Skip to main content

Advertisement

Log in

Genome-wide association study of turnip mosaic virus resistance in non-heading Chinese cabbage

  • Original Article
  • Published:
3 Biotech Aims and scope Submit manuscript

Abstract

A genome-wide association study (GWAS) using 83 diverse non-heading Chinese cabbage (NHCC) accessions identified 42,526 high-quality single nucleotide polymorphism markers associated with turnip mosaic virus (TuMV) resistance. Seventeen associated loci were identified, along with the related genes that were differentially expressed between resistant and susceptible varieties, suggesting that they may be candidate genes for TuMV tolerance. Nine mutant genes of Arabidopsis were selected for inoculation with TuMV-GFP (green fluorescence protein) to further confirm the disease resistance of these genes. Quantitative polymerase chain reaction (qPCR) analysis showed that the virus content in the Arabidopsis mutants with the homologous genes of cell wall-associated proteins, pectin methyl-esterase (PME), transcription factors (TFs), resistance gene (R), VAN3/SFC protein and F-box gene were significantly higher than that in the mutants with the homologous genes of methylation and J protein. Our results provide the basis of further study of the potential function of these candidate TuMV resistance genes and demonstrate that the described diverse NHCC can be efficiently used for GWAS of various quantitative traits. Taken together, the findings of this study will be useful to improve TuMV resistance in NHCC breeding and to discover new genes related to TuMV resistance.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

CMV:

Cucumber mosaic virus

CP:

Coat protein

CT:

Cycle threshold

FLA:

Fasciclin-like domains of AGPs

GFP:

Green fluorescence protein

GLM:

General linear model

GWAS:

Genome-wide association study

J protein:

J-domain protein

MLM:

Mixed linear model

NBS-LRR:

Nucleotide binding site-leucine-rich repeats

NHCC:

Non-heading Chinese cabbage

PRP:

Pathogenesis-related protein

qRT-PCR:

Quantitative real-time PCR-Polymerase chain reaction

QTL:

Quantitative trait locus

SNP:

Single-nucleotide polymorphism

S/TK:

Serine-threorine kinase

TF:

Transcription factors

TuMV:

Turnip mosaic virus

References

  • Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19:1655–1664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aranzana MJ, Kim S, Zhao KY et al (2005) Genome-wide association mapping in Arabidopsis identifies previously known flowering time and pathogen resistance genes [J]. PLoS Genet 1(5):e60

    Article  PubMed  PubMed Central  Google Scholar 

  • Beaulieu C (1993) Pathogenic behavior of pectinase-defective erwinia chrysanthemi mutants on different plants. Mol Plant-Mic Inter MPMI (USA) 6:197

    Article  CAS  Google Scholar 

  • Bradbury PJ, Zhang Z, Kroon DE (2007) TASSEL: software for association mapping of complex traits in diverse samples [J]. Bioinformatics 23(19):2633–2635

    Article  CAS  PubMed  Google Scholar 

  • Breseghello F, Sorrells ME (2005) Association mapping of kernal size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics.

  • Brown PJ, Upadyayula N, Mahone GS et al (2011) Distinct genetic architectures for male and female inflorescence traits of maize. PLoS Genet 7(11):e1002383. https://doi.org/10.1371/journal.pgen.1002383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coltell O, Sorlí JV, Asensio EM, Fernández-Carrión R, Barragán R, Ortega-Azorín C, Estruch R, González JI, Salas-Salvadó J, Lamon-Fava S, Lichtenstein AH, Corella D (2019) Association between taste perception and adiposity in overweight or obese older subjects with metabolic syndrome and identification of novel taste-related genes. Am J Clin Nutr 109:1709–1723

    Article  PubMed  Google Scholar 

  • Duplan V, Rivas S (2014) E3 ubiquitin-ligases and their target proteins during the regulation of plant innate immunity. Front Plant Sci 5:42

    Article  PubMed  PubMed Central  Google Scholar 

  • Hardy O, Vekemans X (2002) SPAGeDI: a versatile computer program to analyze spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  Google Scholar 

  • Huang X, Wei X, Sang T, Zhao Q, Feng Q, Zhao Y, Li C, Zhu C, Lu T, Zhang Z (2010) Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 42:961

    Article  CAS  PubMed  Google Scholar 

  • Huang X, Kurata N, Wei X, Wang ZX, Wang A, Zhao Q, Zhao Y, Liu K, Lu H, Li W (2012) A map of rice genome variation reveals the origin of cultivated rice. Nature 490:497–501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khahani B, Tavakol E, Shariati V, Fornara F (2020) Genome wide screening and comparative genome analysis for Meta-QTLs, ortho-MQTLs and candidate genes controlling yield and yield-related traits in rice. BMC Genomics 21:294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kiba A, Galis I, Hojo Y, Ohnishi K, Yoshioka H, Hikichi Y (2014) SEC14 phospholipid transfer protein is involved in lipid signaling-mediated plant immune responses in Nicotiana benthamiana. PLoS One 9(5):e98150. https://doi.org/10.1371/journal.pone.0098150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim B, Masuta C, Matsuura H, Takahashi H, Inukai T (2008) Veinal necrosis induced by turnip mosaic virus infection in Arabidopsis is a form of defense response accompanying HR-like cell death. Mol Plant-Mic Interact MPMI 21:260

    Article  CAS  PubMed  Google Scholar 

  • Le TN, Schumann U, Smith NA, Tiwari S, Au PC, Zhu QH, Taylor JM, Kazan K, Llewellyn DJ, Zhang R (2014) DNA demethylases target promoter transposable elements to positively regulate stress responsive genes in Arabidopsis. Genome Biol 15:1–18

    Article  Google Scholar 

  • Lee J, Bricker TM, Lefevre M, Pinson SR, Oard JH (2010) Proteomic and genetic approaches to identifying defence-related proteins in rice challenged with the fungal pathogen Rhizoctonia solani. Mol Plant Pathol 7:405–416

    Article  Google Scholar 

  • Li S, Min JY, Krug RM, Sen GC (2006) Binding of the influenza A virus NS1 protein to PKR mediates the inhibition of its activation by either PACT or double-stranded RNA. Virology 349:13–21

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Huang Y, Bergelson J, Nordborg M, Borevitz JO (2010) Association mapping of local climate-sensitive quantitative trait loci in Arabidopsis thaliana. Proc Natl Acad Sci USA 107:21199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Peng Z, Yang X, Wang W, Fu J, Wang J, Han Y, Chai Y, Guo T, Yang N (2013) Genome-wide association study dissects the genetic architecture of oil biosynthesis in maize kernels. Nat Genet 45:43–U72

    Article  CAS  PubMed  Google Scholar 

  • Li X, Guo Z, Yan L, Xiang C, Ding X, Hua W, Li X, Huang J, Xiong L (2017) Genetic control of the root system in rice under normal and drought stress conditions by genome-wide association study. PLoS Genet 13:e1006889

    Article  PubMed  PubMed Central  Google Scholar 

  • Li Z, Liu P, Zhang X et al (2020) Genome-wide association studies and QTL mapping uncover the genetic architecture of ear tip-barrenness in maize. Physiol Plant. https://doi.org/10.1111/ppl.13087

    Article  PubMed  Google Scholar 

  • Liu H, Zhang H, YangGJ Y, Yang Y, Wang X, Vindhya B, Basnayake S, Li D, Song F (2008) Functional analysis reveals pleiotropic effects of rice RING-H2 finger protein gene OsBIRF1 on regulation of growth and defense responses against abiotic and biotic stresses. Plant Mol Biol 68:17–30

    Article  CAS  PubMed  Google Scholar 

  • Liu T, Li Y, Zhang C, Qian Y, Wang Z, Hou X (2012) Overexpression of FLOWERING LOCUS C, isolated from non-heading chinese cabbage (Brassica campestris ssp. chinensis Makino), influences fertility in Arabidopsis. Plant Mol Biol Rep 30:1444–1449

    Article  CAS  Google Scholar 

  • Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425

    Article  Google Scholar 

  • Malosetti M, Cg VDL, Vosman B, van Eeuwijk FA (2007) A mixed-model approach to association mapping using pedigree information with an illustration of resistance to Phytophthora infestans in potato. Genetics 175:879–889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Donovan C, Martin MJ, Gattiker A, Gasteiger E, Bairoch A, Apweiler R (2002) High-quality protein knowledge resource: SWISS-PROT and TrEMBL. Brief Bioinform 3:275

    Article  PubMed  Google Scholar 

  • Ohshima K, Tanaka M, Sako N (1996) The complete nucleotide sequence of turnip mosaic virus RNA Japanese strain. Adv Virol 141:1991–1997

    CAS  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29(9):e45. https://doi.org/10.1093/nar/29.9.e45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piisilä M, Keceli MA, Brader G, Jakobson L, Jõesaar I, Sipari N, Kollist H, Palva ET, Kariola T (2015) The F-box protein MAX2 contributes to resistance to bacterial phytopathogens in Arabidopsis thaliana. BMC Plant Biol 15:53

    Article  PubMed  PubMed Central  Google Scholar 

  • Prodhomme C, Vos PG, Paulo MJ et al (2020) Distribution of P1(D1) wart disease resistance in potato germplasm and GWAS identification of haplotype-specific SNP markers. Theor Appl Genet 133(6):1859–1871. https://doi.org/10.1007/s00122-020-03559-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Risch N, Merikangas K (1996) The future of genetic studies of complex human diseases [J]. Science 273(5281):1516–1517

    Article  CAS  PubMed  Google Scholar 

  • Salerno MI, Gianinazzi S, Arnould C, Gianinazzipearson V (2004) Ultrastructural and cell wall modifications during infection of Eucalyptus viminalis roots by a pathogenic Fusarium oxysporum strain. J Gen Plant Pathol 70:145–152

    Article  Google Scholar 

  • Schneider M, Poux S (2012) UniProtKB amid the turmoil of plant proteomics research. Front Plant Sci 3:270

    Article  PubMed  PubMed Central  Google Scholar 

  • Sharma A, Komatsu S (2002) Involvement of a Ca 2+ -Dependent Protein Kinase Component Downstream to the Gibberellin-Binding Phosphoprotein, RuBisCO Activase, in Rice. Biochem Biophys Res Commun 290:690–695

    Article  CAS  PubMed  Google Scholar 

  • Song X, Ge T, Li Y, Hou X (2015) Genome-wide identification of SSR and SNP markers from the non-heading Chinese cabbage for comparative genomic analyses. Bmc Genomics 16:328

    Article  PubMed  PubMed Central  Google Scholar 

  • Sun C, Zhang F, Yan X, Zhang X, Dong Z, Cui D, Chen F (2017) Genome-wide association study for 13 agronomic traits reveals distribution of superior alleles in bread wheat from the Yellow and Huai Valley of China. Plant Biotechnol J 15(8):953–969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turner SD (2014) qqman: an R package for visualizing GWAS results using Q-Q and manhattan plots. bioRxiv:005165

  • Y B, R S, JL D (2004) Plant disease resistance protein signaling: NBS-LRR proteins and their partners. Curr Opin Plant Biol 7:391–399

    Article  Google Scholar 

  • Yang Y, Yuan JS, Ross J, Noel JP, Pichersky E, Chen F (2006) An Arabidopsis thaliana methyltransferase capable of methylating farnesoic acid. Arch Biochem Biophys 448:123–132

    Article  CAS  PubMed  Google Scholar 

  • Zhang ZW, Ersoz E, Lai CQ, Todhunter RJ, Tiwari HK, Gore MA, Bradbury PJ, Yu JM, Arnett DK, Ordovas JM (2010) Mixed linear model approach adapted for genome-wide association studies. Nat Genet 42:355–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thank Jiangsu Agricultural Industry Technology System [JATS (2019) 416] and Natural science foundation of Jiangsu Province (BK20191308) for providing support to carrying out this research work.

Author information

Authors and Affiliations

Authors

Contributions

RZ, CL, XS, FS, YW, XH and CZ conceived the study. RZ, CL, XS and YW completed the experiments. RZ, CL, XS and FS contributed to data analysis and manuscript preparation. XH and CZ participated in the planning of experiments and revising the manuscript. All authors had read and approved the final version of the manuscript.

Corresponding author

Correspondence to Changwei Zhang.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

13205_2020_2344_MOESM1_ESM.docx

Supplementary file1 Fig.S1. The population structure and phylogenetic tree of non-heading Chinese cabbage (NHCC). (A) The population structure; each color represents one population, and K1to K6 are shown using STRUCTURE. The y-axis quantifies thesubgroup membership, and the x-axis shows the accessions.(B) The delta K was used to define the populationstructure of all NHCC accessions.(C) The neighbor-joining phylogenetic treeof the NHCCaccessions for each population were constructed using SNPs. (DOCX 355 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, R., Liu, C., Song, X. et al. Genome-wide association study of turnip mosaic virus resistance in non-heading Chinese cabbage. 3 Biotech 10, 363 (2020). https://doi.org/10.1007/s13205-020-02344-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13205-020-02344-9

Keywords

Navigation