Register      Login
Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

RNA-Seq-based identification of potential resistance mechanism against the soybean cyst nematode (Heterodera glycines) HG Type 0 in soybean (Glycine max) cv. Dongnong L-204

Haipeng Jiang A , Fanshan Bu A , Lizheng Tian A , Qiuxia Sun A , Dongfang Bao A , Xue Zhao https://orcid.org/0000-0003-3362-1471 A and Yingpeng Han https://orcid.org/0000-0002-9829-6588 A B
+ Author Affiliations
- Author Affiliations

A Key Laboratory of Soybean Biology in Chinese Ministry of Education (Northeastern Key Laboratory of Soybean Biology and Genetics and Breeding in Chinese Ministry of Agriculture), Northeast Agricultural University, Harbin, Heilongjiang 150030, China.

B Corresponding author. Email: hyp234286@aliyun.com

Crop and Pasture Science 71(6) 539-551 https://doi.org/10.1071/CP20060
Submitted: 21 February 2020  Accepted: 18 May 2020   Published: 2 June 2020

Abstract

Soybean cyst nematode (SCN, Heterodera glycines Ichinohe) is the most important disease affecting yield of soybean (Glycine max (L.) Merr.). In China, among the main physiological races of SCN causing serious economic loss of soybean, HG Type 0 is the most widely distributed. Breeding SCN-resistant varieties is one of the safest and most effective ways to manage SCN. Soybean cv. Dongnong L-204 has a green seed coat and is a resource for resistance to SCN; however, the transcriptional variation and main molecular mechanism of resistance of Dongnong L-204 are not clear. We obtained 66.42 Gb of raw reads by using Illumina HiSeq high-throughput sequencing of Dongnong L-204. Transcriptional changes at Days 3, 7 and 10 after HG Type 0 stress are described. In total, 11 279 differentially expressed genes were responsive to HG Type 0 stress, including 6407 SCN-induced and 4872 SCN-suppressed genes. Gene Ontology analysis emphasised the important roles of the terms metabolic process, single-organism process, catalytic activity and binding under HG Type 0 stress. Among them, the terms related to extracellular matrix, extracellular region part, membrane-enclosed lumen, protein-binding transcription factor activity, and symplast and cell junction existed only in pairwise comparisons Day 7 vs Day 0 and Day 10 vs Day 0. KEGG enrichment analysis showed that metabolic pathway played an important role in the stress response to HG Type 0. Cellular processes, metabolism and organismal systems and other pathway-related genes increased significantly after 7 days. Transcription factor analysis showed that transcription factors such as MYB, AP2-EREBP, bHLH, WRKY and NAC may be involved in the anti-HG Type 0 response of Dongnong L-204. At the same time, few transient inducible transcription factors were found and more transient inhibited transcription factors in Dongnong L-204 in the early stage of HG Type 0 syncytial establishment. RT-qPCR was used to analyse expression of 10 genes closely related to the HG Type 0 stress response. The expression of GmWRKYX1 was >60 times higher at Day 10 after HG Type 0 stress than at Day 0. The WRKY transcription-factor family may play an important role in the resistance of Dongnong L-204 to HG Type 0 stress.

Additional keywords: DEGs, race 3, RNA sequencing.


References

Alkharouf NW, Klink VP, Chouikha IB, Beard HS, Macdonald MH, Meyer S, 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, 838–852.
Timecourse microarray analyses reveal global changes in gene expression of susceptible Glycine max (soybean) roots during infection by Heterodera glycines (soybean cyst nematode).Crossref | GoogleScholarGoogle Scholar | 16575592PubMed |

Arelli A, Wilcox J, Myers O, Gibson P (1997) Soybean germplasm resistant to races 1 and 2 of Heterodera glycines. Crop Science 37, 1367–1369.
Soybean germplasm resistant to races 1 and 2 of Heterodera glycines.Crossref | GoogleScholarGoogle Scholar |

Arelli PR, Young LD, Concibido VC (2009) Inheritance of resistance in soybean PI 567516C to LY1 nematode population infecting cv. Hartwig. Euphytica 165, 1–4.
Inheritance of resistance in soybean PI 567516C to LY1 nematode population infecting cv. Hartwig.Crossref | GoogleScholarGoogle Scholar |

Barakat A, DiLoreto DS, Zhang Y, Smith C, Baier K, Powell WA, Wheeler N, Sederoff R, Carlson JE (2009) Comparison of the transcriptomes of American chestnut (Castanea dentata) and Chinese chestnut (Castanea mollissima) in response to the chestnut blight infection. BMC Plant Biology 9, 51
Comparison of the transcriptomes of American chestnut (Castanea dentata) and Chinese chestnut (Castanea mollissima) in response to the chestnut blight infection.Crossref | GoogleScholarGoogle Scholar | 19426529PubMed |

Bencke-Malato M, Cabreira C, Wiebke-Strohm B, Bücker-Neto L, Mancini E, Osorio MB, Homrich MS, Turchetto-Zolet AC, Carvalho MCD, Stolf R, Weber RLM, Westergaard G, Castagnaro AP, Abdelnoor RV, Marcelino-Guimarães FC, Margis-Pinheiro M, Bodanese-Zanettini MH (2014) Genome-wide annotation of the soybean WRKY family and functional characterization of genes involved in response to Phakopsora pachyrhizi infection. BMC Plant Biology 14, 236
Genome-wide annotation of the soybean WRKY family and functional characterization of genes involved in response to Phakopsora pachyrhizi infection.Crossref | GoogleScholarGoogle Scholar | 25201117PubMed |

Bhattacharyya D, Sinha R, Hazra S, Datta R, Chattopadhyay S (2013) De novo transcriptome analysis using 454 pyrosequencing of the Himalayan Mayapple, Podophyllum hexandrum. BMC Genomics 14, 748
De novo transcriptome analysis using 454 pyrosequencing of the Himalayan Mayapple, Podophyllum hexandrum.Crossref | GoogleScholarGoogle Scholar | 24182234PubMed |

Chen S, Liu X (2005) Control of the soybean cyst nematode by the fungi Hirsutella rhossiliensis and Hirsutella minnesotensis in greenhouse studies. Biological Control 32, 208–219.
Control of the soybean cyst nematode by the fungi Hirsutella rhossiliensis and Hirsutella minnesotensis in greenhouse studies.Crossref | GoogleScholarGoogle Scholar |

Chen Y, Wang D, Arelli P, Ebrahimi M, Nelson RL (2006) Molecular marker diversity of SCN-resistant sources in soybean. Genome 49, 938–949.
Molecular marker diversity of SCN-resistant sources in soybean.Crossref | GoogleScholarGoogle Scholar | 17036069PubMed |

Cook DE, Lee TG, Guo X, Melito S, Wang K, Bayless AM, Wang JP, Hughes TJ, Willis DK, Clemente TE, Diers BW, Jiang JM, Hudson ME, Bent AE (2012) Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science 338, 1206–1209.
Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean.Crossref | GoogleScholarGoogle Scholar | 23065905PubMed |

Dassanayake M, Haas JS, Bohnert HJ, Cheeseman JM (2009) Shedding light on an extremophile lifestyle through transcriptomics. New Phytologist 183, 764–775.
Shedding light on an extremophile lifestyle through transcriptomics.Crossref | GoogleScholarGoogle Scholar | 19549131PubMed |

Denoeud F, Aury JM, Da Silva C, Noel B, Rogier O, Delledonne M, Morgante M, Valle G, Wincker P, Scarpelli C, Jaillon O, Artiguenave F (2008) Annotating genomes with massive-scale RNA sequencing. Genome Biology 9, r175
Annotating genomes with massive-scale RNA sequencing.Crossref | GoogleScholarGoogle Scholar | 19087247PubMed |

Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends in Plant Science 5, 199–206.
The WRKY superfamily of plant transcription factors.Crossref | GoogleScholarGoogle Scholar | 10785665PubMed |

Gabriel DW, Rolfe BG (1990) Working models of specific recognition in plant–microbe interactions. Annual Review of Phytopathology 28, 365–391.
Working models of specific recognition in plant–microbe interactions.Crossref | GoogleScholarGoogle Scholar |

Glazebrook J (2001) Genes controlling expression of defense responses in Arabidopsis—2001 status. Current Opinion in Plant Biology 4, 301–308.
Genes controlling expression of defense responses in Arabidopsis—2001 status.Crossref | GoogleScholarGoogle Scholar | 11418339PubMed |

Golldack D, Lüking I, Yang O (2011) Plant tolerance to drought and salinity: stress regulating transcription factors and their functional significance in the cellular transcriptional network. Plant Cell Reports 30, 1383–1391.
Plant tolerance to drought and salinity: stress regulating transcription factors and their functional significance in the cellular transcriptional network.Crossref | GoogleScholarGoogle Scholar | 21476089PubMed |

Grabau ZJ (2013) Management strategies for control of soybean cyst nematode and their effect on nematode community. MSc Thesis, University of Minnesota, Twin Cities, MN, USA.

Han Y, Tan Y, Hu H, Chang W, Teng W (2017) Quantitative trait loci with additive and epistatic effects underlying resistance to two hg types of soybean cyst nematode. Plant Breeding 136, 720–727.
Quantitative trait loci with additive and epistatic effects underlying resistance to two hg types of soybean cyst nematode.Crossref | GoogleScholarGoogle Scholar |

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. Molecular Plant-Microbe Interactions 20, 293–305.
Parallel genome-wide expression profiling of host and pathogen during soybean cyst nematode infection of soybean.Crossref | GoogleScholarGoogle Scholar | 17378432PubMed |

Ithal N, Recknor J, Nettleton D, Maier T, Baum TJ, Mitchum MG (2007b) Developmental transcript profiling of cyst nematode feeding cells in soybean roots. Molecular Plant-Microbe Interactions 20, 510–525.
Developmental transcript profiling of cyst nematode feeding cells in soybean roots.Crossref | GoogleScholarGoogle Scholar | 17506329PubMed |

Jain S, Chittem K, Brueggeman R, Osorno JM, Richards J, Nelson BD (2016) Comparative transcriptome analysis of resistant and susceptible common bean genotypes in response to soybean cyst nematode infection. PLoS One 11, e0159338
Comparative transcriptome analysis of resistant and susceptible common bean genotypes in response to soybean cyst nematode infection.Crossref | GoogleScholarGoogle Scholar | 27441552PubMed |

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. Molecular Breeding 35, 131
Identification of quantitative trait loci underlying resistance to southern root-knot and reniform nematodes in soybean accession PI 567516C.Crossref | GoogleScholarGoogle Scholar | 26028986PubMed |

Khan R, Alkharouf N, Beard HS, MacDonald M, Chouikha I, Meyer S, Grefenstette J, Knap H, Matthews B (2004) Microarray analysis of gene expression in soybean roots susceptible to the soybean cyst nematode two days post invasion. Journal of Nematology 36, 241–248.

Klink VP, Overall CC, Alkharouf NW, MacDonald MH, Matthews BF (2007) 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.
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).Crossref | GoogleScholarGoogle Scholar | 17668236PubMed |

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 11, 5–11.
Suppression of soybean yield potential in the continental united states by plant diseases from 2006 to 2009.Crossref | GoogleScholarGoogle Scholar |

Li Y, Chang RZ (1991) Studies on resistance of soybean germplasm resources to race 4 of soybean cyst nematode. Scientia Agricultura Sinica 5, 110–120.

Li XY, Wang X, Zhang SP, Liu DW, Duan YX, Dong W (2011a) Comparative profiling of the transcriptional response to soybean cyst nematode infection of soybean roots by deep sequencing. Science Bulletin 56, 1904–1911.
Comparative profiling of the transcriptional response to soybean cyst nematode infection of soybean roots by deep sequencing.Crossref | GoogleScholarGoogle Scholar |

Li YH, Qi XT, Chang R (2011b) Evaluation and utilization of soybean germplasm for resistance to cyst nematode in China. In ‘Soybean – molecular aspects of breeding’. pp. 373–396. (IntechOpen: London) 10.5772/14379

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, 256–260.
A soybean cyst nematode resistance gene points to a new mechanism of plant resistance to pathogens.Crossref | GoogleScholarGoogle Scholar | 23235880PubMed |

Maher CA, Kumar-Sinha C, Cao X, Kalyana-Sundaram S, Han B, Jing XJ, Sam L, Barrette T, Palanisamy N, Chinnaiyan AM (2009) Transcriptome sequencing to detect gene fusions in cancer. Nature 458, 97–101.
Transcriptome sequencing to detect gene fusions in cancer.Crossref | GoogleScholarGoogle Scholar | 19136943PubMed |

Moghadam E, Rouhani H, Rastgar M (2009) Biological control of sugar beet cyst forming nematode with trichoderma under in vitro and green house condition. Journal of Science & Technology of Agriculture & Natural Resources 13, 301–312.

Mourtzinis S, Marburger D, Gaska J, Diallo T, Lauer J, Conley S (2017) Corn and soybean yield response to tillage, rotation, and nematicide seed treatment. Crop Science 57, 1–9.

Puthoff DP, Ehrenfried ML, Vinyard BT, Tucker ML (2007) GeneChip profiling of transcriptional responses to soybean cyst nematode, Heterodera glycines, colonization of soybean roots. Journal of Experimental Botany 58, 3407–3418.
GeneChip profiling of transcriptional responses to soybean cyst nematode, Heterodera glycines, colonization of soybean roots.Crossref | GoogleScholarGoogle Scholar | 17977850PubMed |

Schwinn KA (2006) Small family of MYB-regulatory genes controls floral pigmentation intensity and patterning in the genus Antirrhinum. The Plant Cell 18, 831–851.
Small family of MYB-regulatory genes controls floral pigmentation intensity and patterning in the genus Antirrhinum.Crossref | GoogleScholarGoogle Scholar |

Singh M, Khan Z, Kumar K, Dutta M, Pathania A, Dahiya OP, Kumar J (2012) Sources of resistance to Fusarium wilt and root-knot nematode in indigenous chickpea germplasm. Plant Genetic Resources 10, 258–260.
Sources of resistance to Fusarium wilt and root-knot nematode in indigenous chickpea germplasm.Crossref | GoogleScholarGoogle Scholar |

Taketo U, Shunpei S, Chikara M (2007) Comparative serial analysis of gene expression of transcript profiles of tomato roots infected with cyst nematode. Plant Molecular Biology 63, 185–194.

Tian H, Riggs RD, Crippen DL (2000) Control of soybean cyst nematode by chitinolytic bacteria with chitin substrate. Journal of Nematology 32, 370

Tian F, Wang Y, Zhu X, Chen L, Duan Y (2014) Effect of Sinorhizobium fredii strain sneb183 on the biological control of soybean cyst nematode in soybean. Journal of Basic Microbiology 54, 1258–1263.
Effect of Sinorhizobium fredii strain sneb183 on the biological control of soybean cyst nematode in soybean.Crossref | GoogleScholarGoogle Scholar | 24912826PubMed |

Ülker B, Somssich IE (2004) WRKY transcription factors: from DNA binding towards biological function. Current Opinion in Plant Biology 7, 491–498.
WRKY transcription factors: from DNA binding towards biological function.Crossref | GoogleScholarGoogle Scholar | 15337090PubMed |

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. Theoretical and Applied Genetics 121, 1253–1266.
Novel quantitative trait loci for broad-based resistance to soybean cyst nematode (Heterodera glycines Ichinohe) in soybean PI 567516C.Crossref | GoogleScholarGoogle Scholar | 20559815PubMed |

Walters D, Newton A, Lyon G (2005) Induced resistance: helping plants to help themselves. Biologist 52, 28–33.

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 Genomics 16, 148
Whole-genome gene expression profiling revealed genes and pathways potentially involved in regulating interactions of soybean with cyst nematode (Heterodera glycines Ichinohe).Crossref | GoogleScholarGoogle Scholar | 25880563PubMed |

Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB (2008) Alternative isoform regulation in human tissue transcriptomes. Nature 456, 470–476.
Alternative isoform regulation in human tissue transcriptomes.Crossref | GoogleScholarGoogle Scholar | 18978772PubMed |

Zhang H, Kjemtrup-Lovelace S, Li C, Luo Y, Chen L, Song B (2017) Comparative RNA-seq analysis uncovers a complex regulatory network for soybean cyst nematode resistance in wild soybean (Glycine soja). Scientific Reports 7, 9699
Comparative RNA-seq analysis uncovers a complex regulatory network for soybean cyst nematode resistance in wild soybean (Glycine soja).Crossref | GoogleScholarGoogle Scholar | 28852059PubMed |

Zhen-Hua W, Li-Bo S, Hai-Yan WU, Jing L, Xiu-Xia LI (2009) Distribution and developmental process of Heterodera glycines in soybean root. Scientia Agricultura Sinica 42, 3147–3153.

Zhou Z, Jiang Y, Wang Z, Gou Z, Lyu J, Li W, Yu Y, Shu L, Zhao Y, Ma Y, Fang C, Shen Y, Liu T, Li C, Li Q, Wu M, Wang M, Wu Y, Dong Y, Wan W, Wang X, Ding Z, Gao Y, Xiang H, Zhu B, Lee SH, Wang W, Tian Z (2015) Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean. Nature Biotechnology 33, 408–414.
Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean.Crossref | GoogleScholarGoogle Scholar | 25643055PubMed |

Zhou Y, Wang Y, Zhu X, Liu R, Xiang P, Chen J, Liu X, Duan Y (2017) Management of the soybean cyst nematode Heterodera glycines with combinations of different rhizobacterial strains on soybean. PLoSONE 12, e0182654