Theoretical and Applied Genetics

, Volume 133, Issue 1, pp 87–102 | Cite as

Early transcriptional responses to soybean cyst nematode HG Type 0 show genetic differences among resistant and susceptible soybeans

  • Esmaeil Miraeiz
  • Usawadee Chaiprom
  • Alireza Afsharifar
  • Akbar Karegar
  • Jenny M. Drnevich
  • Matthew E. HudsonEmail author
Original Article


Key message

Root transcriptome profiling of three soybean cultivars and a wild relative infected with soybean cyst nematode at migratory phase revealed differential resistance pathway responses between resistant and susceptible genotypes.


The soybean cyst nematode (SCN), Heterodera glycines, is the most serious pathogen of soybean production throughout the world. Using resistant cultivars is the primary management strategy against SCN infestation. To gain insight into the still obscure mechanisms of genetic resistance to nematodes in different soybean genotypes, RNA-Seq profiling of the roots of Glycine max cv. Peking, Fayette, Williams 82, and a wild relative (Glycine soja PI 468916) was performed during SCN infection at the migratory phase. The analysis showed statistically significant changes of expression beginning at eight hours after inoculation in genes associated with defense mechanisms and pathways, such as the phenylpropanoid biosynthesis pathway, plant innate immunity and hormone signaling. Our results indicate the importance of the early plant response to migratory phase nematodes in pathogenicity determination. The transcriptome changes occurring during early SCN infection included a number of genes and pathways specific to the different resistant genotypes. We observed the most extensive resistant transcriptome reaction in PI 468916, where the resistant response was qualitatively different from that of commonly used G. max varieties.



This work was funded by the United Soybean Board (USB). The authors wish to thank Dr. A. Colgrove for preparing the nematode egg mass and C. Fliege for wild soybean seeds and her advice for the germination process. EM would like to thank the Ministry of Science, Research and Technology of Iran for fellowship support.

Author Contribution statement

EM designed and performed the experiments, analyzed the data and wrote the draft manuscript; UC designed and performed the experiments, revised the manuscript and analyzed the data with help from JD; AA and AK revised the manuscript; MH led the project, and revised and reviewed the manuscript.

Compliance with ethical standards

Conflict of interest

The authors of this manuscript declare that they have no conflict of interest.

Supplementary material

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  1. Afzal AJ, Wood AJ, Lightfoot DA (2008) Plant receptor-like serine threonine kinases: roles in signaling and plant defense. Mol Plant-Microb Interact 21:507–517Google Scholar
  2. Ali MA, Abbas A, Kreil DP, Bohlmann H (2013) Overexpression of the transcription factor RAP2.6 leads to enhanced callose deposition in syncytia and enhanced resistance against the beet cyst nematode Heterodera schachtii in Arabidopsis roots. BMC Plant Biol 13:47PubMedPubMedCentralGoogle Scholar
  3. Alkharouf NW, Khan R, Matthews B (2004) Analysis of expressed sequence tags from roots of resistant soybean infected by the soybean cyst nematode. Genome 47:380–388PubMedGoogle Scholar
  4. Alkharouf NW, Klink VP, Chouikha IB, Beard HS, MacDonald MH, Meyer S, Knap HT, Khan R, Matthews BF (2006) Timecourse microarray analyses reveal global changes in gene expression of susceptible Glycine max (soybean) roots during infection by Heterodera glycines (soybean cyst nematode). Planta 224:838–852PubMedGoogle Scholar
  5. Almagro L, Gómez Ros LV, Belchi-Navarro S, Bru R, Ros Barceló A, Pedreño MA (2009) Class III peroxidases in plant defence reactions. J Exp Bot 60:377–390PubMedGoogle Scholar
  6. Andrews S (2010) FastQC: a quality control tool for high throughput sequence data.
  7. Bayless AM, Smith JM, Song J, McMinn PH, Teillet A, August BK, Bent AF (2016) Disease resistance through impairment of α-SNAP–NSF interaction and vesicular trafficking by soybean rhg1. Proc Natl Acad Sci USA 113:E7375–E7382PubMedGoogle Scholar
  8. Bernard RL, Noel GR, Anand SC, Shannon JG (1988) Registration of ‘Fayette’ Soybean. Crop Sci 28:1028–1028Google Scholar
  9. Birkenbihl RP, Diezel C, Somssich IE (2012) Arabidopsis WRKY33 is a key transcriptional regulator of hormonal and metabolic responses towards Botrytis Cinerea infection. Plant Physiol 159:266–285PubMedPubMedCentralGoogle Scholar
  10. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120PubMedPubMedCentralGoogle Scholar
  11. Bonello P, Storer AJ, Gordon TR, Wood DL, Heller W (2003) Systemic effects of Heterobasidion annosum on ferulic acid glucoside and lignin of presymptomatic ponderosa pine phloem, and potential effects on bark-beetle-associated fungi. J Chem Ecol 29:1167–1182PubMedGoogle Scholar
  12. Bybd D Jr, Kirkpatrick T, Barker K (1983) An improved technique for clearing and staining plant tissues for detection of nematodes. J Nematol 15:142PubMedPubMedCentralGoogle Scholar
  13. Cai S, Lashbrook CC (2008) Stamen abscission zone transcriptome profiling reveals new candidates for abscission control: enhanced retention of floral organs in transgenic plants overexpressing Arabidopsis ZINC FINGER PROTEIN2. Plant Physiol 146:1305–1321PubMedPubMedCentralGoogle Scholar
  14. Chin S, Behm C, Mathesius U (2018) Functions of flavonoids in plant-nematode interactions. Plants 7:85–85Google Scholar
  15. Chu S, Wang J, Zhu Y, Liu S, Zhou X, Zhang H, Wang CE, Yang W, Tian Z, Cheng H, Yu D (2017) An R2R3-type MYB transcription factor, GmMYB29, regulates isoflavone biosynthesis in soybean. PLoS Genet 13:1–26Google Scholar
  16. Ciftci-Yilmaz S, Morsy MR, Song L, Coutu A, Krizek BA, Lewis MW, Warren D, Cushman J, Connolly EL, Mittler R (2007) The EAR-motif of the Cys2/His2-type zinc finger protein Zat7 plays a key role in the defense response of Arabidopsis to salinity stress. J Biol Chem 282:9260–9268PubMedGoogle Scholar
  17. Concibido VC, Diers BW, Arelli PR (2004) A decade of QTL mapping for cyst nematode resistance in soybean. Crop Sci 44:1121–1131Google Scholar
  18. Conway JR, Lex A, Gehlenborg N (2017) UpSetR: An R package for the visualization of intersecting sets and their properties. Bioinformatics 33:2938–2940PubMedPubMedCentralGoogle Scholar
  19. Cook DE, Lee TG, Guo X, Melito S, Wang K, Bayless AM, Wang J, Hughes TJ, Willis DK, Clemente TE (2012) Copy number variation of multiple genes at rhg1 mediates nematode resistance in soybean. Science 338:1206–1209PubMedGoogle Scholar
  20. Dao TTH, Linthorst HJM, Verpoorte R (2011) Chalcone synthase and its functions in plant resistance. Phytochem Rev 10:397–412PubMedPubMedCentralGoogle Scholar
  21. Davin LB, Jourdes M, Patten AM, Kim K-W, Vassão DG, Lewis NG (2008) Dissection of lignin macromolecular configuration and assembly: comparison to related biochemical processes in allyl/propenyl phenol and Lignan biosynthesis. Nat Prod Rep 25:1015–1090PubMedGoogle Scholar
  22. Dixon RA, Achnine L, Kota P, Liu CJ, Reddy MS, Wang L (2002) The phenylpropanoid pathway and plant defence—a genomics perspective. Mol Plant Pathol 3:371–390PubMedGoogle Scholar
  23. Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64–W70PubMedPubMedCentralGoogle Scholar
  24. Edens R, Anand S, Bolla R (1995) Enzymes of the phenylpropanoid pathway in soybean infected with Meloidogyne incognita or Heterodera glycines. J Nematol 27:292PubMedPubMedCentralGoogle Scholar
  25. Ewels P, Magnusson M, Lundin S, Käller M (2016) MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics 32:3047–3048PubMedPubMedCentralGoogle Scholar
  26. Gheysen G, Mitchum MG (2008) Molecular insights in the susceptible plant response to nematode infection. Plant Cell Monogr 15:45–82Google Scholar
  27. Hofmann J, Hess PH, Szakasits D, Blöchl A, Wieczorek K, Daxböck-Horvath S, Bohlmann H, van Bel AJ, Grundler FM (2009) Diversity and activity of sugar transporters in nematode-induced root syncytia. J Exp Bot 60:3085–3095PubMedPubMedCentralGoogle Scholar
  28. Hosseini P, Matthews BF (2014) Regulatory interplay between soybean root and soybean cyst nematode during a resistant and susceptible reaction. BMC Plant Biol 14:300PubMedPubMedCentralGoogle Scholar
  29. Ithal N, Recknor J, Nettleton D, Hearne L, Maier T, Baum TJ, Mitchum MG (2007a) Parallel genome-wide expression profiling of host and pathogen during soybean cyst nematode infection of soybean. Mol Plant-Microb Interact 20:293–305Google Scholar
  30. Ithal N, Recknor J, Nettleton D, Maier T, Baum TJ, Mitchum MG (2007b) Developmental transcript profiling of cyst nematode feeding cells in soybean roots. Mol Plant-Microbe Interactions 20:510–525Google Scholar
  31. Jain S, Chittem K, Brueggeman R, Osorno JM, Richards J, Nelson BD Jr (2016) Comparative transcriptome analysis of resistant and susceptible common bean genotypes in response to soybean cyst nematode infection. PLoS ONE 11:e0159338PubMedPubMedCentralGoogle Scholar
  32. Jin J, Hewezi T, Baum TJ (2011) Arabidopsis peroxidase AtPRX53 influences cell elongation and susceptibility to Heterodera schachtii. Plant Signal Behav 6:1778–1786PubMedPubMedCentralGoogle Scholar
  33. Jin J, Tian F, Yang D-C, Meng Y-Q, Kong L, Luo J, Gao G (2016) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucl Acids Res 45(D1), D1040–D1045.PubMedPubMedCentralGoogle Scholar
  34. Kabelka E, Carlson S, Diers B (2005) Localization of two loci that confer resistance to soybean cyst nematode from Glycine soja PI 468916. Crop Sci 45:2473–2481Google Scholar
  35. Kammerhofer N, Radakovic Z, Regis JM, Dobrev P, Vankova R, Grundler FM, Siddique S, Hofmann J, Wieczorek K (2015) Role of stress-related hormones in plant defence during early infection of the cyst nematode Heterodera schachtii in Arabidopsis. New Phytol 207:778–789PubMedPubMedCentralGoogle Scholar
  36. 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 expression of a large number of stress-and defense-related genes in degenerating feeding cells. Plant Physiol 155:1960–1975PubMedPubMedCentralGoogle Scholar
  37. Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucl Acids Res 28:27–30PubMedGoogle Scholar
  38. Kanehisa M, Sato Y, Morishima K (2016) BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol 428:726–731PubMedPubMedCentralGoogle Scholar
  39. Kim M, Diers BW (2013) Fine mapping of the SCN resistance QTL cqSCN-006 and cqSCN-007 from Glycine soja PI 468916. Crop Sci 53:775–785Google Scholar
  40. Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357PubMedPubMedCentralGoogle Scholar
  41. Kinzler AJ, Prokopiak ZA, Vaughan MM, Erhardt PW, Sarver JG, Trendel JA, Zhang Z, Dafoe NJ (2016) Cytochrome P450, CYP93A1, as defense marker in soybean. Biol Plant 60:724–730Google Scholar
  42. 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 226:1389–1409PubMedGoogle Scholar
  43. 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 226:1423–1447PubMedGoogle Scholar
  44. Klink VP, Hosseini P, MacDonald MH, Alkharouf NW, Matthews BF (2009a) Population-specific gene expression in the plant pathogenic nematode Heterodera glycines exists prior to infection and during the onset of a resistant or susceptible reaction in the roots of the Glycine max genotype Peking. BMC Genom 10:111Google Scholar
  45. Klink VP, Hosseini P, Matsye P, Alkharouf NW, Matthews BF (2009b) A gene expression analysis of syncytia laser microdissected from the roots of the Glycine max (soybean) genotype PI 548402 (Peking) undergoing a resistant reaction after infection by Heterodera glycines (soybean cyst nematode). Plant Mol Biol 71:525–567PubMedGoogle Scholar
  46. Klink VP, Hosseini P, Matsye PD, Alkharouf NW, Matthews BF (2010) Syncytium gene expression in Glycine max [PI 88788] roots undergoing a resistant reaction to the parasitic nematode Heterodera glycines. Plant Physiol Biochem 48(2–3):176–193PubMedGoogle Scholar
  47. Klink VP, Hosseini P, Matsye PD, Alkharouf NW, Matthews BF (2011) Differences in gene expression amplitude overlie a conserved transcriptomic program occurring between the rapid and potent localized resistant reaction at the syncytium of the Glycine max genotype Peking (PI 548402) as compared to the prolonged and potent resistant reaction of PI 88788. Plant Mol Biol 75:141–165PubMedGoogle Scholar
  48. 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 10Google Scholar
  49. Korkina L (2007) Phenylpropanoids as naturally occurring antioxidants: from plant defense to human health. Cell Mol Biol 53:15–25PubMedGoogle Scholar
  50. Lee TG, Diers BW, Hudson ME (2016) An efficient method for measuring copy number variation applied to improvement of nematode resistance in soybean. Plant J 88:143–153PubMedGoogle Scholar
  51. Letunic I, Bork P (2017) 20 years of the SMART protein domain annotation resource. Nucl Acids Res 46:D493–D496Google Scholar
  52. Li X, Wang X, Zhang S, Liu D, Duan Y, Dong W (2011) Comparative profiling of the transcriptional response to soybean cyst nematode infection of soybean roots by deep sequencing. Chinese Sci Bull 56:1904Google Scholar
  53. Li X, Wang X, Zhang S, Liu D, Duan Y, Dong W (2012) Identification of soybean microRNAs involved in soybean cyst nematode infection by deep sequencing. PLoS ONE 7:e39650PubMedPubMedCentralGoogle Scholar
  54. Li S, Chen Y, Zhu X, Wang Y, Jung K-H, Chen L, Xuan Y, Duan Y (2018) The transcriptomic changes of Huipizhi Heidou (Glycine max), a nematode-resistant black soybean during Heterodera glycines race 3 infection. J Plant Physiol 220:96–104PubMedGoogle Scholar
  55. Liao Y, Smyth GK, Shi W (2013) featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30:923–930PubMedGoogle Scholar
  56. Liu C-J, Huhman D, Sumner LW, Dixon RA (2003) Regiospecific hydroxylation of isoflavones by cytochrome P450 81E enzymes from Medicago truncatula. Plant J 36:471–484PubMedGoogle Scholar
  57. Liu S, Kandoth PK, Warren SD, Yeckel G, Heinz R, Alden J, Yang C, 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 492:256PubMedGoogle Scholar
  58. Macrae WD, Towers GN (1984) Biological activities of Lignans. Phytochemistry 23:1207–1220Google Scholar
  59. Mahalingam R, Knap H, Lewis S (1998) Inoculation method for studying early responses of Glycine max to Heterodera glycines. J Nematol 30:237PubMedPubMedCentralGoogle Scholar
  60. Matsye PD, Lawrence GW, Youssef RM, Kim K-H, Lawrence KS, Matthews BF, Klink VP (2012) The expression of a naturally occurring, truncated allele of an α-SNAP gene suppresses plant parasitic nematode infection. Plant Mol Biol 80:131–155PubMedGoogle Scholar
  61. Matthews BF, Ibrahim HM, Klink VP (2011) Changes in the expression of genes in soybean roots infected by nematodes. In: Krezhova D (ed) Soybean-genetics and novel techniques for yield enhancement. InTech Open, Rijeka, pp 77–96Google Scholar
  62. Mazarei M, Liu W, Al-Ahmad H, Arelli PR, Pantalone VR, Stewart CN (2011) Gene expression profiling of resistant and susceptible soybean lines infected with soybean cyst nematode. Theor Appl Genet 123:1193PubMedGoogle Scholar
  63. Melton T, Jacobsen B, Noel G (1986) Effects of temperature on development of Heterodera glycines on Glycine max and Phaseolus vulgaris. J Nematol 18:468PubMedPubMedCentralGoogle Scholar
  64. Miedes E, Vanholme R, Boerjan W, Molina A (2014) The role of the secondary cell wall in plant resistance to pathogens. Front Plant Sci 5:358PubMedPubMedCentralGoogle Scholar
  65. Mitchum MG (2016) Soybean resistance to the soybean cyst nematode Heterodera glycines: an update. Phytopathol 106:1444–1450Google Scholar
  66. Mittler R, Kim Y, Song L, Coutu J, Coutu A, Ciftci-Yilmaz S, Lee H, Stevenson B, Zhu J-K (2006) Gain-and loss-of-function mutations in Zat10 enhance the tolerance of plants to abiotic stress. FEBS Lett 580:6537–6542PubMedPubMedCentralGoogle Scholar
  67. Niblack T (2005) Soybean cyst nematode management reconsidered. Plant Dis 89:1020–1026PubMedGoogle Scholar
  68. Niblack T, Arelli P, Noel G, Opperman C, Orf J, Schmitt D, Shannon J, Tylka G (2002) A revised classification scheme for genetically diverse populations of Heterodera glycines. J Nematol 34:279PubMedPubMedCentralGoogle Scholar
  69. Niblack T, Colgrove A, Colgrove K, Bond J (2008) Shift in virulence of soybean cyst nematode is associated with use of resistance from PI 88788. Plant Health Progress. CrossRefGoogle Scholar
  70. Niblack T, Tylka GL, Arelli P, Bond J, Diers B, Donald P, Faghihi J, Gallo K, Heinz RD, Lopez-Nicora H (2009) A standard greenhouse method for assessing soybean cyst nematode resistance in soybean: SCE08 (standardized cyst evaluation 2008). Plant Health Progress 10:33Google Scholar
  71. Reinprecht Y, Perry GE, Pauls KP (2017) A comparison of phenylpropanoid pathway gene families in common bean. Focus on P450 and C4H Genes. In: Santalia Marsolais (ed) The common bean genome. Perez de la Vega, Springer, New York, pp 219–261Google Scholar
  72. Robinson MD, Oshlack A (2010) A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 11:R25PubMedPubMedCentralGoogle Scholar
  73. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140Google Scholar
  74. Ruben E, Jamai A, Afzal J, Njiti V, Triwitayakorn K, Iqbal M, 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 Genom 276:503–516Google Scholar
  75. Sawicki M, Aït Barka E, Clément C, Vaillant-Gaveau N, Jacquard C (2015) Cross-talk between environmental stresses and plant metabolism during reproductive organ abscission. J Exp Bot 66:1707–1719PubMedPubMedCentralGoogle Scholar
  76. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178PubMedGoogle Scholar
  77. Sun F, Liu P, Xu J, Dong H (2010) Mutation in RAP2.6L, a transactivator of the ERF transcription factor family, enhances Arabidopsis resistance to Pseudomonas syringae. Physiol Mol Plant Path 74:295–302Google Scholar
  78. Teillet A, Dybal K, Kerry BR, Miller AJ, Curtis RH, Hedden P (2013) Transcriptional changes of the root-knot nematode Meloidogyne incognita in response to Arabidopsis thaliana root signals. PLoS ONE 8:e61259PubMedPubMedCentralGoogle Scholar
  79. Thoenes P (2004) The role of soybeans in fighting world hunger. Paper presented by the FAO at the VIIth World Soybean Research Conference held in Foz do Iguassu, Brazil, pp 1–5Google Scholar
  80. Van Loon L, Van Strien E (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Path 55:85–97Google Scholar
  81. Wan J, Vuong T, Jiao Y, Joshi T, Zhang H, Xu D, 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 16:148–148Google Scholar
  82. Wang D, Diers B, Arelli P, Shoemaker R, Genetics A (2001) Loci underlying resistance to race 3 of soybean cyst nematode in Glycine soja plant introduction 468916. Theor Appl Genet 103:561–566Google Scholar
  83. Warnes MGR, Bolker B, Bonebakker L, Gentleman R (2016) Package ‘gplots’. Various R programming tools for plotting data. R package version 2.17.0.Google Scholar
  84. Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, New YorkGoogle Scholar
  85. Winstead N, Skotland C, Sasser J (1955) Soybean cyst nematode in North Carolina. Plant Dis Rep 39:9–11Google Scholar
  86. Winter SM, 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 114:461–472PubMedGoogle Scholar
  87. Wu J, Mao X, Cai T, Luo J, Wei L (2006) KOBAS server: a web-based platform for automated annotation and pathway identification. Nucl Acids Res 34:W720–W724PubMedGoogle Scholar
  88. Wubben MJE, Jin J, Baum TJ (2008) Cyst nematode parasitism of Arabidopsis thaliana is inhibited by salicylic acid (SA) and elicits uncoupled SA-independent pathogenesis-related gene expression in roots. Mol Plant-Microbe Interact 21:424–432PubMedGoogle Scholar
  89. Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, Kong L, Gao G, Li C-Y, Wei L (2011) KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucl Acids Res 39:W316–W322PubMedGoogle Scholar
  90. Yang Y, Zhou Y, Chi Y, Fan B, Chen Z (2017) Characterization of Soybean WRKY gene family and identification of soybean WRKY genes that promote resistance to soybean cyst nematode. Sci Rep 7:17804PubMedPubMedCentralGoogle Scholar
  91. Yu N, Diers BW (2017) Fine mapping of the SCN resistance QTL cqSCN-006 and cqSCN-007 from Glycine soja PI 468916. Euphytica 213:54Google Scholar
  92. Yu G-H, Jiang L-L, Ma X-F, Xu Z-S, Liu M-M, Shan S-G, Cheng X-G (2014) A soybean C2H2-type zinc finger gene GmZF1 enhanced cold tolerance in transgenic Arabidopsis. PLoS ONE 9:e109399PubMedPubMedCentralGoogle Scholar
  93. Yu N, Lee TG, Rosa DP, Hudson M, Diers BW (2016) Impact of rhg1 copy number, type, and interaction with Rhg4 on resistance to Heterodera glycines in soybean. Theor Appl Genet 129:2403–2412PubMedGoogle Scholar
  94. Yuan C-P, Li Y-H, Liu Z-X, Guan R-X, Chang R-Z, Qiu L-J (2012) DNA sequence polymorphism of the Rhg4 candidate gene conferring resistance to soybean cyst nematode in Chinese domesticated and wild soybeans. Mol Breed 30:1155–1162PubMedPubMedCentralGoogle Scholar
  95. Yuan C, Wang Y, Zhao H, Zhang L, Wang Y, Liu X, Zhong X, Dong Y (2016) Gene diversity of rhg1 and Rhg4 loci in wild soybeans resistant to soybean cyst nematode race 3. Gene Mol Res 15:gmr7386Google Scholar
  96. Yuan S, Li X, Li R, Wang L, Zhang C, Chen L, Hao Q, Zhang X, Chen H, Shan Z, Yang Z, Chen S, Qiu D, Ke D, Zhou X (2018) Genome-wide identification and classification of Soybean C2H2 Zinc Finger proteins and their expression analysis in legume-rhizobium symbiosis. Fron Microbiol. CrossRefGoogle Scholar
  97. Zhang H, Song B-H (2017) RNA-seq data comparisons of wild soybean genotypes in response to soybean cyst nematode (Heterodera glycines). Genom Data 14:36–39PubMedPubMedCentralGoogle Scholar
  98. Zhang D, Tong J, Xu Z, Wei P, Xu L, Wan Q, Huang Y, He X, Yang J, Shao H (2016) Soybean C2H2-type zinc finger protein GmZFP3 with conserved QALGGH motif negatively regulates drought responses in transgenic Arabidopsis. Front Plant Sci 7:325PubMedPubMedCentralGoogle Scholar
  99. Zhang H, Kjemtrup-Lovelace S, Li C, Luo Y, Chen LP, Song B-H (2017) Comparative RNA-Seq analysis uncovers a complex regulatory network for soybean Cyst nematode resistance in wild Soybean (Glycine soja). Sci Rep 7:9699PubMedPubMedCentralGoogle Scholar
  100. Zhao Y, Chang X, Qi D, Dong L, Wang G, Fan S, Jiang L, Cheng Q, Chen X, Han D, Xu P, Zhang S (2017) A Novel Soybean ERF transcription factor, GmERF113, increases resistance to Phytophthora sojae Infection in Soybean. Front Plant Sci 8:1–16Google Scholar
  101. Zhao D, You Y, Fan H, Zhu X, Wang Y, Duan Y, Xuan Y, Chen L (2018) The role of sugar transporter genes during early infection by root-knot nematodes. Int J Mol Sci 19:302PubMedCentralGoogle Scholar
  102. Zhu L, Guo J, Ma Z, Wang J, Zhou C (2018) Arabidopsis transcription factor MYB102 increases plant susceptibility to aphids by substantial activation of ethylene biosynthesis. Biomolecules. CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Plant Protection, School of AgricultureShiraz UniversityShirazIran
  2. 2.PhD Program in InformaticsUniversity of Illinois at Urbana-ChampaignUrbanaUSA
  3. 3.Plant Virology Research Center, School of AgricultureShiraz UniversityShirazIran
  4. 4.High Performance Biological Computing (HPCBio), Roy J. Carver Biotechnology CenterUniversity of Illinois at Urbana-ChampaignUrbanaUSA
  5. 5.Department of Crop SciencesUniversity of Illinois at Urbana-ChampaignUrbanaUSA

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