Skip to main content
SpringerLink
Log in

CC-NBS-LRR, a set of VvCRP markers, can distinguish cultivars with ripe rot resistance to Colletotrichum pathogens in grapevine

  • Research Report
  • Published:
Horticulture, Environment, and Biotechnology Aims and scope Submit manuscript

Abstract

Grape ripe rot is a fungal disease, which is almost inextinguishable particularly before and after harvest in most vineyards. The management of this disease largely depends on the breeding of resistant varieties. Thus, the search for resistant varieties should parallel the molecular analysis of the markers associated with disease resistance. Here, we tested the leaf inoculation assay of Colletotrichum acutatum and C. gloeosporioides by inoculating them into 350 grapevine varieties. As a result of the phenotypes common to both species, 119 varieties (34%) were classified as resistant. Consequently, we discovered the locus with nucleotide-binding sites and carboxyterminal leucine-rich repeat regions (NBS-LRR) associated with grape ripe rot resistance through genotyping-by-sequencing and genome-wide association study. Ultimately, we identified the Vitis vinifera Colletotrichum resistance protein (VvCRP) markers from chromosome 3, which belongs to the CC-NBS-LRR type, as disease-resistant proteins. These markers were verified as the melting peak, and their chromatograms of nucleotide sequences were visualized in each single nucleotide polymorphism (SNP) loci. All the SNP markers differentiated successfully the resistant from the susceptible cultivars. Interestingly, we also found that a resistant cultivar named Bailey Alicante A has a heterozygous genotype, substantiating its potential usefulness for crops such as grapevine with many hybrids. Altogether, our results indicate that VvCRP markers can be utilized to distinguish grape ripe rot-resistant cultivars, particularly in crossbreeding populations.

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
Fig. 5

Similar content being viewed by others

Data availability

Information of nucleotide sequencing of genomic DNA sequence of two RPP genes were submitted to National Agricultural Biotechnology Information Center (accession numbers are MN398946 to MN398949, MN385623, MN398943 to MN398949). The datasets generated during the current study are available from the corresponding author on reasonable request.

References

  • Agarwal M, Shrivastava N, Padh H (2008) Advances in molecular marker techniques and their applications in plant sciences. Plant Cell Rep 27:617–631

    Article  PubMed  CAS  Google Scholar 

  • Barba P, Cadle-Davidson, Harriman J, Glauvitz C, Brooks J, Hyma S, Reisch K B (2014) Grapevine powdery mildew resistance and susceptibility loci identified on a high-resolution SNP map. Theor Appl Genet 127:73–84

    Article  PubMed  CAS  Google Scholar 

  • Bittner-Eddy PD, Crute IR, Holub EB, Beynon JL (2000) RPP13 is a simple locus in Arabidopsis thaliana for alleles that specify downy mildew resistance to different avirulence determinants in Peronospora parasitica. Plant J 21:177–188

    Article  PubMed  CAS  Google Scholar 

  • Bouquet A, Danglot Y (1996) Inheritance of seedlessness in grapevine (Vitis vinifera L.). Vitis 35:35–42

    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  PubMed  CAS  Google Scholar 

  • Cabezas JA, Cervera MT, Ruiz-García L, Carreño J, Martínez-Zapater JM (2006) A genetic analysis of seed and berry weight in grapevine. Genome 49:1572–1585

    Article  PubMed  CAS  Google Scholar 

  • Cardoso S, Lau W, Dias JE, Fevereiro P, Maniatis N (2012) A Candidate-gene association study for berry colour and anthocyanin content in Vitis vinifera L. PLoS ONE 7(9):e46021

    Article  PubMed  PubMed Central  Google Scholar 

  • Coleman C, Copetti D, Cipriani G, Hoffmann S, Kozma P, Kovács L, Morgante M, Testolin R, Gaspero GD (2009) The powdery mildew resistance gene REN1 co-segregates with an NBS-LRR gene cluster in two Central Asian grapevines. BMC Genet 10:89

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cradic KW, Wells JE, Allen L, Kruckeberg KE, Singh RJ, Grebe SKG (2004) Substitution of 3′-phosphate cap with a carbon-based blocker reduces the possibility of fluorescence resonance energy transfer probe failure in real-time PCR assays. Clin Chem 50:1080–1082

    Article  PubMed  CAS  Google Scholar 

  • Daykin ME, Milholland RD (1984) Histopathology of Ripe Rot caused by Colletotrichum gloeosporioides on Muscadine Grape. Phytopathol 74:1339–1341

    Article  Google Scholar 

  • Doligez A, Bouquet A, Danglot Y, Lahogue F et al (2002) Genetic mapping of grapevine (Vitis vinifera L.) applied to the detection of QTLs for seedlessness and berry weight. Theor Appl Genet 105:780–795

    Article  PubMed  CAS  Google Scholar 

  • Donald TM, Pellerone F, Adam-Blondon AF, Bouquet A, Thomas MR, Dry IB (2002) Identification of resistance gene analogs linked to a powdery mildew resistance locus in grapevine. Theor Appl Genet 104:610–618

    Article  PubMed  CAS  Google Scholar 

  • Dong QH, Cao X, Yang G, Yu HP, Nicholas KK, Wang C, Fang JG (2010) Discovery and characterization of SNPs in Vitis vinifera and genetic assessment of some grapevine cultivars. Sci Hortic 125:233–238

    Article  CAS  Google Scholar 

  • Ellis J, Dodds P, Pryor T (2000) Structure, function and evolution of plant disease resistance genes. Curr Opin Plant Biol 3:278–284

    Article  PubMed  CAS  Google Scholar 

  • Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6:e19379

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Emanuelli F, Battilana J, Costantini L, Cunff LL, Boursiquot JM, This P, Grando MS (2010) A candidate gene association study on muscat flavor in grapevine (Vitis vinifera L.). BMC Plant Biol 10:241

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Emanuelli F, Lorenzi S, Gizeskowiak L, Catalano V, Stefanini M, Troggio M, Myles S, Martinez-Zapater JM, Zyprian E, Moreira FM, Grando MS (2013) Genetic diversity and population structure assessed by SSR and SNP markers in a large germplasm collection of grape. BMC Plant Biol 13:39

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fodor A, Segura V, Denis M, Neuenschwander S, Fournier-Level A, Chatelet P, Homa FAA, Lacombe T, This P, Cunff LL (2014) Genome-wide prediction methods in highly diverse and heterozygous species: proof-of-concept through simulation in grapevine. PLoS ONE 9:e110436

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hong SK, Kim WG, Yun HK, Choi KJ (2008) Morphological variations, genetic diversity and pathogenicity of Colletotrichum species causing grape ripe rot in Korea. Plant Pathol J 24:269–278

    Article  CAS  Google Scholar 

  • Hu Y, Li Y, Hou F, Wan D, Cheng Y, Han Y, Gao Y, Liu J, Guo Y, Xiao S, Wang Y, Wen YQ (2018) Ectopic expression of Arabidopsis broad-spectrum resistance gene RPW8.2 improves the resistance to powdery mildew in grapevine (Vitis vinifera). Plant Sci 267:20–31

    Article  PubMed  CAS  Google Scholar 

  • Hur YY, Jung SM, Yun HK (2015) Current status and prospects of genomics and bioinformatics in grapes. J Plant Biotechnol 42:298–311

    Article  Google Scholar 

  • Hyma KE, Barba P, Wang M, Londo JP, Acharya CB, Mitchell SE et al (2015) Heterozygous mapping strategy (HetMappS) for high resolution genotyping-by-sequencing markers: a case study in grapevine. PLoS ONE 10:e0134880

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467

    Article  PubMed  CAS  Google Scholar 

  • Jang HA, Oh SK (2017) Development of an efficient genotyping-bysequencing (GBS) library construction method for genomic analysis of grapevine. Korean J Agric Sci 44:495–503

    CAS  Google Scholar 

  • Jang MH, Moon YS, Noh JH, Kim SH, Hong SK, Yun HK (2011) In vitro evaluation system for varietal resistance against ripe rot caused by Colletotrichum acutatum in grapevines. Hort Environ Biotechnol 52:52–57

    Article  Google Scholar 

  • Jang HA, Lee KS, Oo MM, Kwak TS, Yoon HY, Thinn KSZ, Kim MR, Kim DG, Lee JJ, Lim GT, Hur YY, Oh SK (2018) Analysis of varietal difference and genetic diversity of grapevine cultivars through the leaf inoculation of Colletotrichum spp,. J Agric Life Sci 52:49–60

    Article  Google Scholar 

  • Jia RZ, Ming R, Zhu YJ (2013) Genome-wide analysis of nucleotide-binding site (NBS) disease resistance (R) genes in sacred lotus (Nelumbo nucifera Gaertn.) reveals their transition role during early evolution of land plants. Tropical Plant Biol 6:98–116

    Article  CAS  Google Scholar 

  • Kashtan N, Roggensack SE, Rodrigue S, Thompson JW, Biller SJ, Coe A, Ding H, Marttinen P, Malmstrom RR, Stocker R, Follows MJ, Stepanauskas R, Chisholm SW (2014) Single-cell genomics reveals hundreds of coexisting subpopulations in wild Prochlorococcus. Science 344:416–420

    Article  PubMed  CAS  Google Scholar 

  • Kim J, Lim CJ, Lee BW, Choi JP, Oh SK, Ahmad R, Kwon SY, Ahn J, Jur CG (2012) A genome-wide comparison of NB-LRR type of resistance gene analogs (RGA) in the plant kingdom. Mol Cells 33:385–392

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kim JE, Oh SK, Lee JH, Lee BM, Jo SH (2014) Genome-wide SNP calling using next generation sequencing data in tomao. Mol Cells 37:36–42

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kortekamp A, Welter L, Vogt S, Knoll A, Schwander F, Topfer R, Zyprian E (2008) Identification, isolation and characterization of a CC-NBS-LRR candidate disease resistance gene family in grapevine. Mol Breed 22:421–432

    Article  CAS  Google Scholar 

  • Kummuang N, Smith BJ, Diehl SV, Graves CJ (1996) Muscadine grape berry rot diseases in Mississippi: disease identification and incidence. Plant Dis 80:238–243

    Article  Google Scholar 

  • Luo H (2015) The use of evolutionary approaches to understand single cell genomes. Front Microbiol 6:191

    Google Scholar 

  • Mejía N, Gebauer M, Muñoz L, Hewstone N, Muñoz C, Hinrichsen P (2007) Identification of QTLs for seedlessness, berry size, and ripening date in a seedless x seedless table grape progeny. Am J Enol Vitic 58:499–507

    Google Scholar 

  • Meyers BC, Dickerman AW, Michelmore RW, Sivaramakrishnan S, Sobral BW, Young ND (1999) Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J 20:317–332

    Article  PubMed  CAS  Google Scholar 

  • Mohr TJ, Mammarella ND, Hoff T, Woffenden BJ, Jelesko JG, McDowell JM (2010) The Arabidopsis downy mildew resistance gene RPP8 is induced by pathogens and salicylic acid and is regulated by W box cis elements. Mol Plant Microbe Interact 23:1303–1315

    Article  PubMed  CAS  Google Scholar 

  • Montgomery J, Wittwer CT, Palais R, Zhou L (2007) Simultaneous mutation scanning and genotyping by high-resolution DNA melting analysis. Nat Protoc 2:59–66

    Article  PubMed  CAS  Google Scholar 

  • Morgante M, De Paoli E, Radovic S (2007) Transposable elements and the plant pan-genomes. Curr Opin Plant Biol 10:149–155

    Article  PubMed  CAS  Google Scholar 

  • Oo MM, Oh SK (2017) Identification and characterization of new record of grape ripe rot disease caused by Colletotrichum viniferum in Korea. Mycobiology 45:421–425

    Article  PubMed  PubMed Central  Google Scholar 

  • Park GR, Jang HA, Jo SH, Park Y, Oh SK, Nam M (2018) Development of SNP marker set for marker-assisted backcrossing (MABC) in cultivating tomato varieties. Korean J Agric Sci 45:385

    CAS  Google Scholar 

  • Phytozome (2017) The plant genomics resource. Accessed in https://phytozome.jgi.doe.gov/

  • Primmer CR, Borge T, Lindell J, Saetre GP (2002) Single-nucleotide polymorphism characterization in species with limited available sequence information: high nucleotide diversity revealed in the avian genome. Mol Ecol 11:603–612

    Article  PubMed  CAS  Google Scholar 

  • Riaz S, Tenscher AC, Ramming DW, Walker MA (2011) Using a limited mapping strategy to identify major QTLs for resistance to grapevine powdery mildew (Erysiphe necator) and their use in marker-assisted breeding. Theor Appl Genet 122:1059–1073

    Article  PubMed  CAS  Google Scholar 

  • Sarah M, Kaur N, Arora N, Mahal AK (2018) Field reaction and metabolic alterations in grape (Vitis vinifera L.) varieties infested with anthracnose. Sci Hortic-Amst 235:286–293

    Article  CAS  Google Scholar 

  • Smith HM, Smith BP, Morales NB, Moskwa S, Clingeleffer PR, Thomas MR (2018) SNP markers tightly linked to root knot nematode resistance in grapevine (Vitis cinerea) identified by a genotyping-by-sequencing approach followed by Sequenom MassARRAY validation. PLoS ONE 13:e0193121

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sunyaev S, Hanke J, Aydin A, Wirkner U, Zastrow I, Reich J, Bork P (1999) Prediction of nonsynonymous single nucleotide polymorphisms in human disease-associated genes. J Mol Med 77:754–760

    Article  PubMed  CAS  Google Scholar 

  • Takken FL, Albrecht M, Tameling WI (2006) Resistance proteins: molecular switches of plant defence. Curr Opin Plant Biol 9:383–390

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Teh SL, Fresnedo-Ramírez J, Clark MD, Gadoury DM, Sun Q, Cadle-Davidson L, Luby JJ (2017) Genetic dissection of powdery mildew resistance in interspecific half-sib grapevine families using SNP-based maps. Mol Breed 37:1

    Article  PubMed  CAS  Google Scholar 

  • Wang M, Yan J, Zhao J, Song W, Zhang X, Xiao Y, Zheng Y (2012) Genome-wide association study (GWAS) of resistance to head smut in maize. Plant Sci 196:25–131

    Google Scholar 

  • Xiao S, Ellwood S, Calis O, Patrick E, Li T, Coleman M, Turner JG (2001) Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. Science 291:118–120

    Article  PubMed  CAS  Google Scholar 

  • Yang S, Zhang X, Yue JX, Tian D, Chen JQ (2008) Recent duplications dominate NBS-encoding gene expansion in two woody species. Mol Genet Genom 280:187–198

    Article  CAS  Google Scholar 

  • Zhang H, Fan X, Zhang Y, Jiang J, Liu C (2017) Identification of favorable SNP alleles and candidate genes for seedlessness in Vitis vinifera L. using genome-wide association mapping. Euphytica 213:136

    Article  CAS  Google Scholar 

  • Zhong WL, Wang L, Wu X, Zhang J, Chen XF, Zhang W, Dou X, Yu B (2016) Development of unlabeled probe based high-resolution melting analysis for detection of filaggrin gene mutation c.3321delA. J Clin Lab Anal 30:892–896

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhou L, Myers AN, Vandersteen JG, Wang L, Wittwer CT (2004) Closed-tube genotyping with unlabeled oligonucleotide probes and a saturating DNA dye. Clin Chem 50:1328–1335

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Next-Generation BioGreen21 Program (Project No. PJ013141012019), Rural Development Administration (RDA), Republic of Korea.

Author information

Authors and Affiliations

  1. Department of Applied Biology, College of Agriculture and Life Sciences, Chungnam National University, Daejeon, 34134, Republic of Korea

    Hyun A. Jang, May Moe Oo, Dae-Gyu Kim, Ha-Yeon Yoon, Mi-Reu Kim, Kyo-Sang Lee, Khaing Shwe Zin Thinn, Saima Arif, Jia Guo Geng, Jiyoung Min & Sang-Keun Oh

  2. National Institute of Horticultural and Herbal Science, Rural Development Administration, Wanju, 55365, Republic of Korea

    Dong Jun Lim & Youn Young Hur

Authors
  1. Hyun A. Jang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. May Moe Oo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dae-Gyu Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ha-Yeon Yoon
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mi-Reu Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kyo-Sang Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Khaing Shwe Zin Thinn
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Saima Arif
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jia Guo Geng
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jiyoung Min
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Dong Jun Lim
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Youn Young Hur
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Sang-Keun Oh
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

S-KO conceived the project, designed content and organized the manuscript. DJL, and YYH coordinated the project. HAJ performed data generation and/or analysis and managed subprojects. MMO, D-GK, H-YY, M-RK, and K-SL prepared DNA samples and inoculation assays. KSZT, SA, JGG, and JYM inoculation assays. HAJ and S-KO wrote the manuscript.

Corresponding author

Correspondence to Sang-Keun Oh.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Heakeun Yun, Ph.D.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 406 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jang, H.A., Oo, M.M., Kim, DG. et al. CC-NBS-LRR, a set of VvCRP markers, can distinguish cultivars with ripe rot resistance to Colletotrichum pathogens in grapevine. Hortic. Environ. Biotechnol. 61, 915–927 (2020). https://doi.org/10.1007/s13580-020-00290-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13580-020-00290-2

Keywords

Search

Navigation