Skip to main content
SpringerLink
Log in

Genetic architecture of wild soybean (Glycine soja) response to soybean cyst nematode (Heterodera glycines)

  • Original Article
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

The soybean cyst nematode (SCN) is one of the most destructive pathogens of soybean plants worldwide. Host-plant resistance is an environmentally friendly method to mitigate SCN damage. To date, the resistant soybean cultivars harbor limited genetic variation, and some are losing resistance. Thus, a better understanding of the genetic mechanisms of the SCN resistance, as well as developing diverse resistant soybean cultivars, is urgently needed. In this study, a genome-wide association study (GWAS) was conducted using 1032 wild soybean (Glycine soja) accessions with over 42,000 single-nucleotide polymorphisms (SNPs) to understand the genetic architecture of G. soja resistance to SCN race 1. Ten SNPs were significantly associated with the response to race 1. Three SNPs on chromosome 18 were localized within the previously identified quantitative trait loci (QTLs), and two of which were localized within a strong linkage disequilibrium block encompassing a nucleotide-binding (NB)-ARC disease resistance gene (Glyma.18G102600). Genes encoding methyltransferases, the calcium-dependent signaling protein, the leucine-rich repeat kinase family protein, and the NB-ARC disease resistance protein, were identified as promising candidate genes. The identified SNPs and candidate genes can not only shed light on the molecular mechanisms underlying SCN resistance, but also can facilitate soybean improvement employing wild genetic resources.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

SCN:

Soybean cyst nematode

HG:

Heterodera glycines

GWAS:

Genome-wide association study

SNP:

Single-nucleotide polymorphisms

QTL:

Quantitative Trait Loci

NB-ARC:

Nucleotide-binding adaptor shared by Apaf-1, resistance proteins, and CEO-4

MAF:

Minor allele frequency

CWR:

Crop wild relatives

LD:

Linkage disequilibrium

LRR:

Leucine-rich repeat

References

  • Arelli PR, Sleper DA, Yue P, Wilcox JA (2000) Soybean reaction to Races 1 and 2 of Heterodera glycines. Crop Sci 40:824–826

    Article  Google Scholar 

  • Auer PL, Lettre G (2015) Rare variant association studies: considerations, challenges and opportunities. Genome Med 7:16. doi:10.1186/s13073-015-0138-2

    Article  PubMed  PubMed Central  Google Scholar 

  • Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635

    Article  CAS  PubMed  Google Scholar 

  • Cheng YT, Li X (2012) Ubiquitination in NB-LRR-mediated immunity. Curr Opin Plant Biol 15:392–399

    Article  CAS  PubMed  Google Scholar 

  • Concibido VC, Diers BW, Arelli PR (2004) A decade of QTL mapping for cyst nematode resistance in soybean. Crop Sci 44:1121–1131

    Article  CAS  Google Scholar 

  • Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676

    Article  CAS  PubMed  Google Scholar 

  • Cook DE, Bayless AM, Wang K, Guo XL, Song QJ, Jiang JM, Bent AF (2014) Distinct copy number, coding sequence, and locus methylation patterns underlie Rhg1-mediated soybean resistance to soybean cyst nematode. Plant Physiol 165:630–647

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Earl DA, Vonholdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Golden AM, Epps JM, Riggs RD, Duclos LA, Fox JA, Bernard RL (1970) Terminology and identity of infraspecific forms of the soybean cyst nematode (Heterodera glycines). Plant Dis Rep 54:544–546

    Google Scholar 

  • Gomez-Gomez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5:1003–1011

    Article  CAS  PubMed  Google Scholar 

  • 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 46:224–233

    Article  CAS  Google Scholar 

  • Guo XL, Chronis D, De La Torre CM, Smeda J, Wang XH, Mitchum MG (2015) Enhanced resistance to soybean cyst nematode Heterodera glycines in transgenic soybean by silencing putative CLE receptors. Plant Biotechnol J 13:801–810

    Article  CAS  PubMed  Google Scholar 

  • Han YP, Zhao X, Cao GL, Wang Y, Li YH, Liu DY, Teng WL, Zhang ZW, Li DM, Qiu LJ, Zheng HK, Li WB (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 Genomics 16:598

    Article  PubMed  PubMed Central  Google Scholar 

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332

    Article  PubMed  PubMed Central  Google Scholar 

  • Hyten DL, Song QJ, Zhu YL, Choi IY, Nelson RL, Costa JM, Specht JE, Shoemaker RC, Cregan PB (2006) Impacts of genetic bottlenecks on soybean genome diversity. P Natl Acad Sci USA 103:16666–16671

    Article  CAS  Google Scholar 

  • Kandoth PK, Ithal N, Recknor J, Maier T, Nettleton D, Baum TJ, Mitchum MG (2011) The soybean Rhg1 locus for resistance to the soybean cyst nematode Heterodera glycines regulates the expression of a large number of stress- and defense-related genes in degenerating feeding cells. Plant Physiol 155:1960–1975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim M, Diers BW (2013) Fine mapping of the SCN resistance QTL cqSCN-006 and cqSCN-007 from Glycine soja PI 468916. Crop Sci 53:775–785

    Article  CAS  Google Scholar 

  • Kim M, Hyten DL, Niblack TL, Diers BW (2011) Stacking rsistance alleles from wild and domestic soybean sources improves soybean cyst nematode resistance. Crop Sci 51:934–943

    Article  Google Scholar 

  • Klink VP, Overall CC, Alkharouf NW, MacDonald MH, Matthews BF (2007a) Laser capture microdissection (LCM) and comparative microarray expression analysis of syncytial cells isolated from incompatible and compatible soybean (Glycine max) roots infected by the soybean cyst nematode (Heterodera glycines). Planta 226:1389–1409

    Article  CAS  PubMed  Google Scholar 

  • Klink VP, Overall CC, Alkharouf NW, MacDonald MH, Matthews BF (2007b) A time-course comparative microarray analysis of an incompatible and compatible response by Glycine max (soybean) to Heterodera glycines (soybean cyst nematode) infection. Planta 226:1423–1447

    Article  CAS  PubMed  Google Scholar 

  • Lecourieux D, Raneva R, Pugin A (2006) Calcium in plant defence-signalling pathways. New Phytol 171:249–269

    Article  CAS  PubMed  Google Scholar 

  • Li H, Peng ZY, Yang XH, Wang WD, Fu JJ, Wang JH, Han YJ, Chai YC, Guo TT, Yang N, Liu J, Warburton ML, Cheng YB, Hao XM, Zhang P, Zhao JY, Liu YJ, Wang GY, Li JS, Yan JB (2013) Genome-wide association study dissects the genetic architecture of oil biosynthesis in maize kernels. Nat Genet 45:43–50

    Article  CAS  PubMed  Google Scholar 

  • Lipka AE, Tian F, Wang QS, Peiffer J, Li M, Bradbury PJ, Gore MA, Buckler ES, Zhang ZW (2012) GAPIT: genome association and prediction integrated tool. Bioinformatics 28:2397–2399

    Article  CAS  PubMed  Google Scholar 

  • Liu SM, Kandoth PK, Warren SD, Yeckel G, Heinz R, Alden J, Yang CL, Jamai A, El-Mellouki T, Juvale PS, Hill J, Baum TJ, Cianzio S, Whitham SA, Korkin D, Mitchum MG, Meksem K (2012) A soybean cyst nematode resistance gene points to a new mechanism of plant resistance to pathogens. Nature 492:256–260

    CAS  PubMed  Google Scholar 

  • Lorenzo O, Piqueras R, Sanchez-Serrano JJ, Solano R (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15:165–178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manosalva P, Manohar M, von Reuss SH, Chen SY, Koch A, Kaplan F, Choe A, Micikas RJ, Wang XH, Kogel KH, Sternberg PW, Williamson VM, Schroeder FC, Klessig DF (2015) Conserved nematode signalling molecules elicit plant defenses and pathogen resistance. Nat Commun 6

  • Mitchum MG, Wrather JA, Heinz RD, Shannon JG, Danekas G (2007) Variability in distribution and virulence phenotypes of Heterodera glycines in Missouri during 2005. Plant Dis 91:1473–1476

    Article  Google Scholar 

  • Morris GP, Ramu P, Deshpande SP, Hash CT, Shah T, Upadhyaya HD, Riera-Lizarazu O, Brown PJ, Acharya CB, Mitchell SE, Harriman J, Glaubitz JC, Buckler ES, Kresovich S (2013) Population genomic and genome-wide association studies of agroclimatic traits in sorghum. P Natl Acad Sci USA 110:453–458

    Article  CAS  Google Scholar 

  • Niblack TL, Arelli PR, Noel GR, Opperman CH, Ore JH, Schmitt DP, Shannon JG, Tylka GL (2002) A revised classification scheme for genetically diverse populations of Heterodera glycines. J Nematol 34:279–288

    CAS  PubMed  PubMed Central  Google Scholar 

  • Niblack TL, Noel GR, Lambert KN (2003) The Illinois SCN type test: practical application of the HG type classification system. J Nematol 35:355

    Google Scholar 

  • 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 Progress. doi:10.1094/PHP-2008-0118-01-RS

    Google Scholar 

  • Qi XP, Li MW, Xie M, Liu X, Ni M, Shao GH, Song C, Yim AKY, Tao Y, Wong FL, Isobe S, Wong CF, Wong KS, Xu CY, Li CQ, Wang Y, Guan R, Sun FM, Fan GY, Xiao ZX, Zhou F, Phang TH, Liu X, Tong SW, Chan TF, Yiu SM, Tabata S, Wang J, Xu X, Lam HM (2014) Identification of a novel salt tolerance gene in wild soybean by whole-genome sequencing. Nat Commun 5:4340

    CAS  PubMed  PubMed Central  Google Scholar 

  • Replogle A, Wang JY, Paolillo V, Smeda J, Kinoshita A, Durbak A, Tax FE, Wang XH, Sawa S, Mitchum MG (2013) Synergistic interaction of CLAVATA1, CLAVATA2, and RECEPTOR-LIKE PROTEIN KINASE 2 in cyst nematode parasitism of Arabidopsis. Mol Plant Microbe In 26:87–96

    Article  CAS  Google Scholar 

  • Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Holsten T, Gardner J, Wang B, Zhai WX, Zhu LH, Fauquet C, Ronald P (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804–1806

    Article  CAS  PubMed  Google Scholar 

  • Song QJ, Hyten DL, Jia GF, Quigley CV, Fickus EW, Nelson RL, Cregan PB (2013) Development and evaluation of SoySNP50 K, a high-density genotyping array for soybean. PLoS ONE 8:e54985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song Q, Hyten DL, Jia G, Quigley CV, Fickus EW, Nelson RL, Cregan PB (2015) Fingerprinting soybean germplasm and its utility in genomic research. G3 (Bethesda) 5:1999–2006

    Article  Google Scholar 

  • Tian P, Smith SM (2015) Characterization of soybean and its wild relatives host resistance and Asian soybean rust (ASR) pathogen variability for durable resistance. Phytopathology 105:2–10

    Article  Google Scholar 

  • Tylka GL, Marett CC (2014) Distribution of the soybean cyst nematode, Heterodera glycines, in the United States and Canada: 1954 to 2014. Plant Health Brief 15:13

    Google Scholar 

  • Van Ooijen G, Mayr G, Kasiem MMA, Albrecht M, Cornelissen BJC, Takken FLW (2008) Structure-function analysis of the NB-ARC domain of plant disease resistance proteins. J Exp Bot 59:1383–1397

    Article  PubMed  Google Scholar 

  • 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 121:1253–1266

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Wen ZX, Tan RJ, Yuan JZ, Bales C, Du WY, Zhang SC, Chilvers MI, Schmidt C, Song QJ, Cregan PB, Wang DC (2014) Genome-wide association mapping of quantitative resistance to sudden death syndrome in soybean. BMC Genom 15:809

    Article  Google Scholar 

  • Williamson VM, Kumar A (2006) Nematode resistance in plants: the battle underground. Trends Genet 22:396–403

    Article  CAS  PubMed  Google Scholar 

  • Winstead NN, Skotland CB, Sasser JN (1955) Soybean cyst nematodes in North Carolina. Plant Dis Rep 39:911

    Google Scholar 

  • Wrather JA, Koenning SR (2006) Estimates of disease effects on soybean yields in the United States 2003 to 2005. J Nematol 38:173–180

    PubMed  PubMed Central  Google Scholar 

  • Wu XL, 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 118:1093–1105

    Article  CAS  PubMed  Google Scholar 

  • Yue P, Sleper DA, Arelli PR (2000) Genetic analysis of resistance to soybean cyst nematode in PI438489B. Euphytica 116:181–186

    Article  Google Scholar 

  • Yue P, Arelli PR, Sleper DA (2001) Molecular characterization of resistance to Heterodera glycines in soybean PI438489B. Theor Appl Genet 102:921–928

    Article  CAS  Google Scholar 

  • Zhang JP, Singh A, Mueller DS, Singh AK (2015a) Genome-wide association and epistasis studies unravel the genetic architecture of sudden death syndrome resistance in soybean. Plant J 84:1124–1136

    Article  CAS  PubMed  Google Scholar 

  • Zhang JP, Song QJ, Cregan PB, Nelson RL, Wang XZ, Wu JX, Jiang GL (2015b) Genome-wide association study for flowering time, maturity dates and plant height in early maturing soybean (Glycine max) germplasm. BMC Genom 16:217

    Article  CAS  Google Scholar 

  • Zhang H, Mittal N, Leamy L, Barazani O, Song B-H (2016a) Back into the wild—apply untapped genetic diversity of wild relatives for crop improvement. Evolut Appl 10:5–24

    Article  Google Scholar 

  • Zhang HY, Li CY, Davis EL, Wang JS, Griffin JD, Kofsky J, Song BH (2016b) Genome-wide association study of resistance to soybean cyst nematode (Heterodera glycines) HG Type 2.5.7 in wild soybean (Glycine soja). Front. Plant Sci 7:1214

    Google Scholar 

  • Zhou ZK, Jiang Y, Wang Z, Gou ZH, Lyu J, Li WY, Yu YJ, Shu LP, Zhao YJ, Ma YM, Fang C, Shen YT, Liu TF, Li CC, Li Q, Wu M, Wang M, Wu YS, Dong Y, Wan WT, Wang X, Ding ZL, Gao YD, Xiang H, Zhu BG, Lee SH, Wang W, Tian ZX (2015) Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean. Nat Biotechnol 33:408–414

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the two anonymous reviewers for their helpful suggestions. We also thank Dr. Jiaoping Zhang at Iowa State University for his great assistance in performing permutation and Dr. Arelli Prakash for helpful discussion.

Availability of data and material

The data sets analyzed during the current study can be retrieved in the publically accessible database: http://www.soybase.org/.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of North Carolina at Charlotte, Charlotte, NC, 28223, USA

    Hengyou Zhang & Bao-Hua Song

  2. Soybean Genomics and Improvement Laboratory, USDA-ARS, Beltsville, MD, 20705, USA

    Qijian Song

  3. SAS Institute, Cary, NC, 27513, USA

    Joshua D. Griffin

Authors
  1. Hengyou Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qijian Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Joshua D. Griffin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bao-Hua Song
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bao-Hua Song.

Ethics declarations

Funding

This study was funded by the National Institute of General Medical Sciences of the National Institutes of Health, Award Number: R15GM122029; North Carolina Biotechnology Center, Award number: 2014-CFG-8005; Charlotte Research Institute, Award Number: 1603-020; and University of North Carolina at Charlotte.

Conflict of interest

The authors declare that this research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Ethical approval

This article does not contain any studies with animals performed by any of the authors.

Additional information

Communicated by S. Hohmann.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, H., Song, Q., Griffin, J.D. et al. Genetic architecture of wild soybean (Glycine soja) response to soybean cyst nematode (Heterodera glycines). Mol Genet Genomics 292, 1257–1265 (2017). https://doi.org/10.1007/s00438-017-1345-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-017-1345-x

Keywords

Search

Navigation