glycine lines. J Nematol 46:1–7PubMedPubMedCentralGoogle Scholar
  128. Tamulonis TP, Luzzi BM, Hussey RS, Parrott WA, Boerma HR (1997a) DNA markers associated with resistance to Javanese root-knot nematode in soybean. Crop Sci 37:783–788CrossRefGoogle Scholar
  129. Tamulonis JP, Luzzi BM, Hussey RS, Parrott WA, Boerma HR (1997b) RFLP mapping of resistance to southern root-knot nematode in soybean. Crop Sci 37:1903–1909CrossRefGoogle Scholar
  130. Taylor AL, Sasser JN (1978) Biology, identification and control of root-knot nematodes. Department Plant Pathology, North Carolina State University, RaleighGoogle Scholar
  131. Tylka GL, Marett CC (2014) Distribution of the soybean cyst nematode, Heterodera glycines, in the United States and Canada: 1954 to 2014. Plant Health Prog. http://www.soybeanresearchinfo.com/pdf_docs/SCN_Distribution_PHB2014.pdf. Accessed 12 May 2016
  132. Valliyodan B, Qiu Dan, Patil G, Zeng P, Huang J, Dai L, Chen C, Li Y, Joshi T, Song L, Vuong TD, Musket TA, Xu D, Shannon JG, Shifeng C, Liu X, Nguyen HT (2016) Landscape of genomic diversity and trait discovery in soybean. Sci Rep 6:23598PubMedPubMedCentralCrossRefGoogle Scholar
  133. Varshney RK, Graner A, Sorrells ME (2005) Genomics-assisted breeding for crop improvement. Trends Plant Sci 10:621–630PubMedCrossRefGoogle Scholar
  134. Vierling RA, Faghihi J, Ferris VR, Ferris JM (1996) Association of RFLP markers conferring broad-based resistance to the soybean cyst nematode (Heterodera glycines). Theor Appl Genet 92:83–86PubMedCrossRefGoogle Scholar
  135. Vuong TD, Sleper DA, Shannon JG, Nguyen HT (2010) Novel quantitative trait loci for broad-based resistance to soybean cyst nematode (Heterodera glycines Ichinohe) in soybean PI 567516C. Theor Appl Genet 121:1253–1266PubMedCrossRefGoogle Scholar
  136. 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 181:101–113CrossRefGoogle Scholar
  137. Vuong TD, Jiao Y, Shannon JG, Nguyen HT (2013) Nematode Resistance in Soybean. Transl Genom Crop Breed Biotic Stress 11:95–124CrossRefGoogle Scholar
  138. Vuong TD, Sonah H, Meinhardt CG, Deshmukh R, Kadam S, Nelson RL, Shannon JG, Nguyen HT (2015) Genetic architecture of cyst nematode resistance revealed by genome-wide association study in soybean. BMC Genom 16:593–605CrossRefGoogle Scholar
  139. Walters SA, Baker KR (1994) Current distribution of five major Meloidogyne species in the United States. Plant Dis 78:772–774CrossRefGoogle Scholar
  140. Wan J, Vuong T, Jiao Y, Joshi T, Zhang H, Dong Xu, Nguyen HT (2015) Whole-genome gene expression profiling revealed genes and pathways potentially involved in regulating interactions of soybean with cyst nematode (Heterodera glycines Ichinohe). BMC Genom 16:1–48CrossRefGoogle Scholar
  141. Wang D, Diers BW, Arelli PR, Shoemaker RC (2001) Loci underlying resistance to race 3 of soybean cyst nematode in Glycine soja plant introduction 468916. Theor Appl Genet 103:561–566CrossRefGoogle Scholar
  142. Webb DM (1995) Quantitative trait loci associated with cyst nematode resistance and uses thereof. US patent application, US20110083224 A1Google Scholar
  143. Webb DM, Baltazar BM, Rao-Arelli AP, Schupp J, Clayton K, Keim P, Beavis WD (1995) Genetic mapping of soybean cyst nematode race-3 resistance loci in the soybean PI 437654. Theor Appl Genet 91:558–574CrossRefGoogle Scholar
  144. Weisemann JM, Matthews BF, Devine TE (1992) Molecular markers located proximal to the soybean cyst nematode resistance gene, Rhg4. Theor Appl Genet 85:136–138PubMedGoogle Scholar
  145. Westphal A, Xing L (2006) Root-knot nematodes: Diseases of soybean. Purdue Extension. BP-130-W. https://www.extension.purdue.edu/extmedia/BP/BP-130-W.pdf. Accessed 12 May 2016
  146. Williams C, Gilman DF, Fontenot DS, Birchfield W (1981) Inheritance of reaction to the reniform nematode in soybean. Crop Sci 21:93–94CrossRefGoogle Scholar
  147. Winstead NN, Skotland CB, Sasser JN (1955) Soybean cyst nematode in North Carolina. Plant Dis Rep 39:9–11Google Scholar
  148. Winter SMJ, Rajcan I, Shelp BJ (2006) Soybean cyst nematode: challenges and opportunities. Can J Plant Sci 86:25–32CrossRefGoogle Scholar
  149. Winter SMJ, Shelp BJ, Anderson TR, Welacky TW, Rajcan I (2007) QTL associated with horizontal resistance to soybean cyst nematode in Glycine soja PI464925B. Theor Appl Genet 114:461–472PubMedCrossRefGoogle Scholar
  150. Wrather JA, Koenning SR (2006) Estimates of disease effects on soybean yields in the United States 2003 to 2005. J Nematol 38:173–180PubMedPubMedCentralGoogle Scholar
  151. Wrather JA, Koenning SR (2009) Effects of diseases on soybean yields in the United States 1996 to 2007. Plant Health Progress https://www.plantmanagementnetwork.org/pub/php/research/2009/yields/. Accessed 26 April 2016
  152. Wrather JA, Chambers AY, Fox JA, Moore WF, Sciumbato GL (1995) Soybean disease loss estimates for the southern United States, 1974 to 1994. Plant Dis 79:1076–1079Google Scholar
  153. Wrather JA, Shannon G, Balardin R, Carregal L, Escobar R, Gupta GK, Ma Z, Morel W, Ploper D, Tenuta A (2010) Effect of diseases on soybean yield in the top eight producing countries in 2006. Plant Health Progress. https://www.plantmanagementnetwork.org/sub/php/research/2010/loss/loss.pdf. Accessed 26 April 2016
  154. Wu X, Blake S, Sleper DA, Shannon JG, Cregan P, Nguyen HT (2009) QTL, additive and epistatic effects for SCN resistance in PI 437654. Theor Appl Genet 118:1093–1105PubMedCrossRefGoogle Scholar
  155. 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 110:13469–13474PubMedPubMedCentralCrossRefGoogle Scholar
  156. Yue P, Arelli PR, Sleper DA (2001a) Molecular characterization of resistance to Heterodera glycines in soybean PI 438489B. Theor Appl Genet 102:921–928CrossRefGoogle Scholar
  157. Yue P, Sleper DA, Arelli PR (2001b) Mapping resistance to multiple races of Heterodera glycines in soybean PI 89772. Crop Sci 41:1589–1595CrossRefGoogle Scholar
  158. Zhou Z, Jiang Y, Wang Z, Gou Z et al (2015) Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean. Nat Biotechnol 33:408–414PubMedCrossRefGoogle Scholar
  159. Zhu C, Gore M, Buckler ES, Yu J (2008) Status and prospects of association mapping in plants. Plant Genome 1:5–20CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Ki-Seung Kim
    • 1
    • 2
  • Tri D. Vuong
    • 1
  • Dan Qiu
    • 1
  • Robert T. Robbins
    • 3
  • J. Grover Shannon
    • 4
  • Zenglu Li
    • 5
  • Henry T. Nguyen
    • 1
  1. 1.Division of Plant Sciences and National Center for Soybean BiotechnologyUniversity of MissouriColumbiaUSA
  2. 2.KSK’s Current Address: LG Chem-FarmHannong, Ltd.DaejeonKorea
  3. 3.Department of Plant PathologyUniversity of ArkansasFayettevilleUSA
  4. 4.Division of Plant SciencesUniversity of Missouri-Fisher Delta Research CenterPortagevilleUSA
  5. 5.Center for Applied Genetic Technologies and Department of Crop and Soil SciencesUniversity of GeorgiaAthensUSA

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